European society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis

Endometriosis is a common gynaecological condition of un- known aetiology that primarily affects women of reproductive age. The accepted first-line imaging modality is pelvic ultra- sound. However, magnetic resonance imaging (MRI) is in- creasingly performed as an additional investigation in complex cases and for surgical planning. There is currently no international consensus regarding patient preparation, MRI protocols or reporting criteria. Our aim was to develop clinical guidelines for MRI evaluation of pelvic endometriosis based on literature evidence and consensus expert opinion. This work was performed by a group of radiologists from the Electronic supplementary material The online version of this article (doi:10.1007/s00330-016-4673-z) contains supplementary material, which is available to authorized users. * M. Bazot [email protected] N. Bharwani [email protected] C. Huchon [email protected] K. Kinkel [email protected] T. M. Cunha [email protected] A. Guerra [email protected] L. Manganaro [email protected] L. Buñesch [email protected] A. Kido [email protected] K. Togashi [email protected] I. Thomassin-Naggara [email protected] A. G. Rockall [email protected] 1 Department of Radiology, Tenon Hospital, 58 Avenue Gambetta, Paris 75020, France 2 Department of Radiology, St Mary’s Hospital, Imperial College Healthcare NHS Trust, 3rd Floor Queen Elizabeth the Queen Mother Building, Praed Street, London W2 1NY , UK 3 Department of Obtetrics and Gynaecology, CHI Poissy Saint-Germain en Laye,V ersailles University France, 10 rue du champ Gaillard, 78300 Poissy, France 4 Institut de radiologie, Clinique des Grangettes, 7, chemin des Grangettes, CH 1224 Chêne-Bougeries, Switzerland 5 Serviço de Radiologia, Instituto Português de Oncologia de Lisboa Francisco Gentil, Rua Prof. Lima Basto, 1099-023 Lisboa, Portugal 6 Department of Radiology, Hospital da Luz, Lisbon, Portugal 7 Department of Radiological Sciences, Sapienza University of Rome, Vle. Regina Elena 324, 00162 Rome, Italy 8 Department of Radiology (Urogenital Section), Hospital Clínic Barcelona, Villarroel, 170, Barcelona 08036, Spain 9 Department of Diagnostic Radiology, Kyoto University Hospital, 54 Shogoin-Kawahara-cho, Sakyo-ku, Kyoto 606-8507, Japan 10 Department of Radiology, The Royal Marsden Hospital, Fulham Road, London SW3 6JJ, UK Eur Radiol (2017) 27:2765–2775 DOI 10.1007/s00330-016-4673-z European Society of Urogenital Radiology (ESUR), experts in gynaecological imaging and a gynaecologist expert in meth- odology. The group discussed indications for MRI, technical requirements, patient preparation, MRI protocols and criteria for the diagnosis of pelvic endometriosis on MRI. The expert panel proposed a final recommendation for each criterion using Oxford Centre for Evidence Based Medicine (OCEBM) 2011 levels of evidence. Key Points  This report provides guidelines for MRI in endometriosis.  Minimal and optimal MRI acquisition protocols are provided.  Recommendations are proposed for patient preparation , best MRI sequences and reporting criteria.

Endometriosis . Guidelines . Magnetic resonance imaging (MRI) . Protocols . Evidence-based Medicine/ standards Abbreviations 2D Two-dimensional 3D Three-dimensional DPE Deep pelvic endometriosis DWI Diffusion-weighted imaging ESUR European Society of Urogenital Radiology FPI- ESUR Female Pelvic Imaging working group of the European Society of Urogenital Radiology GPP Good practice point HASTE Half-Fourier acquisition single shot turbo-spin- echo IM Imtramuscular IV Intravenous LE Level of evidence MRI Magnetic resonance imaging OCEBM Oxford Centre for Evidence Based Medicine SC Subcutaneous SNR Signal-to-noise ratio SWI Susceptibility-weighted imaging T Tesla T1W T1-weighted T2W T2-weighted TVS Transvaginal sonography US Ultrasound

Endometriosis is a common gynaecological condition that is defined as functional ectopic endometrial glands and stroma outside the uterus. This disease affects women of reproductive age, with a prevalence of approximately 10% [ 1]. Patients can be asymptomatic or present with chronic pelvic pain and/or infertility. The combination of laparoscopy and histological verifi- cation of endometrial glands and/or stroma is considered to be the gold standard for diagnosis of the disease [ 2]. Ultrasonography (US) is the f irst-line imaging modal- ity for the assessment of pelvic endometriosis but has

with respect to field-of-view and operator dependence [ 3–8]. Magnetic resonance imaging (MRI) is usually performed as an additional examination in complex cases or prior to surgery and is highly accurate in the evaluation of endometriosis [ 9–18]. However, there is no international consensus on patient prepara- tion, best MRI sequences or reporting criteria. The aim of this work was to develop guidelines for optimal MRI protocols and image interpretation in en- dometriosis based on a detailed literature review and consensus expert opinion from the Female Pelvic Imaging working group of the European Society of Urogenital Radiology (FPI-ESUR).

