DSOG Guideline Bulletin: Diagnostic approach for patients with endometriosis

The aim of this guideline was to update an existing guideline from 2012. An update was evident due to the scientific progress and political focus on endometriosis in recent years. Based on recent evidence, we aimed to provide clinical recommendations for training and use of ultrasound, magnetic resonance imaging (MRI), computed tomography, and diagnostic scoring systems, as well as diagnostic considerations when evaluating patients suspected for endometriosis. Current literature was searched for consensus and discrepancies. A total of eight research questions were formulated to review different aspects, when diagnosing endometriosis. The level of evidence was graded according to the Oxford Centre for Evidence-based Medicine Levels of Evidence and up- or downgraded depending on the study quality. According to the current literature, no diagnostic imaging tool can replace histologic verification of endometriosis except ultrasound when diagnosing lesions in the abdominal wall. Skills for diagnosing endometriosis in the posterior compartment with transvaginal ultrasound (TVUS) can be achieved within 50-60 scans. TVUS seems equivalent to MRI when endometriosis is suspected in the vagina, the sacrouterine ligaments, the rectovaginal fascia, and the rectosigmoid. Additionally, ultrasound has a high sensitivity for diagnosing endometriotic lesions in the abdominal wall, while MRI seems superior for deep infiltrating endometriosis (DIE) in the bladder, the ureter, the lumbosacral plexus, lungs and oral segment of the colon starting from the rectosigmoid. No biomarkers are currently recommended for diagnosing endometriosis. When considering bowel involvement, 60-96% of DIE in the colon is localized in the rectum with decreasing rates in the oral segments with a prevalence of affected appendix of 2.6-4.1%. Measuring the distance from the anocutaneus transition to the nodule is feasible with TVUS. The most promising grading systems for endometriosis are the EFI, #ENZIAN and AAGL scoring systems. The level of evidence across studies ranged from 1b to 5. Article Details This work is licensed under a Creative Commons Attribution 4.0 International License. CC BY. The paper and it's contents belong to the author, and can be used by others when giving appropriate credit to the authors and the creator (DJOG). How to Cite

[1] S. Guerriero, G. Condous, T. van den Bosch, L. Valentin, F.P.G. Leone, D. Van Schoubroeck, C. Exacoustos, A.J.F. Installé, W.P. Martins, M.S. Abrao, G. Hudelist, M. Bazot, J.L. Alcazar, M.O. Gonçalves, M.A. Pascual, S. Ajossa, L. Savelli, R. Dunham, S. Reid, U. Menakaya, T. Bourne, S. Ferrero, M. Leon, T. Bignardi, T. Holland, D. Jurkovic, B. Benacerraf, Y. Osuga, E. Somigliana, D. Timmerman, Systematic approach to sonographic evaluation of the pelvis in women with suspected endometriosis, including terms, definitions and measurements: a consensus opinion from the International Deep Endometriosis Analysis (IDEA) group, Ultrasound Obstet. Gynecol. 