{"paper_id":"18c6a3bd-48b2-4ef9-9d13-34e0f1e086ad","body_text":"248\nTVUS soft markers in clinically significant superficial endometriosis:  \nan ultrasonographic, clinical, and laparoscopic correlation\nA. Sofia Sanchez-Gomez1,2,a*, Victor M. Garcia-Gallegos1,3, Manuel A. Lopez-de La T orre1, and  \nMarco A. Lopez-Zepeda1\n1Clinica de Excelencia en Endometriosis, Zapopan; 2Departamento de Imagenologia Diagnostica y T erapeutica, Grupo RIO Centro Integral de \nDiagnostico Medico, Guadalajara; 3Departamento de Imagenologia Diagnostica y T erapeutica, Hospital San Javier, Guadalajara. Jalisco, Mexico\nORCID: a0000-0001-7054-6250\nFULL RESEARCH ARTICLE\n*Corresponding author:  \nA. Sofia Sanchez-Gomez  \nE-mail: dra.anasofiasanchez@gmail.com \n2696-8444 / © 2023 Federación Mexicana de Radiología e Imagen, A.C. Published by Permanyer. This is an open access article under the \nCC BY-NC-ND (https://creativecommons.org/licenses/by-nc-nd/4.0/ ).\nAvailable online: 29-12-2023\nJ Mex Fed Radiol Imaging. 2023;2(4):248- 258\nwww.JMeXFRI.com\nFEDERACIÓN MEXICANADE RADIOLOGÍA E IMAGEN, A.C\nJournal of the Mexican Federation of Radiology and Imaging\nOfficial Journal of the \nJournal of the Mexican Federation \nof Radiology and Imaging\nReceived for publication: 10-04-2023\nAccepted for publication: 20-07 -2023\nDOI: 10.24875/JMEXFRI.M23000063\nABSTRACT \nIntroduction: Ultrasonographic soft markers can be useful diagnostic findings in endometriosis. We evaluated women with \nsuperficial endometriosis with only soft markers on basal transvaginal ultrasound (TVUS) with bowel preparation and their \nrelationship with chronic pelvic pain and laparoscopy findings. Materials and methods: This retrospective cohort study \nincluded patients with clinical suspicion of endometriosis. They had soft markers on basal TVUS with bowel preparation and \nunderwent laparoscopy for the first time. Symptoms, such as dysmenorrhea, dyschezia, deep dyspareunia, and dysuria, were \nquantified with a visual analog scale. The ultrasonographic soft markers were ovarian tenderness, adhesions, obliteration of \nthe cul-de-sac (CDS), and obliteration of the vesico-uterine pouch (VUP). Laparoscopic findings were adhesions and \nsuperficial endometriotic lesions. Results: A total of 25 women with superficial endometriosis with only soft markers on basal \nTVUS with bowel preparation and who underwent therapeutic laparoscopy were included. The mean age was 32.28 ± 5.67 \nyears. The type and intensity (mean ± SD) of chronic pelvic pain were severe dysmenorrhea (7 .60 ± 3.08), moderate \ndyspareunia (4.84 ± 3.51), and mild dyschezia and dysuria (3.44 ± 3.89 and 2.12 ± 2.92, respectively). All had at least one \npositive ultrasonographic soft marker. Most patients had moderate-to-severe dysmenorrhea and only soft markers on ultrasound \nexaminations. Patients with superficial endometriotic lesions, regardless of size or extension, found at laparoscopy reported \nsevere dysmenorrhea. Conclusion: TVUS soft markers were associated with clinically significant superficial endometriosis. \nTVUS soft markers are not usually reported during routine examination. They may improve the diagnostic yield of superficial \nendometriosis.\nKeywords: Endometriosis. Superficial endometriosis. Ultrasonographic soft markers. T ransvaginal ultrasound. Chronic pelvic \npain. Laparoscopic pelvic surgery.\nINTRODUCTION\nEndometriosis is endometrial-like tissue found out -\nside the uterine cavity. It is a gynecologic disease  \nthat represents one of the greatest gynecologic \nchallenges in diagnosis and treatment today 1. There \nare three types of endometriosis: peritoneal, ovarian, \nand deep infiltrative endometriosis (DIE) 2. Peritoneal \nendometriosis, also called superficial endometriosis, is \nthe most common type. It occurs in up to 80% of \nwomen with a confirmed diagnosis 3 and is associated \nwith infertility and chronic pelvic pain, such as severe \ndysmenorrhea and dyspareunia 4. Early diagnosis of \nendometriosis can lead to more effective treatment  \n\nA.S. Sanchez-Gomez et al. TVUS soft markers in superficial endometriosis \n249\nand an improved quality of life for affected women. \nTransvaginal ultrasound (TVUS) is a first-line imaging \ntool for assessing women with endometriosis 5-7.  \nA systematic review by the Cochrane group states that \nTVUS with bowel preparation has high sensitivity and \nspecificity for diagnosing endometriomas and DIE, \ncompared to laparoscopic results 8. However, no \nrecommendations were made regarding superficial \nendometriosis or its correlation with ultrasound, clinical, \nor laparoscopic findings. \nThe literature on the role of TVUS with bowel prepa -\nration for detecting superficial endometriosis is sparse 4. \nOkaro et al.9 first described the concept of soft markers \nbased on the degree of ovarian and uterine mobility \nand tenderness on ultrasound examination in contrast \nwith a hard marker defined as a structural abnormality \n(an endometrioma or hydrosalpinx). Soft markers as \nindirect ultrasound findings have been associated with \nsuperficial endometriosis 9, but their diagnostic useful -\nness is unknown. This study focused on soft markers \nin basal TVUS with bowel preparation and their rela -\ntionship to chronic pelvic pain and surgical findings \nvisualized by laparoscopy in women with superficial \nendometriosis.