MRI protocols for the diagnosis of pelvic endometriosis were collected from one non-European and seven European institutions. Inclusion criteria to participate in the guideline development process were: to be a mem- ber of the FPI-ESUR working group, and to perform regular MRI examinations and/or publications related to endometriosis. All but one investigators included in this guidelines process were experts in gynaecological imaging, the last being a gynaecologist expert in methodology. A questionnaire was established containing the following information: patient preparation, magnet field strength, type of coil, type of MRI sequences, use of intravenous contrast in- jection, and vaginal and/or rectal opacification. Published literature was reviewed through a Medline liter- ature search of abstracts in the English language of studies in human subjects, including the following keywords:‘endome- triosis’ and ‘MR imaging’ up to June 2015. Articles that did not include technical details matching the information request- ed in the questionnaire were excluded. The details were en- tered into an Excel spread sheet and the results discussed and divided into topics with agreement and disagreement. Topics with disagreement were compared to the literature. Experts in favour of one technical option were asked to support their views using data from the literature. The expert panel pro- posed a final recommendation for each criterion using Oxford Centre for Evidence Based Medicine (OCEBM) 2011 levels of evidence 2766 Eur Radiol (2017) 27:2765–2775 The summary of valid scientific data for each question analysed by the experts included a level of evidence (LE) based on the quality of available data and defined according to the rating scheme developed by the FrenchNational Authority for Health: LE1: high-power randomized comparative trials or meta- analyses of randomized comparative trials; LE2: low-power randomized trials, well-conducted non- randomized comparative studies and cohort studies; LE3: non-consecutive studies or studies without consis- tently applied reference standards; LE4: non-randomized comparative studies with substan- tial bias, retrospective studies, cross-sectional studies and case series. The practice guidelines were summarised from the re- sponses provided by the experts, and grades were attributed as follows: Grade A: established scientific evidence (LE1); Grade B: scientific presumption (LE2); Grade C: based on a low level of evidence (LE3 or LE4). Recommendations based on professional consensus were reduced to a minimum (Good Practice Point: GPP) and were used in the queries when liter- ature was lacking in evidence.

Indications for MRI in endometriosis No data exist in the literature about the indications for MR imaging for pelvic endometriosis: evaluation of pelvic pain, infertility or indeterminate adnexal mass. In accordance with the analysis performed in our different ESUR centres, more than 90% of MRI examinations are performed for staging deep pelvic endometriosis that is the main indication. Hence, an indeterminate adnexal mass represents an ancillary indica- tion of MR imaging. No consensus exists in the literature regarding the use of MRI in comparison to US. In practice, radiological papers tend to favour MRI whereas gynaecological publi- cations underline the value of US [ 19, 20]. This assess- ment is in line with recent published meta-analyses [21–24]. The first confirmed that transvaginal sonography (TVS) should remain the first-line method in the evalua- tion of patients with suspicion of deep pelvic endometri- osis (DPE) [ 21]. Two further meta-analyses demonstrated that the overall diagnostic performance of TVS for detect- ing DPE is fair but a high specificity is present for all locations [22, 23]. Based on the results of these meta- analyses, further investigat ions, especially MRI, are rec- ommended in a symptomatic patient in the presence of negative US findings (LE1) [ 22, 23]. Finally, an addition- al meta-analysis suggested that MRI is a useful preopera- tive test for predicting the diagnosis of multiple sites of DPE (LE1) [ 24]. In patients with equivocal US, MRI is recommended as a second-line technique in the preoperative workup of DPE (grade A). Technical requirements Technical requirements for each centre are presented in Table 