Fusion imaging for evaluation of deep infiltrating endometriosis: feasibility and preliminary results

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1 Ultrasound Obstet Gynecol 2015; 46: Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: /uog Fusion imaging for evaluation of deep infiltrating endometriosis: feasibility and preliminary results A.-E. MILLISCHER*, L. J. SALOMON, P. SANTULLI, B. BORGHESE, B. DOUSSET ** and C. CHAPRON *Radiology, Centre de Radiologie Bachaumont IMPC-Paris, Paris, France; Hôpital Universitaire Necker-Enfants Malades, AP-HP, Université Paris Descartes, Maternité; Société Française pour l Amélioration des Pratiques Echographiques, SFAPE, Paris, France; Université Paris Descartes, Sorbone Paris Cité, Faculté de Médecine, Assistance Publique Hôpitaux de Paris (AP-HP), Groupe Hospitalier Universitaire (GHU) Ouest, Centre Hospitalier Universitaire (CHU) Cochin, Department of Gynecology Obstetrics II and Reproductive Medicine, Paris, France; Gynecology, Institut Cochin, Université Paris Descartes, CNRS (UMR 8104), Inserm, Unité de Recherche U1016, Paris, France; Gynecology, Université Paris Descartes, Faculté de Médecine, EA 1833, ERTi, AP-HP, CHU Cochin, Paris, France; **Service de Chirurgie Viscerale Hopital Cochin-Paris, Paris, France KEYWORDS: fusion; MRI; real-time virtual sonography; RVS; TVS ABSTRACT Objective Magnetic resonance imaging (MRI) and ultrasound scanning complement each other in screening for and diagnosis of endometriosis. Fusion imaging, also known as real-time virtual sonography, is a new technique that uses magnetic navigation and computer software for the synchronized display of real-time ultrasound and multiplanar reconstructed MR images. Our aim was to evaluate the feasibility and ability of fusion imaging to assess the main anatomical sites of deep infiltrating endometriosis (DIE) in patients with suspected active endometriosis. Methods This prospective study was conducted over a 1-month period in patients referred to a trained radiologist for an ultrasound-based evaluation for endometriosis. Patients with a prior pelvic MRI examination within the past year were offered fusion imaging, in addition to the standard evaluation. All MRI examinations were performed on a 1.5-T MRI machine equipped with a body phased-array coil. The MRI protocol included acquisition of at least two fast spin-echo T2-weighted orthogonal planes. The Digital Imaging Communications in Medicine dataset acquired at the time of the MRI examination was loaded into the fusion system and displayed together with the ultrasound image on the same monitor. The sets of images were then synchronized manually using one plane and one anatomical reference point. The ability of this combined image to identify and assess the main anatomical sites of pelvic endometriosis (uterosacral ligaments, posterior vaginal fornix, rectum, ureters and bladder) was evaluated and compared with that of standard B-mode ultrasound and MRI. Results Over the study period, 100 patients were referred for ultrasound examination because of endometriosis. Among them were 20 patients (median age, 35 (range, 27 49) years) who had undergone MRI examination within the past year, with a median (range) time interval between MRI and ultrasound examination of 171 (1 350) days. All 20 patients consented to undergo additional evaluation by fusion imaging. However, in three (15%) cases, fusion imaging was not technically possible because of changes since the initial MRI examination resulting from either interval surgery (n = 2; 10%) or pregnancy (n = 1; 5%). Data acquisition, matching and fusion imaging were performed in under 10 min in each of the other 17 cases. The overall ability of each technique to identify and assess the main anatomical landmarks of endometriosis was as follows: uterosacral ligaments: ultrasound, 88% (30/34); MRI, 100% (34/34); fusion imaging, 100% (34/34); posterior vaginal fornix: ultrasound, 88% (30/34); MRI, 100% (34/34); fusion imaging, 100% (34/34); rectum: ultrasound, 100% (17/17); MRI, 82.3% (14/17); fusion imaging, 100% (17/17); ureters: ultrasound, 0%; MRI, 100% (34/34); fusion imaging, 100% (34/34); and bladder: ultrasound, 100%; MRI, 100%; fusion imaging, 100%. Conclusion Fusion imaging is feasible for the assessment of endometriotic lesions. Because it combines information from both ultrasound and MRI techniques, fusion imaging allows better identification of the main anatomical sites of DIE and has the potential to improve the performance of ultrasound and MRI examination. Copyright 2014 ISUOG. Published by John Wiley & Sons Ltd. Correspondence to: Dr A.-E. Millischer, Radiology, Centre de Radiologie Bachaumont IMPC-Paris, Necker Hospital, 149 rue de Sèvres Paris 75015, France ( aemillischer@gmail.com) Accepted: 21 October 2014 Copyright 2014 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER

2 110 Millischer et al. INTRODUCTION Endometriosis is defined as the presence of ectopic endometrial glands and stromata outside the uterus. In deep infiltrating endometriosis (DIE), which affects up to 30% of women with endometriosis, nodules from the endometriosis penetrate into the retroperitoneal space or pelvic organ walls to a depth of at least 5 mm 1. DIE is thought to contribute to female pelvic pain and infertility 2 4. The main pelvic DIE locations are the uterosacral ligaments (USL), rectosigmoid colon, vagina, ureters and bladder. Solving the problem of accurate presurgical evaluation of endometriosis is critical to the provision of accurate planning of treatment and counseling of patients 5,6. In recent years, a number of publications have attempted to address this by analyzing the diagnostic performance of transvaginal sonography (TVS) and magnetic resonance imaging (MRI), the two non-invasive methodologies most frequently used for the diagnosis of DIE Numerous studies have demonstrated the usefulness of TVS as a first-line technique, owing to its widespread availability and cost effectiveness 6,12,13,17,18.Moreover, TVS allows for a dynamic examination, which can be useful for the diagnosis of adhesions 19. However, TVS suffers from high interobserver variability in the diagnosis of pelvic endometriosis, and its performance is highly dependent on the sonographer s experience 20.Incontrast,MRI provides visualization of the whole pelvis, with a larger field of view and excellent tissue contrast resolution 21. The diagnosis of DIE, therefore, might benefit from using a combination of MRI and real-time ultrasound. MRI and ultrasound fusion technology, also known as real-time virtual sonography (RVS), was recently introduced to the medical field and has been used successfully for the diagnosis and treatment of tumors It has also been used recently in obstetrics for prenatal imaging 32. This technology uses computer software to provide a synchronized display of real-time ultrasound images and multiplanar reconstruction images from MRI that correspond to the image plane of the real-time ultrasound. This study was undertaken to evaluate the feasibility and ability of fusion imaging in assessing the main anatomical sites of endometriosis in patients with suspected active endometriosis. METHODS This was a prospective study of women with suspected endometriosis referred for TVS. It was conducted over a 1-month period (February 2013) in a referral center, employing a single radiologist (A.E.M.) with a high level of expertise in gynecological ultrasonography (7 years of referral practice and a mean of 1800 scans/year). Patients who had undergone MRI within the previous 12 months were asked to participate in the study. All pelvic MRI examinations were performed on a 1.5-T MRI machine (Sonata, Siemens, Erlangen, Germany). The patient was placed in a supine position, in a phased-array coil. All sequences were performed with saturation bands placed anteriorly and posteriorly to eliminate artifacts from the high subcutaneous fat signal. The patients fasted for 3 hours beforehand, and received a bowel preparation (Microlax : sorbitol, citrate and sodium lauryl sulfoacetate) 12 hours before the MRI. No antiperistaltic drugs were administered. The acquisition protocols, including sequences, parameters and slice thicknesses, are listed in Table 1. Routine MRI protocols did not include three-dimensional (3D) acquisition. All ultrasound procedures, conventional TVS and fusion imaging, were performed with no time constraints, using the same Hitachi Aloka Ascendus (Hitachi, EZU-RV7) ultrasound system and the same two-dimensional probe (EUP-V53W 6 9-MHz transvaginal transducer). The fusion imaging system (Hitachi-Aloka Ascendus fusion imaging software with position sensor unit and magnetic sensor unit for fusion imaging (EZU-RV3S)) comprised a position-sensing unit mounted on the ultrasound unit, a magnetic field transmitter and a sensor fixed to the probe using a specific bracket (Figure 1). The magnetic field transmitter was placed near the area of Table 1 Parameters for magnetic resonance imaging sequences T2 Turbo SE sequence GRE sequence 2D-TRUFI SS Parameter Sagittal Transverse Transverse T1 Transverse T1 FS Coronal TR (ms) TE (ms) ,8 2, Echo train length Flip angle (degrees) FOV (mm) Matrix Signals acquired (n) Sections (n) Acquisition times (s) For all sequences, the section thickness was 4 mm and the section gap was 1 mm. 2D, two-dimensional; FOV, field of view; FS, fat saturation; GRE, gradient echo; SE, spin echo; SS, single shot; T1, T1-weighted; T2, T2-weighted; TE, echo time; TR, repetition time; TRUFI, true fast imaging with steady state free precession.