\nMATERIALS AND METHODS \nThis retrospective cohort study was conducted from \nJanuary 2018 to December 2019 at the Clinica of \nExcelencia in Endometriosis in Zapopan, Jalisco, \nMexico. Women referred with a clinical suspicion and \nwith only soft markers on basal TVUS with bowel \npreparation for endometriosis and who underwent  \ntherapeutic laparoscopy for the first time were included. \nWomen with ultrasound findings suggestive of DIE or \nendometriomas, missing clinical and/or laparoscopic \ndata, or conversion to open surgery were excluded. \nInformed consent was not required for this study of \ninformation collected during routine clinical care. The \nInstitutional Ethics and Research Committees approved \nthe protocol.\nDevelopmental study and clinical  \nvariables\nA search for ultrasound reports and images of women \nwith chronic pelvic pain referred with a clinical suspicion \nof endometriosis and presenting only soft markers on \nbasal TVUS with bowel preparation with failure of drug \ntreatment, defined as persistence of pain on a visual \nanalog scale over 6, with at least 6 months of progestin \nuse, and who underwent therapeutic laparoscopy for \nthe first time.\nThe variables were age and chronic pelvic pain last -\ning at least 6 months, assessed by clinical interview as \ndysmenorrhea, dyschezia, dyspareunia, and/or dysuria. \nA visual analog scale was used to classify pain, with  \n0 being absent, 1-3 mild, 4-7 moderate, and 8-10 severe. \nDefinition of ultrasonographic soft \nmarkers\nOvarian tenderness  was categorized by severity as \nabsent, mild, moderate, or severe, according to the \npatient1. A tenderness-guided ultrasound examination \nwas performed with or without an acoustic window \nbetween the  transvaginal probe and the surrounding \nvaginal structures, coupled with an ‘active’ role of the \npatient, who indicated the site and intensity of any ten -\nderness during the examination 9. \nOvarian adhesions were considered absent, mild (+), \nor strong (+++) by applying pressure with the transducer \nand external pressure with the other hand and \nvisualizing in real time if the ovary was fixed to the \nuterus or the pelvic wall 1. Direct visualization of \nadhesions is possible when there is pelvic fluid. \nObliteration of the cul-de-sac (CDS) if there is no \nsliding between the uterus and the anterior rectal wall \nwhen pressure is applied with the transducer and the \nleft hand of the operator.\nObliteration of the vesico-uterine pouch (VUP) if \nthere is no sliding between the bladder dome and the \nanterior wall of the uterus when pressure is applied to \nthe abdomen with the transducer and the operator’s left \nhand.\nImage acquisition protocol\nGrayscale TVUS and power Doppler examinations \nwere performed using a Samsung Accuvix XG system \n(Samsung Group, Suwon, South Korea) with a 4-9 MHz  \nendocavitary transducer. The patient was in the lithot -\nomy position, and the TVUS bowel preparation protocol \nfor endometriosis was performed according to the \nInternational Deep Endometriosis Analysis (IDEA) \ngroup1. The TVUS technique for detecting superficial \nendometriosis was performed with detailed scanning of \nthe peritoneum in the right anterior compartment (RAC), \nthe left anterior compartment (LAC), the right posterior \ncompartment (RPC), and the left posterior compart -\nment (LPC) of the pelvis. The surface of the ovaries \nand the serosa of the rectosigmoid were also evaluated \n\nJ Mex  Fed  Radiol  iMaging . 2023;2(4):248-258\n250\nin detail. All ultrasound examinations were performed \nby a single radiologist (VGG), who is an expert in endo -\nmetriosis with 15 years of experience.\nSurgical laparoscopic findings\nAfter the ultrasound examination, all women under -\nwent laparoscopic surgery performed by a team of endo-\nmetriosis experts (MLT and MLZ) who were informed of \nthe ultrasound findings. The presence of adhesions on \nlaparoscopic examination of both ovaries, CDS, VUP, \nRAC, LAC, RPC, LPC, and RPC was determined as \nabsent, mild (+), moderate (++), or severe (+++), referred \nto as a qualitative finding by the surgeon10. The presence \nand length of superficial endometriotic lesions directly \nvisualized during laparoscopic examination in the RAC, \nLAC, RPC, LPC, and RPC were considered absent,  \n< 1 cm, 1-3 cm, or > 3 cm 10.