48 (2016) 318–332. https://doi.org/10.1002/uog.15955. DOI: https://doi.org/10.1002/uog.15955 [2] DSOG Guideline: Behandling af endometriomer - hos kvinder UDEN aktuelt graviditetsønske, (2017). https://static1.squarespace.com/static/5467abcce4b056d72594db79/t/599eaca2cd0f68a0fd1c69e8/1503571107434/EndometriomUDENGraviditetsønske+udkast.pdf. [3] DSOG Guideline: Behandling af endometriomer - hos kvinder MED aktuelt graviditetsønske, (2017). https://static1.squarespace.com/static/5467abcce4b056d72594db79/t/599eaca2cd0f68a0fd1c69e8/1503571107434/EndometriomUDENGraviditetsønske+udkast.pdf. [4] DSOG guideline: Gynækologisk ultralyd. Systematisk undersøgelse og oplæring, (2020). https://static1.squarespace.com/static/5467abcce4b056d72594db79/t/6046833ab6bc6b305748cc1e/1615233858037/ULGuidelineDSOG.pdf. [5] V. Nisenblat, P.M.M. Bossuyt, C. Farquhar, N. Johnson, M.L. Hull, Imaging modalities for the non-invasive diagnosis of endometriosis, Cochrane Database Syst. Rev. 2016 (2016). https://doi.org/10.1002/14651858.CD009591.pub2. DOI: https://doi.org/10.1002/14651858.CD009591.pub2 [6] C.B. Wykes, T.J. Clark, K.S. Khan, Accuracy of laparoscopy in the diagnosis of endometriosis: A systematic quantitative review, BJOG An Int. J. Obstet. Gynaecol. 111 (2004) 1204–1212. https://doi.org/10.1111/j.1471-0528.2004.00433.x. DOI: https://doi.org/10.1111/j.1471-0528.2004.00433.x [7] C.M. Becker, A. Bokor, O. Heikinheimo, A. Horne, F. Jansen, L. Kiesel, K. King, M. Kvaskoff, A. Nap, K. Petersen, ESHRE guideline: endometriosis, Hum. Reprod. (2022) 1–26. [8] B. Gerges, W. Li, M. Leonardi, B.W. Mol, G. Condous, Meta-analysis and systematic review to determine the optimal imaging modality for the detection of bladder deep endometriosis, Eur. J. Obstet. Gynecol. Reprod. Biol. 261 (2021) 124–133. https://doi.org/10.1016/j.ejogrb.2021.04.030. DOI: https://doi.org/10.1016/j.ejogrb.2021.04.030 [9] F. Barra, C. Scala, E. Biscaldi, V.G. Vellone, M. Ceccaroni, C. Terrone, S. Ferrero, Ureteral endometriosis: A systematic review of epidemiology, pathogenesis, diagnosis, treatment, risk of malignant transformation and fertility, Hum. Reprod. Update. 24 (2018) 710–730. https://doi.org/10.1093/humupd/dmy027. DOI: https://doi.org/10.1093/humupd/dmy027 [10] S. Guerriero, L. Saba, M.A. Pascual, S. Ajossa, I. Rodriguez, V. Mais, J.L. Alcazar, Transvaginal ultrasound vs magnetic resonance imaging for diagnosing deep infiltrating endometriosis: systematic review and meta-analysis, Ultrasound Obstet. Gynecol. 51 (2018) 586–595. https://doi.org/10.1002/uog.18961. DOI: https://doi.org/10.1002/uog.18961 [11] T. Indrielle-Kelly, D. Fischerova, P. Hanuš, F. Frühauf, M. Fanta, P. Dundr, D. Lavu, D. Cibula, A. Burgetova, Early Learning Curve in the Assessment of Deep Pelvic Endometriosis for Ultrasound and Magnetic Resonance Imaging, Biomed Res. Int. 2020 (2020). https://doi.org/10.1155/2020/8757281. DOI: https://doi.org/10.1155/2020/8757281 [12] A. Hernández Gutiérrez, E. Spagnolo, P. Hidalgo, A. López, I. Zapardiel, R. Rodriguez, Magnetic resonance imaging versus transvaginal ultrasound for complete survey of the pelvic compartments among patients with deep infiltrating endometriosis, Int. J. Gynecol. Obstet. 146 (2019) 380–385. https://doi.org/10.1002/ijgo.12894. DOI: https://doi.org/10.1002/ijgo.12894 [13] A.M.G. Pereira, V.S.C. Brizon, N. Carvas Junior, M. de S.R. de Carvalho, E.M. Cuvero, A.M. Buehler, T. da V. Pereira, R.G.C. Lopes, Can Enhanced Techniques Improve the Diagnostic Accuracy of Transvaginal Sonography and Magnetic Resonance Imaging for Rectosigmoid Endometriosis? A Systematic Review and Meta-analysis, J. Obstet. Gynaecol. Canada. 