3 Fusion imaging of endometriosis 111 Transmitter Attachment Orientation mark of magnetic position sensor Orientation mark of magnetic position sensor Magnetic position sensor Flexible magnetic transmitter stand Figure 1 Schematic diagram of the ultrasound unit, showing the magnetic field transmitter and a sensor fixed to the probe by a specific bracket. scanning. During scanning, the magnetic tracking system determined the position and movement of the moveable sensor fixed to the probe, within a defined operating volume; displacement of the probe had to remain within cm of the magnetic field transmitter. Orientation and position data were transmitted to the ultrasound system for computation with the MRI data. The DICOM (Digital Imaging Communications in Medicine) datasets (axial and sagittal acquisitions) from the previous MRI examination were loaded into the ultrasound system using a CD-R (recordable compact disc). To visualize the two imaging modalities simultaneously, it was necessary to define common reference points between the MRI and ultrasound images. Since the position of the uterus could be slightly different between the MRI acquisition and ultrasound scan, we used a one-point method with subsequent adjustments. In practice, it was possible at any time to simply realign the two imaging modalities by freezing the MRI image when visualizing a characteristic plane, scanning the patient to find the same ultrasound plane, and pressing an adjustment key to start simultaneous visualization of both modalities (or the converse: first freezing the ultrasound image and then finding the corresponding MRI view). To facilitate the procedure, up to four MRI sequences could be loaded simultaneously during the fusion imaging procedure. The ultrasound system automatically converts each sequence in a volume of data and all constructed volumes are spatially synchronized. During the procedure, it is easy to move from one volume to another simply by pressing a key, without having to resynchronize. Thus, optimal image quality can be maintained. A single radiologist (A.E.M.) evaluated prospectively the feasibility of assessing, with each of the three techniques (TVS, MRI and fusion imaging), the five main pelvic anatomical locations that are affected by DIE: the USL, posterior vaginal fornix (PVF), rectum, ureters and bladder. A location was judged to have been assessed successfully by a technique when the examination allowed for appropriate evaluation of the related landmarks (pathological or otherwise), based on previously published criteria for TVS and MRI (Table 2). Institutional review board approval was not required because this study had no impact on the routine management of the patients care. However, information about the study was provided and oral consent was sought prior to all examinations. RESULTS Over the 1-month study period, 100 patients were referred for a TVS-based assessment for endometriosis, including 20 patients with a prior MRI examination within the past year. These patients were asked to undergo fusion imaging examination, and all consented to do so. The mean ± SD age and median (range) of the 20 patients were 36.2 ± 6.9 years and 35 (27 49) years. The median (range) time interval between fusion imaging and MRI examinations was 171 (1 350) days. Baseline patient characteristics are summarized in Table 3. The primary indications for MRI were dysmenorrhea (n = 20) associated with dyschezia (n = 16) and/or dyspareunia (n = 18) and infertility (n = 14). The primary indication

4 112 Millischer et al. Table 2 Published deep infiltrating endometriosis diagnostic criteria for transvaginal ultrasound (TVS) and magnetic resonance imaging (MRI) TVS 9,11,33 MRI 5,21 Normal Pathological Normal Pathological USL Smooth linear structure Irregular nodule Hypointense on T2; Fibrotic thickening smooth linear structure PVF Thickness < 4 mm Thickness > 4 mm Thickness < 4 mm Thickness > 4mm Rectum/sigmoid Hypoechogenic, regular wall Hypoechogenic mass Hypointense on T2; layers thin and regular Hypointense on T2; fibrotic mass throughout anterior wall Bladder Regular wall Hypoechogenic nodule Hypointense on T2; linear and regular serosa Hypointense nodule on T2 Ureters Hypoechogenic, thin linear structure USL, uterosacral ligaments; PVF, posterior vaginal fornix. Dilated, fluid-fed structure Thin and hypointense on T2; linear