\nStatistical analysis\nThe variables are described as means and standard \ndeviations for numerical data and frequencies and per -\ncentages for categorical data. An analysis of variance \n(ANOVA) was performed between each variable. \nPearson’s chi-square test was then performed to deter-\nmine p-values. A significance level of p < 0.05 was \nused. The statistical analysis was performed using \nSPSS version 26 (IBM Corp., Armonk, NY, USA). \nRESULTS\nA total of 33 women were assessed. Eight patients \nwere excluded: seven due to a lack of clinical and/or \nlaparoscopic data and one who converted to open \nsurgery. We included 25 women with clinically  \nsuspected endometriosis and only ultrasonographic \nsoft markers on basal TVUS with bowel preparation \nwho underwent therapeutic laparoscopy for the first \ntime (Table 1). In all patients, the type and intensity \n(mean ± SD) of chronic pelvic pain found were severe \ndysmenorrhea (7.60 ± 3.08), moderate dyspareunia \n(4.84 ± 3.51), and mild dyschezia and dysuria (3.44 ± \n3.89 and 2.12 ± 2.92, respectively). Dysmenorrhea was \nthe predominant pain reported by all patients. Patients \nwith dyschezia and dysuria tended to have stronger \nadhesions, represented by a severity of +++. These \nresults suggest that patients with suspected endome -\ntriosis should be thoroughly examined for dyschezia \nand dysuria, as these symptoms may indicate severe \nadhesions. \nFigure 1, a power Doppler TVUS, shows the pres -\nence of adhesions after external mobilization maneu -\nvers without a separation plane between the right ovary \n(RO) and the abdominal wall. Figure 2, a grayscale \nTVUS, shows the findings of a patient with severe dys -\nmenorrhea, moderate dyschezia, and dyspareunia. No \nmovement was detected when performing external \nmobilization maneuvers on the RO and anterior rectal \nwall, and the patient reported severe pain, concluding \nadhesions as a soft marker for superficial endometrio -\nsis. Figure 3 shows a static laparoscopic image of a \npatient with CDS obliteration and focal tenderness on \nTVUS (data not shown), and superficial endometriotic \nlesions and adhesions on the CDS and pelvic perito -\nneal defects are seen at the retrocervical level. The \nlaparoscopic findings confirmed the severity and extent \nof the endometriotic lesions, with many patients having \nlesions larger than 3 cm. Case 24 presents a woman \nwith moderate dysmenorrhea, dyspareunia, and signifi -\ncant adhesions in multiple compartments (RAC 1-3 cm, \nLAC 1-3 cm, RPC 1-3 cm, and LPC 1-3 cm).\nAssociation of ultrasonographic soft \nmarkers with type and intensity of chronic \npelvic pain\nThe frequency of ultrasonographic soft markers and \nchronic pelvic pain is shown in Table 2. Patients with \nmoderate tenderness in the RO reported moderate dys-\nmenorrhea (6.62 ± 2.44) and dyspareunia (5.00 ± 3.29). \nThose with severe tenderness in the RO reported \nsevere dysmenorrhea (8.50 ± 1.73). Moderate tender -\nness was found in patients with moderate pain (4.81 ± \n3.37). In contrast, patients with mild tenderness in the \nleft ovary (LO) had severe dysmenorrhea (9.00 ± 1.67). \nThose with moderate tenderness reported severe  \ndysmenorrhea (8.27 ± 1.42), and those with severe \ntenderness had moderate dysmenorrhea (5.00 ± 4.54). \nFigure 4 shows a grayscale TVUS of a patient with \nsevere dysmenorrhea and dyspareunia, in which the \nLO is shown without a separation plane of the uterus \nand abdominal wall. No movement was seen, and the \npatient reported severe pain with external mobilization \nmaneuvers, concluding adhesions as a soft marker of \nsuperficial endometriosis. Figure 5 shows  a grayscale \nTVUS of a patient with severe dysmenorrhea, moderate \ndyschezia, and dyspareunia, in which CDS obliteration \nand focal tenderness were found. There is no separa -\ntion plane, and adhesions were seen during dynamic \nmaneuvers.\n\nA.S. Sanchez-Gomez et al. TVUS soft markers in superficial endometriosis \n251\nTable 1. Pain characteristics, ultrasonographic soft markers, and laparoscopic findings in 25 patients with clinically significant superficial endometriosis\nCase Age, \nyears\nChronic pelvic pain a Ultrasonographic soft markers Laparoscopic findings\nDysmenorrhea Dyspareunia Dyschezia Dysuria Tenderness\nRO/LO\nAdhesionsb\nRO/LO\nCDS\nObliteration\nVUP\nObliteration\nAdhesionsb\nRO/LO\nAdhesionsb\nCDS/VUP\nLocalization \nand length of \nendometriotic \nlesions\n1 19 10 0 8 7 RO mild\nLO mild\nNo/no No No No/no No/no RAC: < 1cm\nRPC: 1-3 cm\n2 23 10 0 5 3 RO absent\nLO mild\nNo/+++ No No No/no No/no RAC: < 1 cm\nRPC: 1-3 cm\n3 27 8 6 0 0 RO moderate\nLO mild\nNo/no No No No/+ No/no LAC: < 1 cm\nRPC: < 1 cm\nLPC: < 1 cm\n4 26 10 0 0 0 RO mild\nLO absent\nNo/no No No +++/++ No/+ RPC: > 3 cm\nLPC: > 3 cm\n5 29 10 0 0 0 RO absent\nLO moderate\nNo/+ No No ++/+++ No/+++ RPC: > 3 cm\nLPC: > 3 cm\n6 31 9 8 8 0 RO mild\nLO moderate\n+/+ Yes No No/+++ +++/+++ RPC: > 3 cm\nLPC: > 3 cm\n7 35 8 9 7 6 RO moderate\nLO moderate\nNo/+ No No No/no No/no RPC: 1-3 cm\nLPC: 1-3 cm\n8 43 0 9 4 4 RO absent\nLO severe\n+/+++ No No No/+ No/++ LPC: 1-3 cm\n9 32 10 3 6 0 RO mild\nLO mild\n+/+ No No No/no ++/no LAC: > 3 cm\nRPC: 1-3 cm\nLPC: < 1 cm\n10 40 10 5 0 0 RO severe\nLO moderate\n+++/no No No +++/no No/no RPC: > 3 cm\nLPC: > 3 cm\n11 25 7 0 0 6 RO moderate\nLO moderate\nNo/no No No No/no No/no RPC: 1-3 cm\nLPC: 1-3 cm\n12 36 7 5 0 0 RO moderate\nLO moderate\n+++/+++ Yes No No/no No/no RPC: < 1 cm\nLPC: < 1 cm\n13 32 10 5 0 0 RO mild\nLO moderate\n+++/+++ Yes No +++/+++ No/no RPC: > 3 cm\nLPC: > 3 cm\n14 29 10 10 10 5 RO mild\nLO severe\nNo/+++ Yes No ++/+++ No/++ RPC: > 3 cm\nLPC: > 3 cm\n15 34 1 7 6 0 RO moderate\nLO severe\nNo/no No No No/no No/no LPC: 1-3 cm\n16 38 10 5 8 6 RO absent\nLO mild\nNo/+ Yes No No/+++ No/+++ RAC: < 1 cm\nLAC: < 1 cm\n17 33 8 6 5 0 RO absent\nLO moderate\nNo/+ No No No/no No/no LAC: > 3 cm\nRPC: > 3 cm\n18 34 9 9 9 9 RO severe\nLO severe\n+/+ No No ++/++ No/++ RPC: 1-3 cm\nLPC: 1-3 cm\n19 32 0 9 0 0 RO absent\nLO severe\nNo/+++ No No No/+++ +/no RAC: 1-3 cm\nLAC: 1-3 cm\nRPC: > 3 cm\nLPC: > 3 cm\n20 29 9 7 0 0 RO moderate\nLO moderate\n+/no No No ++/no No/no RPC: 1-3 cm\nLPC: 1-3 cm\n21 36 9 4 10 5 RO severe\nLO severe\nNo/+++ No No No/no ++/no None\n22 35 6 0 0 0 RO severe\nLO severe\n+++/+++ No No No/no No/no RAC: < 1 cm\nLAC: < 1 cm\nRPC: 1-3 cm\nLPC: < 1 cm\n23 37 7 0 0 2 RO moderate\nLO moderate\n+++/+++ Yes No +++/+++ No/+++ RPC: > 3 cm\nLPC: > 3 cm\n24 31 6 6 0 0 RO moderate\nLO mild\n++++/++ No No +++/+++ No/+++ RAC: 1-3\nLAC: 1-3 cm\nRPC: 1-3 cm\nLPC: 1-3 cm\n25 41 6 8 0 0 RO mild\nLO moderate\n+/+ No No +++/+++ No/+++ None\naVisual analogue scale; bAdhesion severity represented by +, ++ or +++ as mild, moderate, and strong; RO: right ovary; LO: left ovary; CDS: Cul-De-Sac;  \nVUP: vesico-uterine pouch; RAC: right anterior compartment; LAC: left anterior compartment; RPC: right posterior compartment; LPC: left posterior compartment.\n\nJ Mex  Fed  Radiol  iMaging . 2023;2(4):248-258\n252\nFigure 1. Power Doppler TVUS, of a woman with severe dysmenorrhea. The image shows the RO without any separation plane from the \nabdominal wall (arrowheads). When performing external mobilization maneuvers, no movement was seen, and the patient reported moderate \npain, suggesting adhesions as a soft marker for superficial endometriosis. \nTVUS: transvaginal ultrasound; RO: right ovary.\nAn association was found between patients with mild \nand strong right-side adhesions and severe dysmenor -\nrhea (7.16 ± 3.76 and 7.66 ± 1.86, respectively). Women \nwith mild adhesions reported severe dyspareunia  \n(7.33 ± 2.25). Figure 6 shows a laparoscopic static image \nof a woman with severe dysmenorrhea and  moderate \ndyspareunia with superficial endometriotic lesions at the \nRAC. Grayscale TVUS demonstrated RO adhesions and \nfocal tenderness (data not shown). Patients with mild \nadhesions on the left side reported severe dysmenorrhea \n(8.75 ± 1.38) and moderate dyschezia and dyspareunia \n(5.37 ± 3.54 and 6.00 ±  3.20, respectively). Those with \nsevere adhesions reported moderate dysmenorrhea (6.50 \n± 3.77). Figure 7 shows a laparoscopic static image of \nsuperficial endometriotic lesions and adhesions in the \nLAC in a patient with severe dysmenorrhea and focal LO \ntenderness on TVUS (data not shown).\nThe CDS was obliterated in women with severe  \ndysmenorrhea (8.83 ± 1.47) and moderate dyschezia and \ndyspareunia (4.33 ± 4.80 and 5.50 ± 3.39, respectively). \nAssociation between the severity of \nadhesions visualized during laparoscopy \nand the type and intensity of chronic \npelvic pain\nLaparoscopic findings are shown in Table 3, and \nthere were no complications. Patients with moderate \nor severe right-sided adhesions reported severe dys -\nmenorrhea (9.50 ± 9.57 and 8.16 ±  2.04, respectively). \nPatients with moderate right-sided adhesions had \nmoderate dyschezia and dyspareunia (4.00 ± 3.28 and \n6.50 ± 4.50, respectively). Patients with severe right-\nsided adhesions reported moderate dyspareunia (4.00 \n± 3.28). Severe dysmenorrhea (9.50 ± 0.70) was found \nin women with moderate left-sided and severe adhe -\nsions (7.55 ±  3.32). Patients with moderate left-sided \nadhesions reported moderate dyschezia, dyspareu -\nnia, and dysuria (4.50 ±  6.36). Patients with severe \nleft-sided adhesions reported moderate dyspareunia \n(5.66 ± 3.64).