1. A summary of literature review is provided for each specific criterion. Ta bl e 1 Technical requirements Paris London Geneva Lisbon Lisbon Roma Barcelona Kyoto Device (Tesla) 1.5 1.5/3.0 3.0 1.5 1.5/3.0 3.0 1.5/3.0 1.5/3.0 P ha sed -a rr ay Yes Yes Ye s Yes Ye s Ye s Ye s Ye s Endocavitary probe No No No No No No No No Timing of MRI No No > Day 8 No No No No No Fasting 3h No 6h 6h 4h 6h 4h 4h Special diet No No No No No No No No Bowel enema Y es No Y es No Y es Y es No No Bladder emptying 2h No No 2h 1h 1h No No IV catheter No (Option) Y es Y es Y es Y es Y es Y es No Anti-peristaltic agent SC IV IM IV IV IV IV SC Belt strapping Yes No Yes Yes No No No Yes V aginal opacification No No Yes* Yes* Ye s* No No No Rectal opacification No Y es Y es* Yes* Ye s* Ye s* No No S upi ne p osi tion Yes Yes Ye s Yes Ye s Ye s Ye s Ye s Prone position Y es** No No No No No No No IM intramuscular,IV intravenous, SC subcutaneous * If doubt or symptoms present (i.e. dyspareunia, dyschezia) ** If claustrophobic Eur Radiol (2017) 27:2765–2775 2767 1.5 Tesla versus 3.0 Tesla systems The majority of published studies use a 1.5T magnet. Only four publications used 3.0T but suggested promising results [11, 16, 25, 26]. At 3.0T, improved signal-to-noise ratio results in the acquisition of high-spatial resolution images and accu- rate depiction of all locations of DPE [ 11, 16, 25]. However, there is increased image heterogeneity at 3.0T when compared to 1.5T, which can have a negative effect on the fat-saturation techniques routinely utilised in the evaluation of endometri- osis [ 16, 27]. The application of the Dixon technique may overcome this and achieve stronger fat-suppression [27]. Both 1.5T and 3.0T seem valuable for the evaluation of DPE; however, studies comparing the systems are lacking. Therefore, no recommendation can be made for the use of a specific device and further work is necessary to perform this comparison (Fig. 1). Array type In line with different publications, pelvic phased-array coils provide a higher SNR than is possible with a body coil (LE3) [28, 29]. In addition, three studies have reported additional value of endocavitary coils in conjunction with pelvic phased-array [9, 30, 31]. Drawbacks in terms of cost and ac- ceptability limit its potential use in the evaluation of DPE. Pelvic phased array coils are recommended in the evalua- tion of DPE at both 1.5T and 3.0T (grade C). Timing of MRI examination Several studies reported discrepant results regarding timing of MRI evaluation. Fiaschetti et al. examined patients between days 8 and 12 of the menstrual cycle, due to the possibility of spontaneous T1W -signal intensity of blood prior to day 8 of the menstrual cycle [32]. Bazot et al. suggested that the pres- ence of pelvic free fluid (e.g. menstruation, post-ovulatory phase) is a useful aid to image interpretation (Fig. 2)[ 33, 34]. Tamai et al. reported that during menstruation the uterus can demonstrate marked pseudo-thickening of the junctional zone, suggesting an inappropriate diagnosis of adenomyosis [35]. They went on to suggest that MRI should be avoided in the menstrual phase [ 35]. In addition, these authors reported that the evaluation of uterine peristalsis is optimal during the peri-ovulatory phase [36]. Solak et al. reported no significant difference in size of lesions in the early days of menstruation compared to the mid-menstrual period for abdominal wall endometriosis [37]. Finally, Botterill et al. did not observe a significant difference in disease extent between menstruating and non-menstruating scans [38]. No recommendation can be proposed for timing of MRI in relation to the menstrual cycle in the evaluation of DPE. Patient preparation There was no consensus regarding patient preparation before MRI. The committee felt that the protocol should be tailored to the main indication for pelvic MRI (diagnosis/staging of DPE, indeterminate adnexal mass). Fasting When fasting prior to the MRI study was mentioned, the length of fast was variable at 3, 4 or 6 h (LE2) [ 16, 17, 19, 20, 32, 33, 39]. However, the majority of studies did not men- tion this pre-imaging preparation. Fasting is recommended in the evaluation of DPE (grade B). Bowel preparation Most studies did not mention the use of bowel preparation prior to pelvic MRI. Where authors