structure Thickened linear structure with hypointense spicular nodule on T2 Table 3 Baseline characteristics of patients (n = 20) with suspected active endometriosis undergoing real-time virtual sonography Characteristic Mean ± SD or n (%) Age (years) 36.2 ± 6.9 Body mass index (kg/m 2 ) ± 5.02 Parity 0.64 ± 1.03 Gravidity 1.27 ± 1.56 Infertility 14 (70) Dysmenorrhea 20 (100) Dyschezia 16 (80) Dyspareunia 18 (90) for the ultrasound examination was DIE screening (n = 20). Four (20%) patients underwent surgery within 2 months after the fusion imaging examination. Data acquisition, matching of landmarks and fusion imaging occurred in under 10 min in 17 (85%) cases. Fusion imaging was not feasible for three patients: in the intervening time between MRI and TVS, two (10%) had undergone a surgical procedure and in one the uterine position had changed (from anteflexed to retroflexed uterus) due to pregnancy. Matching landmarks had to be identified clearly in both MRI and ultrasound images. This was achieved using standardized planes of the female pelvis (sagittal and axial) on T2-weighted MRI. Following the appropriate adjustments of both images, volume navigation was achieved in all cases. Fusion imaging allowed superimposition of the MRI and ultrasound images, providing a combination of real-time imaging capabilities with high tissue contrast (Figures 2 6 and Videoclip S1). It also allowed addition of real-time Doppler signals to the MRI images. The mean± SD increased duration of the TVS examination due to the additional time required for fusion imaging was 10 ± 5 min. Table 4 compares assessment by TVS, MRI and fusion imaging of each of the five anatomical sites of DIE (USL, PVF, rectum, ureters and bladder). DISCUSSION This study demonstrates that fusion imaging improves visualization of the main pelvic anatomical sites of endometriotic lesions. The goal of this technique is to combine the dynamic, real-time qualities of TVS with the accuracy and tissue contrast capability of MRI 33.This is particularly relevant for endometriotic evaluations, because TVS and MRI complement each other well in examination of this pathology. TVS is an effective diagnostic method and the first-line tool of investigation when endometriosis is suspected 6,12,16,34,35. It is available widely, simple to perform and safe. It also provides high spatial resolution and real-time imaging. However, expert sonographers are needed to perform TVS; endometriotic screening requires a lot of experience and the learning curve may be long 18.In particular, TVS evaluation of some anatomical structures, such as the USL, vaginal fornix and ureters, is difficult. This has been reported by several authors 14,18,20 and is underscored by the results from our study. In contrast, MRI has gained increasing importance because of its higher inter- and intraobserver agreement and better detection of endometriotic nodules in areas that are poorly evaluated by TVS 33,36. High-contrast tissue resolution enables powerful analysis of the urinary tract 37. Although the accuracy of detection of endometriosis by MRI increases with the radiologist s expertise 34,35,MRIis considered a less biased, more reproducible modality than is TVS, and can be performed even in the absence of an expert operator 36,38. It also has fewer technical limitations than does TVS (e.g. in obese women and virgin patients). Finally, its large field of view is a major asset in this multifocal pathology. However, MRI suffers from limited availability and does not allow for a dynamic examination in real time. Fusion imaging has great potential in the assessment of endometriosis because it combines the advantages of TVS and MR imaging modalities, and correspondingly overcomes their weaknesses, providing superior spatial, contrast and temporal resolution to that possible with

5 Fusion imaging of endometriosis 113 Figure 2 Fusion imaging of normal uterosacral ligaments (arrows). Simultaneous display of corresponding sagittal planes obtained by magnetic resonance imaging (left) and transvaginal sonography (right). Figure 3 Fusion imaging of anterior rectal wall endometriotic nodule (arrows). Simultaneous display of corresponding sagittal planes obtained by magnetic resonance imaging (MRI, left) and transvaginal sonography (TVS, right). Nodule appears hypointense on T2-weighted MRI and is hypoechogenic on TVS.