\n\nA.S. Sanchez-Gomez et al. TVUS soft markers in superficial endometriosis \n253\nFigure 2. Grayscale TVUS of a woman with severe dysmenorrhea, moderate dyschezia, and dyspareunia. The image shows the RO without \nany separation plane from the uterus or anterior rectal wall. When performing external mobilization maneuvers, no movement was seen, and \nthe patient reported severe pain, concluding adhesions as a soft marker for superficial endometriosis (arrowheads). \nRO: right ovary; TVUS: transvaginal ultrasound; U: uterus; R: rectum.\nFigure 3. Static laparoscopic image of a woman with severe \ndysmenorrhea and dyspareunia, with CDS obliteration on TVUS (data \nnot shown). The image shows superficial endometriotic lesions \n(dotted circles) and pelvic peritoneal defects (arrowheads) causally \nrelated to endometriosis, as this patient had neither pregnancy nor \nprevious surgical procedures. \nCDS: Cul de Sac; TVUS: transvaginal ultrasound.\nPatients with mild adhesions in the CDS had severe \ndysmenorrhea. Women with moderate adhesions at \nthis level had moderate dysmenorrhea and dysuria \n(6.33 ± 5.50 and 6.00 ±  2.64, respectively) and \nsevere dyschezia and dyspareunia (7.66 ±  3.21 and \n9.33 ± 0.57, respectively). Patients with severe adhe -\nsions reported severe dysmenorrhea (8.00 ±  1.89) \nand moderate dyspareunia (4.50 ±  3.67). Patients \nwith moderate adhesions of the VUP reported severe \ndysmenorrhea and dyschezia (9.50 ±  0.70 and 8.00 \n± 2.82, respectively). Patients with severe adhesions \nat this level reported severe dysmenorrhea, dysche -\nzia, and dyspareunia (9.00 ±  0, 8.00 ± 0, and 8.00 ± \n0, respectively). Ultrasonographic RO and LO adhe -\nsions were associated with surgical RO adhesions  \n(p = 0.02) and LO adhesions (p = 0.04), respectively. \nThere were no significant differences compared with \nother parameters.\n\nJ Mex  Fed  Radiol  iMaging . 2023;2(4):248-258\n254\nFigure 4. Grayscale TVUS of a woman with severe dysmenorrhea and \ndyspareunia. The image shows the LO without any separation plane between \nthe uterus and AW. When performing external mobilization maneuvers, no \nmovement was seen, and the patient reported severe pain, concluding \nadhesions as a soft marker for superficial endometriosis (arrowheads). \nAW: abdomino-pelvic; LO: left ovary; TVUS: transvaginal ultrasound; U: uterus.\nTable 2. Association between ultrasonographic soft markers and type and intensity of chronic pelvic pain a in 25 patients with clinically significant \nsuperficial endometriosis \nDescription n (%) Dysmenorrhea\nMean ± SD\nDyschezia\nMean ± SD\nDyspareunia\nMean ± SD\nDysuria\nMean ± SD\nRO tenderness\nAbsent 6 (24.0) 6.33 ± 4.96 3.66 ± 3.14 4.83 ± 4.07 2.16 ± 2.56\nMild 7 (28.0) 9.28 ± 1.49 4.57 ± 4.42 4.85 ± 4.01 1.71 ± 2.98\nModerate 8 (32.0) 6.62 ± 2.44 1.62 ± 3.02 5.00 ± 3.29 1.75 ± 2.71\nSevere 4 (16.0) 8.50 ± 1.73 4.75 ± 5.50 4.50 ± 3.69 3.50 ± 4.35\nLO tenderness\nAbsent 1 (4.0) 10.00 ± 0 - - -\nMild 6 (24.0) 9.00 ± 1.67 4.50 ± 3.67 3.33 ± 2.80 2.66 ± 3.20\nModerate 11(44.0) 8.27 ± 1.42 1.81 ± 3.18 4.81 ± 3.37 1.27 ± 2.41\nSevere 7 (28.0) 5.00 ± 4.54 5.57 ± 4.39 6.85 ± 3.62 3.28 ± 3.45\nRO adhesionsb\nAbsent 13 (52.0) 7.76 ± 3.39 4.53 ± 4.03 4.30 ± 3.90 2.92 ± 2.95\nMild 6 (24.0) 7.16 ± 3.76 4.50 ± 3.88 7.33 ± 2.25 2.16 ± 3.71\nStrong 6 (24.0) 7.66 ± 1.86 - 3.50 ± 2.73 0.33 ± 0.81\nLO adhesions \nAbsent 7 (28.0) 7.85 ± 3.23 2.00 ± 3.46 3.57 ± 3.40 1.85 ± 3.18\nMild 8 (32.0) 8.75 ± 1.38 5.37 ± 3.54 6.00 ± 3.20 2.62 ± 3.73\nStrong 10 (40.0) 6.50 ± 3.77 2.90 ± 4.17 4.80 ± 3.85 1.90 ± 3.73\nCDS \nNormal 6 (24.0) 7.21 ± 3.37 3.15 ± 3.67 4.63 ± 3.62 2.10 ± 3.05\nObliterated 19 (76.0) 8.83 ± 1.47 4.33 ± 4.80 5.50 ± 3.39 2.16 ± 2.71\nVUPc\nNormal 25 (100) 7.60 ± 3.08 3.44 ± 3.89 4.84 ± 3.51 2.12 ± 2.92\naVisual analogue scale; bAdhesion severity represented by +, ++ or +++ as mild, moderate, or severe/strong.  cNo case with obliterated VUP; RO: right ovary;  \nLO: left ovary; CDS: Cul-De-Sac; VUP: vesico-uterine pouch. \nFigure 5. Grayscale TVUS of a woman with severe dysmenorrhea, \nmoderate dyschezia, and dyspareunia. CDS obliteration and focal \ntenderness. There is no separation plane (arrowheads) and adhesions \nwere seen during dynamic maneuvers.\nAW: abdomino-pelvic wall; CDS: Cul de Sac;  LO: left ovary; TVUS: transvaginal \nultrasound; U: uterus.\n\nA.S. Sanchez-Gomez et al. TVUS soft markers in superficial endometriosis \n255\nFigure 6. Laparoscopic static image showing superficial endometriotic lesions at the RAC (dotted circle) of a woman with severe dysmenorrhea \nand moderate dyspareunia. In grayscale TVUS, RO had adhesion and focal tenderness (data not shown).\nRAC: right anterior compartment; RO: right ovary; TVUS: transvaginal ultrasound. \nFigure 7. Laparoscopic static image shows superficial endometriotic \nlesions (dotted circles) and adhesions at the LAC (arrowheads) of a \npatient with severe dysmenorrhea and focal tenderness at the LO \ndocumented by TVUS (data not shown). \nLAC: left anterior compartment; LO: left ovary; TVUS: transvaginal ultrasound.