42 (2020) 488-499.e4. https://doi.org/10.1016/j.jogc.2019.07.016. DOI: https://doi.org/10.1016/j.jogc.2019.07.016 [14] M.K. Aas-Eng, B. Dauser, M. Lieng, L.M. Diep, M. Leonardi, G. Condous, G. Hudelist, Transvaginal sonography accurately measures lesion-to-anal-verge distance in women with deep endometriosis of the rectosigmoid, Ultrasound Obstet. Gynecol. 56 (2020) 766–772. https://doi.org/10.1002/uog.21995. DOI: https://doi.org/10.1002/uog.21995 [15] C. Chapron, N. Chopin, B. Borghese, H. Foulot, B. Dousset, M.C. Vacher-Lavenu, M. Vieira, W. Hasan, A. Bricou, Deeply infiltrating endometriosis: Pathogenetic implications of the anatomical distribution, Hum. Reprod. 21 (2006) 1839–1845. https://doi.org/10.1093/humrep/del079. DOI: https://doi.org/10.1093/humrep/del079 [16] C. Chapron, A. Fauconnier, M. Vieira, H. Barakat, B. Dousset, V. Pansini, M.C. Vacher-Lavenu, J.B. Dubuisson, Anatomical distribution of deeply infiltrating endometriosis: Surgical implications and proposition for a classification, Hum. Reprod. 18 (2003) 157–161. https://doi.org/10.1093/humrep/deg009. DOI: https://doi.org/10.1093/humrep/deg009 [17] M. Piketty, N. Chopin, B. Dousset, A.E. Millischer-Bellaische, G. Roseau, M. Leconte, B. Borghese, C. Chapron, Preoperative work-up for patients with deeply infiltrating endometriosis: Transvaginal ultrasonography must definitely be the first-line imaging examination, Hum. Reprod. 24 (2009) 602–607. https://doi.org/10.1093/humrep/den405. DOI: https://doi.org/10.1093/humrep/den405 [18] R.S. da Cunha Araujo, S.B. Maia, J.D. Lúcio, M.D. de Lima, H.S.A.A. Ribeiro, P.A.A.G. Ribeiro, Mapping of endometriosis in patients with unilateral endometrioma, Med. (United States). 100 (2021). https://doi.org/10.1097/MD.0000000000026979. DOI: https://doi.org/10.1097/MD.0000000000026979 [19] P. Rousset, N. Peyron, M. Charlot, F. Chateau, F. Golfier, D. Raudrant, E. Cotte, S. Isaac, F. Réty, P.J. Valette, Bowel endometriosis: Preoperative diagnostic accuracy of 3.0-T MR enterography-initial results, Radiology. 273 (2014) 117–124. https://doi.org/10.1148/radiol.14132803. DOI: https://doi.org/10.1148/radiol.14132803 [20] M.S. Abrão, J.A. Dias, G.P. Rodini, S. Podgaec, M.A. Bassi, M. Averbach, Endometriosis at several sites, cyclic bowel symptoms, and the likelihood of the appendix being affected, Fertil. Steril. 94 (2010) 1099–1101. https://doi.org/10.1016/j.fertnstert.2009.10.031. DOI: https://doi.org/10.1016/j.fertnstert.2009.10.031 [21] M. Mabrouk, D. Raimondo, M. Mastronardi, I. Raimondo, S. Del Forno, A. Arena, N. Sutherland, A. Borgia, G. Mattioli, P. Terzano, R. Seracchioli, Endometriosis of the Appendix: When to Predict and How to Manage—A Multivariate Analysis of 1935 Endometriosis Cases, J. Minim. Invasive Gynecol. 27 (2020) 100–106. https://doi.org/10.1016/j.jmig.2019.02.015. DOI: https://doi.org/10.1016/j.jmig.2019.02.015 [22] R.L. Gustofson, N. Kim, S. Liu, P. Stratton, Endometriosis and the appendix: a case series and comprehensive review of the literature, Fertil. Steril. 