advocated the use of bow- el preparation, the type of preparation varied. The most com- monly utilised method was bowel enema with either rectal suppository pills (e.g. bisacodyl) or water [39, 40]. In addition, there was variable use of dietary preparation, ranging from Fig. 1 Sagittal 2D T2-weighted MR images in the same patient performed at (a) 1.5 Tesla and (b) 3.0 Tesla provide similar good imaging quality for the evaluation of pelvic anatomy, especially uterine zonal anatomy. Note the quality of abdominal strapping on both 1.5 and 3.0 T examinations (arrows) 2768 Eur Radiol (2017) 27:2765–2775 nothing to low-residue diet 3 days prior to MRI accompanied by enema, magnesium sulphate and fluid re-hydration the day before the study [41]. Bowel preparation is advocated as ‘best practice’ for the detection of DPE (GPP) (Fig. 3). Bladder emptying No studies have been published in the medical literature addressing the importance of bladder distension for de- tection of anterior DPE. When bladder distension is discussed, authors describe a moderately filled or full bladder in order to correct the angle of uterine anteversion and thereby improve visualisation of the re- gion, allowing detection of small nodules located ante- rior to or in the vesicouterine pouch and to displace the bowel superiorly reducing artefact caused by bowel mo- tion (LE4) [ 12, 16, 39, 42–46]. Excessive bladder distension is not recommended as associated detrusor contractions may cause artefact and can complicate the identification of small pari etal nodules (LE4) (Fig. 3) [42, 44, 46]. To achieve the appropriate distension, au- thors mainly ask their patients not to empty their blad- der for 1 h prior to the examination [ 16, 39]. A moderately full bladder is recommended in the evalua- tion of DPE (grade C). Patient position All centres performed MRI with a patient in the supine position. A recent systematic review specifically looked at possible interventions aimed to reduce anxiety, distress and the need for sedation in adults undergoing MRI exams, and confirmed evidence for the benefit of prone scanning in reducing claus- trophobia (LE2) [47]. Fig. 2 Sagittal 2D T2-weighted MR images performed at 1.5 Tesla showing the benefits of anti- peristaltic agents on image quality. Imaging performed in the same patient before (a)a n da f t e r (b) administration of glucagon demonstrating a dramatic improvement in image quality. Note the presence of pelvic fluid in the pouch of Douglas underlining a clear demarcation between peritoneal and posterior subperitoneal compartments (double arrow) (reprinted with permission - Bazot M. Ed. Lavoisier-Paris 2016) Fig. 3 Sagittal 2D T2-weighted MR images performed at 1.5 Tesla showing the benefits of patient preparation on image quality. ( a) Imaging performed with a full urinary bladder and without bowel preparation is sub-optimal for int erpretation and disease may be overlooked. (b) MR imaging performed in a different patient following bowel preparation with Normacol and 2 h after emptying her urinary bladder. Note the superior image quality in ( b) and the large endometriotic lesion on the anterior rectosigmoid colon (arrows) Eur Radiol (2017) 27:2765–2775 2769 The supine position is recommended in the evaluation of pelvic endometriosis (GPP). The prone position is an ‘option’ in claustrophobia (grade B). Abdominal strapping A few papers recommend the use of a broad abdominal belt in MRI examinations for the evaluation of endometriosis (Fig.1) [34, 48, 49]. The purpose is to reduce artefact caused by re- spiratory movement and it has been recommended to apply the belt at the end of expiration (LE3) [ 50, 51]. Abdominal strapping is recommended in the evaluation of pelvic endometriosis (grade C). Anti-peristaltic agent The use of an anti-peristaltic agent (e.g. glucagon, butyl-sco- polamine), unless contraindicated (e.g. diabetes or phaeochromocytoma), is the most efficient way to limit bowel motion artefact (Fig. 2)( L E 4 )[52]. Recently, Gutzeit et al. suggested that intravenous spasmolysis is more reliable than intramuscular administration, and glucagon is better than butyl-scopolamine [52]. An anti-peristaltic agent is recommended in the evaluation of DPE (grade C). Vaginal opacif ication Four studies provided discrepant results on the value of vaginal opacification