\nAssociation between the severity of \nendometriotic lesions and the type and \nintensity of chronic pelvic pain\nPatients with moderate and severe pelvic pain had \nendometriotic lesions. There was no association between \nlesion length and pain severity (Table 4). Patients with \nlesions less than 1 cm in length in the RAC reported \nsevere dysmenorrhea (8.66 ± 2.30), moderate dyschezia \n(4.33 ± 4.04), mild dyspareunia (1.66 ± 2.88), and dysuria \n(3.00 ± 3.00). Patients with lesions 1-3 cm in length at \nthis level reported severe dyspareunia (7.5 ±  2.12).\nPatients with lesions less than 1 cm in length in the \nLAC reported severe dysmenorrhea (8.00 ±  2.00). \nThose with lesions 1-3 cm in length reported moderate \ndysmenorrhea (5.00 ±  4.58) and severe dyspareunia \n(8.00 ± 1.73). Patients with lesions larger than 3 cm \nreported severe dysmenorrhea (9.00 ±  1.41) and mod-\nerate dyschezia (5.50 ±  0.70).\nPatients reported severe dysmenorrhea with endo -\nmetriotic lesions in the RPC smaller than 1 cm (7.50 ± \n0.70), 1-3 cm (8.12 ± 1.64), and larger than 3 cm  \n\nJ Mex  Fed  Radiol  iMaging . 2023;2(4):248-258\n256\nTable 3. Association between adhesion severity visualized at laparoscopy and the type and intensity of chronic pelvic paina in 25 patients with clinically \nsignificant superficial endometriosis\nDescription n (%) Dysmenorrhea\nMean ± SD\nDyschezia  \nMean ± SD\nDyspareunia  \nMean ± SD\nDysuria \nMean ± SD\nRO adhesionsb,c\nAbsent 15 (60.0) 6.86 ± 3.60 4.46 ± 3.58 4.73 ± 3.45 2.16 ± 2.56\nModerate 4 (16.0) 9.50 ± 9.57 04.75 ± 5.50 6.50 ± 4.50 3.50 ± 4.35\nSevere 6 (24.0) 8.16 ± 2.04 - 4.00 ± 3.28 0.33 ± 0.81\nLO adhesions\nAbsent 12 (48.8) 7.91 ± 2.57 3.91 ± 3.70 3.83 ± 3.21 2.25 ± 2.92\nMild 2 (8.0) 4.00 ± 5.65 2.00 ± 2.82 7.50 ± 2.12 2.00 ± 2.82\nModerate 2 (8.0) 9.50 ± 0.70 4.50 ± 6.36 4.50 ± 6.36 4.50 ± 6.36\nSevere 9 (36.0) 7.55 ± 3.32 2.88 ± 4.37 5.66 ± 3.64 1.44 ± 2.40\nCDS adhesions \nAbsent 15 (60.0) 7.53 ± 3.13 3.13 ± 3.66 4.40 ± 3.18 1.80 ± 2.75\nMild 1 (4.0) 10 ± 0 - - -\nModerate 3 (12.0) 6.33 ± 5.50 7.66 ± 3.21 9.33 ± 0.57 6.00 ± 2.64\nSevere 6 (24.0) 8.00 ± 1.89 2.66 ± 4.13 4.50 ± 3.67 1.33 ± 2.42\nVUP adhesions\nAbsent 21 (84.0) 7.71 ± 2.83 2.95 ± 3.72 4.61 ± 3.63 2.28 ± 3.01\nMild 1 4.0 - - -\nModerate 2 (8.0) 9.50 ± 0.70 8.00 ± 2.82 3.50 ± 0.70 2.50 ± 3.53\nSevere 1 (4.0) 9.00 ± 0 8.00 ± 0 8.00 ± 0 -\naVisual analogue scale;  bAdhesion severity represented by +, ++ or +++ as mild, moderate, or severe.  bNone case with mild adhesions in RO; RO: right ovary; \nLO: left ovary; CDS: Cul-De-Sac; VUP: vesico-uterine pouch.\nTable 4. Association between endometriotic lesion length found at laparoscopy and type and intensity of chronic pelvic pain a in 25 patients with \nclinically significant superficial endometriosis\nDescription n (%) Dysmenorrhea\nMean ± SD\nDyschezia  \nMean ± SD\nDyspareunia  \nMean ± SD\nDysuria \nMean ± SD\nEndometriotic lesion length in the RAC b\nAbsent 20 (80.0) 7.90 ± 2.82 3.65 ± 4.00 5.05 ± 3.48 2.20 ± 3.03\n< 1 cm 3 (12.0) 8.66 ± 2.30 4.33 ± 4.04 1.66 ± 2.88 3.00 ± 3.00\n1-3 cm 2 (8.0) 3.00 ± 4.24 - 7.5 ± 2.12 -\nEndometriotic lesion length in the LAC\nAbsent 17 (68.0) 7.82 ± 3.06 3.41 ± 4.00 4.52 ± 3.79 2.23 ± 2.68\n< 1 cm 3 (12.0) 8.00 ± 2.00 2.66 ± 4.61 3.66 ± 3.21 2.00 ± 3.46\n1-3 cm 3 (12.0) 5.00 ± 4.58 3.00 ± 5.19 8.00 ± 1.73 3.00 ± 5.19\n> 3 cm 2 (8.8) 9.00 ± 1.41 5.50 ± 0.70 4.50 ± 2.12 -\nEndometriotic lesion length in the RPC\nAbsent 6 (24.4) 6.00 ± 4.51 6.00 ± 3.57 5.50 ± 3.27 3.66 ± 3.01\n< 1 cm 2 (8.8) 7.50 ± 0.70 - 5.50 ± 0.70 -\n1-3 cm 8 (32.0) 8.12 ± 1.64 3.37 ± 3.77 4.25 ± 3.99 3.00 ± 3.5\n> 3 cm 9 (36.0) 8.22 ± 3.27 2.55 ± 4.03 4.77 ± 3.96 0.77 ± 1.71\nEndometriotic lesion length in the LPC\nAbsent 6 (24.0) 8.83 ± 1.60 6.00 ± 3.52 3.83 ± 3.25 3.50 ± 3.01\n< 1 cm 4 (16.0) 7.75 ± 1.70 1.50 ± 3.00 3.50 ± 2.64 -\n1-3 cm 7 (7.0) 5.71 ± 3.72 3.71 ± 3.77 6.71 ± 3.19 3.57 ± 3.64\n> 3 cm 8 (32.0) 8.25 ± 3.49 2.25 ± 4.20 4.62 ± 4.20 0.87 ± 1.80\naVisual analogue scale; bNo case with length of endometriotic lesions > 3 cm in the RAC; RAC: right anterior compartment; LAC: left anterior compartment;  \nRPC: right posterior compartment; LPC: left posterior compartment.\n\nA.S. Sanchez-Gomez et al. TVUS soft markers in superficial endometriosis \n257\n(8.22 ± 3.27). Patients with lesions at this level reported \nmoderate dyspareunia (5.50 ±  0.70) for lesions smaller \nthan 1 cm, lesions 1-3 cm (4.25 ±  3.99), and lesions \nlarger than 3 cm (4.77 ±  3.96). Patients with lesions \nsmaller than 1 cm in the LPC reported severe dysmen -\norrhea (7.75 ± 1.70). Those with lesions between 1 and \n3 cm reported moderate dysmenorrhea (5.71 ±  3.72) \nand severe dyspareunia (6.71 ± 3.19). Patients with \nlesions larger than 3 cm in this area reported severe \ndysmenorrhea (8.25 ±  3.49). A one-way ANOVA \nshowed a significant association between dyspareunia \nintensity and VUP adhesions (p = 0.010).