86 (2006) 298–303. https://doi.org/10.1016/j.fertnstert.2005.12.076. DOI: https://doi.org/10.1016/j.fertnstert.2005.12.076 [23] J.D. Horton, K.J. DeZee, E.P. Ahnfeldt, M. Wagner, Abdominal wall endometriosis: a surgeon’s perspective and review of 445 cases, Am. J. Surg. 196 (2008) 207–212. https://doi.org/10.1016/j.amjsurg.2007.07.035. DOI: https://doi.org/10.1016/j.amjsurg.2007.07.035 [24] J.H.J. Hensen, A.C. Van Breda Vriesman, J.B.C.M. Puylaert, Abdominal wall endometriosis: Clinical presentation and imaging features with emphasis on sonography, Am. J. Roentgenol. 186 (2006) 616–620. https://doi.org/10.2214/AJR.04.1619. DOI: https://doi.org/10.2214/AJR.04.1619 [25] S.E. Allen, N.B. Rindos, S. Mansuria, Abdominal wall endometriosis: an update in diagnosis, perioperative considerations and management, Curr. Opin. Obstet. Gynecol. 33 (2021) 288–295. https://doi.org/10.1097/GCO.0000000000000714. DOI: https://doi.org/10.1097/GCO.0000000000000714 [26] C. Nezhat, S.R. Lindheim, L. Backhus, M. Vu, N. Vang, A. Nezhat, C. Nezhat, Thoracic endometriosis syndrome: A review of diagnosis and management, J. Soc. Laparoendosc. Surg. 23 (2019). https://doi.org/10.4293/JSLS.2019.00029. DOI: https://doi.org/10.4293/JSLS.2019.00029 [27] S. Korom, H. Canyurt, A. Missbach, D. Schneiter, M.O. Kurrer, U. Haller, P.J. Keller, M. Furrer, W. Weder, Catamenial pneumothorax revisited: Clinical approach and systematic review of the literature, J. Thorac. Cardiovasc. Surg. 128 (2004) 502–508. https://doi.org/10.1016/j.jtcvs.2004.04.039. DOI: https://doi.org/10.1016/S0022-5223(04)00772-X [28] M.J. Ciudad, N. Santamaría, A. Bustos, J. Ferreirós, B. Cabeza, A. Gómez, Imaging findings in catamenial pneumothorax, Radiologia. 49 (2007) 263–267. https://doi.org/10.1016/S0033-8338(07)73768-2. DOI: https://doi.org/10.1016/S0033-8338(07)73768-2 [29] H. V. Posniak, A. Keshavarzian, R. Jabamoni, Diaphragmatic endometriosis: CT and MR findings, Gastrointest. Radiol. 15 (1990) 349–351. https://doi.org/10.1007/BF01888817. DOI: https://doi.org/10.1007/BF01888817 [30] G. Picozzi, D. Beccani, F. Innocenti, M. Grazzini, M. Mascalchi, MRI features of pleural endometriosis after catamenial haemothorax, BMJ Case Rep. (2009) 2–4. https://doi.org/10.1136/bcr.09.2008.0903. DOI: https://doi.org/10.1136/bcr.2006.071415 [31] J. Rangunwala, J. Sitta, K. Vyas, M. Roda, Multimodality Thoracoabdominal Imaging Findings in a Rare Case of Thoracic Endometriosis Syndrome, Cureus. 12 (2020) 1–9. https://doi.org/10.7759/cureus.6819. DOI: https://doi.org/10.7759/cureus.6819 [32] T. Sanada, J. Park, M. Hagiwara, N. Ikeda, T. Nagai, J. Matsubayashi, K. Saito, CT and MRI findings of bronchopulmonary endometriosis: a case presentation, Acta Radiol. Open. 7 (2018) 205846011880116. https://doi.org/10.1177/2058460118801164. DOI: https://doi.org/10.1177/2058460118801164 [33] P. Rousset, C. Rousset-Jablonski, M. Alifano, A. Mansuet-Lupo, J.N. Buy, M.P. Revel, Thoracic endometriosis syndrome: CT and MRI features, Clin. Radiol. 69 (2014) 323–330. https://doi.org/10.1016/j.crad.2013.10.014. DOI: https://doi.org/10.1016/j.crad.2013.10.014 [34] A.C. Siquara De Sousa, S. Capek, K.K. Amrami, R.J. Spinner, Neural involvement in endometriosis: Review of anatomic distribution and mechanisms, Clin. Anat. 28 (2015) 1029–1038. https://doi.org/10.1002/ca.22617. DOI: https://doi.org/10.1002/ca.22617 [35] B. Gui, A.L. Valentini, V. Ninivaggi, M. Miccò, V. Zecchi, P.P. Grimaldi, F. Cambi, M. Guido, L. Bonomo, Shining light in a dark landscape: MRI evaluation of unusual localization of endometriosis, Diagnostic Interv. Radiol. 