with gel in the diagnosis of posterior DPE (Fig.4) (LE4) [14, 32, 45, 53]. The first reported an improvement in sensitivity between pre- and post-contrast MRI in the diagnosis of DPE; however, this improvement was only significant for junior radiologists [45]. The second did not find any significant difference in the diagnosis of vaginal or rectal endometriosis with or without vaginal opacification, whatever the level of expertise of readers (LE4) [14]. The third reported better eval- uation for the detection of vagin al and uterosacral endometri- osis but not for pouch of Douglas or rectovaginal septum dis- ease (LE4) [32]. Finally, the most recent study reported a sig- nificant improvement in the diagnosis of pouch of Douglas obliteration in the presence of vaginal opacification (LE4) [53]. V aginal opacification with sonographic gel is considered as an ‘option’ in the evaluation of DPE (GPP). Rectal opacification No consensus exists in the literature on the value of rectal opacification in the diagnosis of DPE (Fig. 4). In practice, two different types of contrast medium are used (sonographic g e lo rw a t e r )[11, 14, 45, 53]. Discrepant results are available with some authors claiming that rectal opacification provides a better evaluation of pouch of Douglas and rectosigmoid colon endometriosis [32, 41, 43, 53], while several other stud- ies argued that this technique was useless in the evaluation of posterior DPE locations [10, 11, 14]. In this setting, different arguments against systematic rectal opacification are sug- gested including time, patient discomfort, movement artefact and rectosigmoid colon spasm [10]. Rectal opacification is suggested as an‘option’ in the eval- uation of pelvic endometriosis (GPP). Fig. 4 Sagittal 2D T2-weighted MR images performed in two different patients at 1.5 Tesla following vaginal and rectal opacification with sonographic gel and with ( a) or without ( b) bowel preparation. V aginal distension demonstrates thickening of the posterior vaginal fornix (white arrow) without involvement of the pouch of Douglas or rectum posteriorly that is clearly analysable ( a). V aginal and rectal opacification without bowel preparation cannot permit an accurate analysis of potential deep posterior endometriosis, especially potential rectal endometriosis (b) 2770 Eur Radiol (2017) 27:2765–2775 MRI protocol MRI sequences (T able2) There is significant variability in the literature regarding the MRI protocols used [11, 16–18, 31–33, 44, 45, 54–56]. T2-weighted MRI T2W MR sequences without fat-suppression technique are the best sequences for detecting pelvic endometriosis (LE2) [ 33]. Most MRI studies are performed using at least two orthogonal T2W planes [ 11, 16–18, 31–33, 44, 45, 54–56]. Further studies are required to clarify the field-of- view used for the axial acqui sition and which additional T2W MR plane should be used. Axial 2D-T2W MRI from renal hila to pubic bone, allowing a systematic visualisa- tion of kidneys and potential analysis of the right iliac fossa (i.e. caecum, appendix, small bowel) should be rec- ommended [ 33]. The use of thin section-oblique 2D-T2W imaging improves the success of conventional MRI (sag- ittal and axial) for assessment of uterosacral and parametrial endometriosis (LE3) [ 13, 15]. In addition, several authors have recently reported the potential value of 3D-T2W imaging in the evaluation of DPE [ 16, 54]. In contrast, no studies have demonstrated the value of coro- nal 2D-T2W MRI sequence in the evaluation of pelvic endometriosis. Three 2D-T2W MRI sequences (sagittal, axial, oblique) are recommended in the evaluation of DPE (grade B). The addition of 3D-T2W MRI sequence is proposed as an ‘option’ (grade C). T1-weighted MRI Several studies have underlined that T1W MRI is the gold standard for the diagnosis of endometriotic cysts (LE2) [ 57, 58]. The 2D or 3D Dixon technique providing four simulta- neous different T1W contrasts during the same acquisition and a stronger fat suppression in the female pelvis when com- pared to a 3D-FSPGR sequence should progressively become the reference technique (LE4) [58]. There has been no compar- ative study between conventional fat saturated T1W sequences and the Dixon technique in the identification of endometrial implant. The reduced spatial res olution of