\nUltrasonographic CDS obliteration was significantly \nassociated with LO adhesions and CDS adhesions \nfound at laparoscopy (p = 0.01 and p < 0.02, respec -\ntively). No significant differences were found compared \nwith other parameters.\nDISCUSSION\nThis study demonstrates the association between \nsoft markers on basal TVUS with bowel preparation in \npatients with clinically significant superficial endometri -\nosis and laparoscopy findings. Our study sheds light \non the complexity of endometriosis. It emphasizes the \nneed for comprehensive assessment, including an \nevaluation of the ultrasound-based soft markers. \nSuperficial endometriosis has been diagnosed with \na median delay of 5 years 11. The detection of ultra -\nsound-based soft markers may be helpful for an early \ndiagnosis. Okaro et al. 9, in a study of 120 women, \ndemonstrated only ultrasonographic soft markers in 51 \n(53.1%) of 96 patients. Pelvic adhesions and peritoneal \nendometriotic lesions were found in 37 (72.5%) of 51 \npatients. On the other hand, Reid et al. 12 studied the \naccuracy of ultrasound in predicting the site of endo -\nmetriotic involvement during laparoscopy. They found \nthat ovarian immobility on TVUS was significantly asso -\nciated with ipsilateral pelvic pain, uterosacral ligamen -\ntous lesions, pelvic wall adhesions, endometriomas, \nand CDS obliteration. The authors suggested that a \npatient with mobile ovaries is unlikely to have superfi -\ncial endometriosis without endometriomas, which is \nconsistent with our findings. In summary, ultrasono -\ngraphic soft markers are defined as focalized tender -\nness, adhesions, absence of uterine and ovarian \nmobility, and obliteration of VUP or CDS 9. Site-specific \ntenderness and ovarian mobility as indirect ultra -\nsound-based markers of pelvic pathology improved the \nability to predict or rule out diagnosis in women with \nchronic pelvic pain 9. Soft markers on TVUS with bowel \npreparation may be sufficient to indicate clinically sig -\nnificant superficial endometriosis.\nThe severity of symptoms is not directly related to \nthe severity of the disease and should be considered \nalong with the soft markers in the TVUS to determine \nthe presence and extent of clinically significant super -\nficial endometriosis.  Menakaya et al. 13 showed an \noverall accuracy of 84.9% in predicting the exact level \nof laparoscopic findings with an excellent correlation \n(0.82). However, the authors did not consider symptom \nseverity, which was addressed in our study. Most of \nthe patients in our study suffered moderate to severe \ndysmenorrhea and had only soft markers on their \nultrasound examination, all of whom had at least one \npositive ultrasonographic soft marker. Dyspareunia, \ndyschezia, and dysuria can also be present without \nDIE. This finding is consistent with a previous study 12 \nthat found a significant association between ovarian \ntenderness on ultrasound and CDS adhesions and a \nstrong association between right-sided adhesions on \nultrasound and laparoscopy findings. Patients with \nsevere dyschezia in our study had adhesions in the \nCDS and VUP at laparoscopy. Women with severe \ndyspareunia also had right-sided adhesions on ultra -\nsound and at surgery, adhesions in the LO, CDS, and \nVUP, and endometriotic lesions in the RAC and LAC. \nThe relevance of the diagnosis of clinically significant \nsuperficial endometriosis lies in its significant impact  \non the health of women, especially those suffering  \nfrom chronic pelvic pain. Soft markers found in TVUS \nare often classified as mild disease but may indicate \nclinically significant superficial endometriosis, so  \nlaparoscopic examination and timely treatment are \nrecommended.\nThis study has several strengths. All patients were \nreferred with a clinical suspicion of endometriosis and \nunderwent surgery performed by experienced laparo -\nscopic gynecologists. One of the main limitations is the \nsample size, which was reduced for various reasons. \nA very specific patient selection was conducted, exclud-\ning those who had DIE, ovarian involvement, or other \nsurgical procedures. Patients who previously under -\nwent surgery may have adhesions due to their surgical \nhistory, making assessment more difficult. An analysis \nof the excluded patients revealed that most patients \nundergo multiple surgeries at a young age to relieve \nchronic pelvic pain, leaving us with only younger \npatients (mean age, 32.28 years) with a shorter dura -\ntion of disease. Ovarian mobility assessment and \nsite-specific tenderness are subjective and require \nexperience in the use of TVUS in assessing pelvic pain.\n\nJ Mex  Fed  Radiol  iMaging . 