23 (2017) 272–281. https://doi.org/10.5152/dir.2017.16364. DOI: https://doi.org/10.5152/dir.2017.16364 [36] C. Bourgioti, O. Preza, E. Panourgias, K. Chatoupis, A. Antoniou, M.E. Nikolaidou, L.A. Moulopoulos, MR imaging of endometriosis: Spectrum of disease, Diagn. Interv. Imaging. 98 (2017) 751–767. https://doi.org/10.1016/j.diii.2017.05.009. DOI: https://doi.org/10.1016/j.diii.2017.05.009 [37] L.P. Chamié, D.M.F.R. Ribeiro, D.A. Tiferes, A.C. De Macedo Neto, P.C. Serafini, Atypical sites of deeply infiltrative endometriosis: Clinical characteristics and imaging findings, Radiographics. 38 (2018) 309–328. https://doi.org/10.1148/rg.2018170093. DOI: https://doi.org/10.1148/rg.2018170093 [38] P. Lomoro, I. Simonetti, A. Nanni, R. Cassone, F. Di Pietto, G. Vinci, M.S. Prevedoni, S. Romano, L. Sammarchi, Extrapelvic Sciatic Nerve Endometriosis, the Role of Magnetic Resonance Imaging: Case Report and Systematic Review, J. Comput. Assist. Tomogr. 43 (2019) 976–980. https://doi.org/10.1097/RCT.0000000000000916. DOI: https://doi.org/10.1097/RCT.0000000000000916 [39] D.F. O, I. Flores, E. Waelkens, T. D’Hooghe, Noninvasive diagnosis of endometriosis: Review of current peripheral blood and endometrial biomarkers, Best Pract. Res. Clin. Obstet. Gynaecol. 50 (2018) 72–83. https://doi.org/10.1016/j.bpobgyn.2018.04.001. DOI: https://doi.org/10.1016/j.bpobgyn.2018.04.001 [40] H. Greenbaum, B.E.L. Galper, D.H. Decter, V.H. Eisenberg, Endometriosis and autoimmunity: Can autoantibodies be used as a non-invasive early diagnostic tool?, Autoimmun. Rev. 20 (2021) 102795. https://doi.org/10.1016/j.autrev.2021.102795. DOI: https://doi.org/10.1016/j.autrev.2021.102795 [41] M. Hirsch, J.M.N. Duffy, C.J. Davis, M. Nieves Plana, K.S. Khan, Diagnostic accuracy of cancer antigen 125 for endometriosis: a systematic review and meta-analysis, BJOG An Int. J. Obstet. Gynaecol. 123 (2016) 1761–1768. https://doi.org/10.1111/1471-0528.14055. DOI: https://doi.org/10.1111/1471-0528.14055 [42] T. American, F. Society, Revised American Fertility Society classification of endometriosis: 1985., Fertil. Steril. 43 (1985) 351–352. https://doi.org/10.1016/s0015-0282(16)48430-x. DOI: https://doi.org/10.1016/S0015-0282(16)48430-X [43] A.S. for R. Medicine, Revised American Society for Reproductive Medicine classification of endometriosis: 1996, Water Supply. 18 (2000) 298–299. https://doi.org/10.5363/tits.21.6_102. DOI: https://doi.org/10.5363/tits.21.6_102 [44] S. Vesali, M. Razavi, M. Rezaeinejad, A. Maleki-Hajiagha, S. Maroufizadeh, M. Sepidarkish, Endometriosis fertility index for predicting non-assisted reproductive technology pregnancy after endometriosis surgery: a systematic review and meta-analysis, BJOG An Int. J. Obstet. Gynaecol. 127 (2020) 800–809. https://doi.org/10.1111/1471-0528.16107. DOI: https://doi.org/10.1111/1471-0528.16107 [45] I. Thomassin-Naggara, S. Lamrabet, A. Crestani, A. Bekhouche, C.A. Wahab, E. Kermarrec, C. Touboul, E. Daraï, Magnetic resonance imaging classification of deep pelvic endometriosis: Description and impact on surgical management, Hum. Reprod. 