currently available Dixon techniques might prevent the identification of small peri- toneal implants compared to conventional fat-saturated T1W sequences. This hypothesis requires further research. Data are lacking for the evaluation of DPE using T1W MRI. Preliminary papers have suggested fat-suppressed T1W MRI to be of value in the diagnosis of peritoneal endometri- osis, but this finding must be confirmed [ 59, 60]. T1 W MRI sequences without and with fat suppression are recommended in the evaluation of adnexal endometriosis (grade B) The ‘Dixon technique’ may be used as an alternative to standard T1W sequence (grade C). Intravenous contrast-enhanced MRI Few data are available regarding the value of gadolinium in the evaluation of endometriosis. A clear distinction must be made regarding the indication for MRI (diagno- sis/staging of endometriosis/characterisation of US- indeterminate adnexal mass). Three studies reported data for the evaluation of different DPE locations [14, 61, 62]. Firstly, Onbas et al. suggested that Ta bl e 2 MRI sequences MRI sequence Paris London Geneva Lisbon Lisbon Roma Barcelona Kyoto 2DT2W sagittal Y es Y es Y es Y es Y es Y es Y es Y es 2DT2W axial LP * P* LP* LP* LP* P* P* P* 2DT2W coronal No No Y es No Y es Y es Y es No 2DT2W oblique Y es Y es Y es Y es Y es Y es No No 3DT2W Yes No No No No Yes No No T2 * No No No No No No No No SSFSE/Haste Y es No Y es No No No No Y es 2D/3D T1W 3D 2D 2D 2D 3D 3D 2D 2D T1W no FS § Yes Ye s Ye s Ye s Ye s Ye s Yes Yes T1W with FS§ Yes Ye s Ye s Ye s Ye s Ye s Yes Yes Gadolinium ± ± ± ± ± ± ± ± Peristalsis ± No No No No No No Yes DWI No No No No No Yes No Yes T1W T1-weighted, T2W T2-weighted, 2D two-dimensional,3D three-dimensional LP* : from renal hila to pubic bone P* : from iliac crests to pubic bone T2* : susceptibility-weighted MR sequence FS§ : fat-saturation technique Eur Radiol (2017) 27:2765–2775 2771 dynamic MRI could be useful to depict abdominal wall endo- metriosis [61]. Secondly, Scardapane et al. underlined that the combination of MR colonography and 3D-T1W MRI allows easier recognition of colorectal endometriosis and higher inter-observer agreement (LE3) [62]. Finally, Bazot et al. sug- gested the absence of benefit of intravenous gadolinium for the diagnosis of rectosigmoid colon, vaginal and bladder en- dometriosis, whatever the level of expertise of readers (LE3) (Fig. 5)[ 14]. These variable results contrast with the usefulness of gad- olinium when dealing with endometriotic adnexal masses. Using conventional T2W and T1W sequences, MRI has only moderate accuracy in distinction of endometrial cysts from other haemorrhagic adnexal lesions [63, 64]. The use of gad- olinium may help to distinguish an endometrioma from a lu- teal ovarian cyst or tubo-ovarian abscess displaying intense wall enhancement [ 65]. Moreover, gadolinium enhancement is crucial for depicting strongly enhancing mural nodules if Fig. 5 Sagittal 2D MR images performed at 1.5 Tesla demonstrating the use of sonographic gel to opacify and distend the vagina. (a) Sagittal 2D T2-weighted image demonstrating an endometriotic plaque involving the posterior vaginal fornix (white arrow). Following distension of the vagina with sonographic gel, the plaque is better delineated on both T2-weighted (b) and fat-suppressed T1-weighted (c ) sequences (white arrows) (reprinted with permission - Bazot M. Ed. Lavoisier-Paris) Fig. 6 Axial 2D MR images performed at 1.5 Tesla demonstrating the use of gadolinium in the diagnosis of indeterminate adnexal mass related to endometrial cyst complicated with clear cell carcinoma. (a) Axial 2D T2- weighted image demonstrates a large unilocular cyst containing papillary projections and/or solid portion (arrows). Axial without (b)a n dw i t h(c) fat-suppressed T1-weighted sequences display high signal content related to endometriotic fluid. Axial oblique dynamic contrast enhanced MR images (d) display location of region of interest (ROI) within external myometrium (M) and vegetation (V) and the initial increase in the signal intensity of solid tissue (arrow) that is steeper than that of myometrium (M), corresponding to a curve type 3 (V) highly suggestive of carcinoma confirmed at histopathological examination 2772 Eur Radiol (2017) 27:2765–2775 atypical features suggest potential malignancy on either