2023;2(4):248-258\n258\nCONCLUSION\nOur study showed that soft markers on a well-  \nperformed ultrasound examination were the only find -\nings that indicated clinically significant superficial endo -\nmetriosis. These subjective ultrasound findings are not \nusually reported during routine examinations. TVUS-\nbased soft markers can triage appropriate patients for \nfurther investigation. Our results must be confirmed in \nprospective studies with a larger and more diverse \npatient population.\nAcknowledgments\nThe authors thank Professor Ana M. Contreras-\nNavarro for her guidance in preparing and writing this \nscientific paper. This original research in the Radiology \nSpecialty field was an awarded thesis at the Primera \nConvocatoria Nacional 2023, “Las Mejores Tesis para \nPublicar en el JMeXFRI.”\nFunding\nThis research received no external funding.\nConflicts of interest\nThe authors declare no conflicts of interest.\nEthical disclosures\nProtection of individuals.  This study complied with \nthe Declaration of Helsinki (1964) and its \namendments.\nConfidentiality of data.  The authors declare they \nfollowed their center’s protocol for sharing patient data.\nRight to privacy and informed consent.  Informed \nconsent was not required for this observational study \nof information collected during routine clinical care.\nUse of artificial intelligence.  The authors state that \nthey did not use generative artificial intelligence to \nprepare this manuscript and/or create tables, figures, \nor figure legends.\nREFERENCES\n 1. Guerriero S, Condous G, Van den Bosch T, Valentin L, F. Leone FP, D. \nVan S, et al. Systematic approach to sonographic evaluation of the pelvis \nin women with suspected endometriosis, including terms, definitions, and \nmeasurements: a consensus opinion from the International Deep  \nEndometriosis Analysis (IDEA) group. Ultrasound Obstet Gynecol. 2016; \n48(3):318-332. doi:10.1002/uog.15955.\n 2. International Working Group of AAGL, ESGE, ESHRE and WES;  \nTomassetti C, Johnson NP, Petrozza J, Abrao MS, Einarsson JI, Horne \nAW, et al. An international terminology for endometriosis, 2021. Hum \nReprod Open. 2021;2021(4): hoab029. doi:10.1093/hropen/hoab029. \n 3. Horne AW, Daniels J, Hummelshoj L, Cox E, Cooper KG. Surgical  \nremoval of superficial peritoneal endometriosis for managing women with \nchronic pelvic pain: time for a rethink? BJOG. 2019;126(12):1414-1416. \ndoi: 10.1111/1471-0528.15894.\n 4. Pedrassani M, Guerriero S, Pascual MÁ, Ajossa S, Graupera B,  \nPagliuca M, et al. Superficial endometriosis at ultrasound examination-a \ndiagnostic criteria proposal. Diagnostics (Basel). 2023. 27;13(11):1876. \ndoi:10.3390/diagnostics13111876.\n 5. Benacerraf BR, Groszmann Y. Sonography should be the first imaging \nexamination done to evaluate patients with suspected endometriosis. J \nUltrasound Med 2012; 31:651-653. doi: 10.7863/jum.2012.31.4.651.\n 6. Chamié PL, Blasbalg R, Mendes Alves Pereira R, Warmbrand G,  \nSerafini PC. Findings of pelvic endometriosis at transvaginal US, MR \nimaging, and laparoscopy. RadioGraphics. 2011; 31(4):E77-100. \ndoi:10.1148/rg.314105193.\n 7. Chamié LP. Imaging diagnosis of endometriosis. J Mex Fed Radiol  \nImaging. 2022;1(3):138-150. doi: 10.24875/JMEXFRI.M22000019.\n 8. Nisenblat V, Bossuyt PM, Farquhar C, Johnson N, Hull ML. Imaging \nmodalities for the non-invasive diagnosis of endometriosis. Cochrane \nDatabase Syst Rev. 2016; 26;2(2):CD009591. doi: 10.1002/14651858.\nCD009591.pub2.\n 9. Okaro E, Condous G, Khalid A, Timmerman D, Ameye L, Huffel SV,  \net al. The use of ultrasound-based ‘soft markers’ for the prediction of \npelvic pathology in women with chronic pelvic pain–can we reduce the \nneed for laparoscopy? BJOG. 2006;113(3):251-256. doi:10.1111/j.1471-  \n0528.2006.00849.x.\n 10. Menakaya U, Reid S, Infante F, Condous G. Systematic evaluation of \nwomen with suspected endometriosis using a 5-domain sonographically \nbased approach. J Ultrasound Med. 2015;34(6):937-947. doi:10.7863/\nultra.34.6.937. \n 11. Ghai V, Jan H, Shakir F, Haines P, Kent A. Diagnostic delay for super -\nficial and deep endometriosis in the United Kingdom. J Obstet Gynaecol. \n2020;40(1):83-89. doi:10.1080/01443615.2019.1603217.\n 12. Reid S, Leonardi M, Lu C, Condous G. The association between  \nultrasound-based ‘soft markers’ and endometriosis type/location: a pros-\npective observational study. Eur J Obstet Gynecol Reprod Biol. 2019; \n234:171-178. doi: 10.1016/j.ejogrb.2019.01.018.\n 13. Menakaya U, Reid S, Lu C, Gerges B, Infante F, Condous G.  \nPerformance of ultrasound-based endometriosis staging system \n(UBESS) for predicting level of complexity of laparoscopic surgery for \nendometriosis. Ultrasound Obstet Gynecol. 2016;48(6):786-795. \ndoi:10.1002/uog.15858.","source_license":"CC0","license_restricted":false}