35 (2020) 1589–1600. https://doi.org/10.1093/humrep/deaa103. DOI: https://doi.org/10.1093/humrep/deaa103 [46] E. Montanari, A. Bokor, G. Szabó, W. Kondo, C.H. Trippia, M. Malzoni, A. Di Giovanni, H.R. Tinneberg, A. Oberstein, R.M. Rocha, M. Leonardi, G. Condous, H. Alsalem, J. Keckstein, G. Hudelist, Accuracy of sonography for non-invasive detection of ovarian and deep endometriosis using #Enzian classification: prospective multicenter diagnostic accuracy study, Ultrasound Obstet. Gynecol. 59 (2022) 385–391. https://doi.org/10.1002/uog.24833. DOI: https://doi.org/10.1002/uog.24833 [47] M.S. Abrao, M.P. Andres, C.E. Miller, J.A. Gingold, M. Rius, J.S. Neto, F. Carmona, AAGL 2021 Endometriosis Classification: An Anatomy-based Surgical Complexity Score, J. Minim. Invasive Gynecol. 28 (2021) 1941-1950.e1. https://doi.org/10.1016/j.jmig.2021.09.709. DOI: https://doi.org/10.1016/j.jmig.2021.09.709 [48] V.H. Eisenberg, J.L. Alcazar, N. Arbib, E. Schiff, R. Achiron, M. Goldenberg, D. Soriano, Applying a statistical method in transvaginal ultrasound training: lessons from the learning curve cumulative summation test (LC-CUSUM) for endometriosis mapping, Gynecol. Surg. 14 (2017). https://doi.org/10.1186/s10397-017-1022-4. DOI: https://doi.org/10.1186/s10397-017-1022-4 [49] M. Bazot, E. Daraï, D.J. Biau, M. Ballester, L. Dessolle, Learning curve of transvaginal ultrasound for the diagnosis of endometriomas assessed by the cumulative summation test (LC-CUSUM), Fertil. Steril. 95 (2011) 301–303. https://doi.org/10.1016/j.fertnstert.2010.08.033. DOI: https://doi.org/10.1016/j.fertnstert.2010.08.033 [50] S. Guerriero, M.A. Pascual, S. Ajossa, I. Rodriguez, M. Zajicek, M. Rolla, N. Rams Llop, V. Yulzari, R. Bardin, F. Buonomo, O. Comparetto, M. Perniciano, L. Saba, V. Mais, J.L. Alcazar, Learning curve for ultrasonographic diagnosis of deep infiltrating endometriosis using structured offline training program, Ultrasound Obstet. Gynecol. 54 (2019) 262–269. https://doi.org/10.1002/uog.20176. DOI: https://doi.org/10.1002/uog.20176 [51] A. Tammaa, N. Fritzer, G. Strunk, A. Krell, H. Salzer, G. Hudelist, Learning curve for the detection of pouch of Douglas obliteration and deep infiltrating endometriosis of the rectum, Hum. Reprod. 29 (2014) 1199–1204. https://doi.org/10.1093/humrep/deu078. DOI: https://doi.org/10.1093/humrep/deu078 [52] S. Piessens, M. Healey, P. Maher, J. Tsaltas, L. Rombauts, Can anyone screen for deep infiltrating endometriosis with transvaginal ultrasound?, Aust. New Zeal. J. Obstet. Gynaecol. 54 (2014) 462–468. https://doi.org/10.1111/ajo.12242. DOI: https://doi.org/10.1111/ajo.12242 [53] M. Leonardi, J. Ong, M. Espada, N. Stamatopoulos, E. Georgousopoulou, G. Hudelist, G. Condous, One‐Size‐Fits‐All Approach Does Not Work for Gynecology Trainees Learning Endometriosis Ultrasound Skills, J. Ultrasound Med. 39 (2020) 2295–2303. https://doi.org/10.1002/jum.15337. DOI: https://doi.org/10.1002/jum.15337 [54] U. Menakaya, F. Infante, C. Lu, C. Phua, A. Model, F. Messyne, M. Brainwood, S. Reid, G. Condous, Interpreting the real-time dynamic ‘sliding sign’ and predicting pouch of Douglas obliteration: an interobserver, intraobserver, diagnostic-accuracy and learning-curve study, Ultrasound Obstet. Gynecol. 48 (2016) 113–120. https://doi.org/10.1002/uog.15661. DOI: https://doi.org/10.1002/uog.15661