ultra- sound (US) or T2W (LE4) (Fig. 6)[ 66, 67]. Finally, endome- triosis and pelvic inflammatory disease are two conditions that can be easily confused, especially in situations where they co- exist. Hence, the presence of a strong wall enhancement with- in adnexal masses is useful to suggest pelvic inflammatory disease (LE3) [65, 68]. No recommendation can be achieved regarding the use of gadolinium in the evaluation of DPE (Fig. 5). The use of gadolinium is recommended as an‘option’ in the evaluation of indeterminate adnexal endometriosis (grade C). Diffusion-weighted MRI (DWI) No data are available on DWI for the evaluation of DPE. Two recent studies have suggested its potential value in the evalu- ation of abdominal wall and sacral nerve root abnormalities endometriosis (LE4) [37, 69, 70]. A role for DWI has also been suggested in differentiation of endometriomas from haemorrhagic cysts with significantly lower ADC values in endometriomas when compared with haemorrhagic ovarian cysts at all b values [ 71]. No recommendation can be achieved for the use of DWI in the evaluation of DPE. Susceptibility-weighted MRI (SWI) Two recent studies using SWI suggest that the presence of signal voids reflecting acute to chronic haemorrhage are very sensitive in the diagnosis of extra-ovarian endometriosis, es- pecially abdominal wall endometriosis (LE4) [37, 72]. Endometriotic cysts contain blood degradation products secondary to recurrent cyclic bleeding from ectopic endome- trial tissue giving rise to punctate or curvilinear signal voids along the cyst wall on SWI [ 57, 73]. However, a pitfall of imaging with SWI is susceptibility artefact caused by intesti- nal gas, particularly at 3.0T. No recommendation can be proposed for the use of susceptibility-weighted MR imaging in the evaluation of deep endometriosis. Half-Fourier acquisition single shot turbo spin echo Half-Fourier acquisition single shot turbo-spin-echo (SSFSE, HASTE) enables multiphase and multislice image acquisition producing kinematic images for the evaluation of pelvic ad- hesions [74]. HASTE imaging is used to evaluate uterine function by assessing uterine peristalsis, identifiable as rhythmic and sub- tle wave-like endometrial and subendometrial myometrium movements [75–77]. During the peri-ovulatory phase, uterine peristalsis is significantly reduced in subjects with endometri- osis when compared to normal controls that may be due to increased, sustained contractions in endometriosis patients (LE4) [36, 78]. This abnormal uterine peristalsis in endome- triosis patients could interfere with fertility [79]. Half-Fourier acquisition single shot turbo spin echo is rec- ommended for the evaluation of uterine peristalsis (grade C). Reporting criteria A consensus exists in the ESUR group and in the literature about the criteria used in the diagnosis of endometrial cysts [57] and different locations of DPE [ 15, 33]( Appendix 1).

These recommendations argue that: 1. MRI should be considered as a second-line technique ex- amination after US in the evaluation of pelvic endometriosis 2. MRI is recommended before surgery for optimal preoper- ative staging 3. Some requirements for the acquisition of MR images have to be observed to provide optimal studies. Future research for the evaluation of endometriosis using MRI: 1. Patients with clinical suspicion and negative US 2. Intra-individual comparison between 1.5T and 3.0T 3. Management of medical treatment 4. Diagnostic performance without and with bowel prepara- tion to evaluate DPE 5. Evaluation of the clinical impact of MRI as a pre- operative test.

The committee would like to thank Mr Arnold Stipsits, ESUR secretary, for his help with co-ordination of the committee members. The scientific guarantor of this publication is Pr. Marc Bazot. The authors of this manuscript declare no relationships with any compa- nies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was not required because this manuscript pre- sents guidelines only and has not required the use of patient-sensitive data. Some study subjects or cohorts have not been previously reported. Methodology: Guidelines based on expert opinion and literature review Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Eur Radiol (2017) 27:2765–2775 2773

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