6 114 Millischer et al. Figure 4 Fusion imaging of anterior rectal wall endometriotic nodule. Simultaneous display of corresponding sagittal planes obtained by magnetic resonance imaging (MRI, left) and transvaginal sonography (TVS, right). On T2-weighted MRI, nodule was hypointense (arrows) and very difficult to identify due to fecal impaction, even after bowel preparation; on TVS, hypoechogenic nodule was easily identified (arrow). This figure emphasizes the ability of fusion imaging to overcome the weakness of MRI regarding visualization of rectal lesions. Figure 5 Fusion imaging of ureteral lesion with double pigtail stent. Simultaneous display of corresponding sagittal planes obtained by magnetic resonance imaging (MRI, left) and transvaginal sonography (TVS, right). Stent (arrows) was clearly identified using MRI and was identified (arrows) after focus screening on TVS. each technique alone. As well as the tissue contrast capabilities of MRI, it benefits from the dynamic, real-time qualities of TVS which allow diagnosis of adhesions, a major component in DIE 34,39 41 : TVS assessment of endometriotic lesions includes applying gentle pressure with the transvaginal probe in the area of interest to determine the fixation of the endometriotic nodule to adjacent structures. Our study confirmed some weaknesses of TVS and MRI. MRI has been shown to have higher sensitivity

7 Fusion imaging of endometriosis 115 Figure 6 Fusion imaging of bladder uterus adhesion adjacent to a Cesarean section scar. Simultaneous display of corresponding sagittal planes obtained by magnetic resonance imaging (MRI, left) and transvaginal sonography (TVS, right). The thin linear hyposignal (arrows) on T2-weighted MRI corresponds to the adhesion (arrow) visualized using TVS. Table 4 Appropriate assessment of endometriotic sites by transvaginal sonography (TVS), magnetic resonance imaging (MRI) and fusion imaging in 17 patients with suspected active endometriosis Imaging modality USL PVF* Rectum Ureters Bladder TVS 30/34 (88) 30/34 (88) 17/17 (100) 0/34 (0) 17/17 (100) MRI 34/34 (100) 34/34 (100) 14/17 (82) 34/34 (100) 17/17 (100) Fusion imaging 34/34 (100) 34/34 (100) 17/17 (100) 34/34 (100) 17/17 (100) Data are given as n/n (%). *Denominator in this column is 34 because left and right involvement of the posterior vaginal fornix (PVF) was assessed. USL, uterosacral ligaments. for USL, vaginal 6,42 and ureteral lesions 37 ; technical limitations and/or poor tissue contrast can hamper the ability of standard TVS to detect USL and ureteral lesions. We found that MRI performed better than did TVS in visualizing these anatomical sites sufficiently for their assessment (USL in 100% vs 88% cases; PVF in 100% vs 88%). Fusion imaging, however, overcame the limitations of TVS: synchronizing the MRI images aided in locating the targeted structure with TVS. Previous studies have reported that TVS and MRI are both highly accurate for the detection of rectal endometriosis 5,10,12,21,43, with better accuracy for TVS because of its better delineation of the intestinal layers 16,21,35. This is consistent with our findings (identified in 100% of cases on TVS vs 82% on MRI), emphasizing the difficulty in identifying pathology of the rectum with MRI, especially when there is fecal impaction. Again, by combining the two modalities, fusion imaging improved on the performance of MRI. We envisage various other contexts in which application of fusion imaging could be of benefit. Although this was not evaluated in the present study, fusion imaging could be used in follow-up examinations of pelvic diseases, which, after an initial MRI reference examination, require frequent measurements of ovarian mass, leiomyomas and endometrial assessment. In the past, it was difficult to compare MRI and ultrasound measurements because of the necessity of obtaining identical anatomical planes. This problem can be circumvented with fusion imaging, which allows perfect alignment of corresponding ultrasound and MR images. Our findings also support the potential of fusion imaging for training purposes to improve the operator s accuracy in both TVS and MRI, because it allows easier recognition of anatomical structures and location of DIE lesions in both modalities, due to the point-to-point image fusion of volume data from each. However, further studies are required to evaluate the ability of fusion imaging to optimize these learning curves. Finally, image-guided invasive procedures may also benefit from fusion imaging. The limited availability of MRI machines, as well as limitations on the use of metallic materials in the magnetic field, has prevented the development of MRI-guided invasive procedures. Fusion imaging should allow real-time ultrasound-guided procedures to be enhanced with information provided by MRI 26, In contrast to our report using prenatal fusion imaging, in which MRI and ultrasound had to be performed on the same day to avoid changes in fetal position or in anatomy resulting from fetal growth 32,a greater time interval between MRI and fusion imaging examinations is possible for other uses, such as in the current study, in which the interval was as much as 1 year. Indeed, pelvic structures (except the bowel) move and change very little over time, and movement is even

8 116 Millischer et al. less likely in patients with endometriosis, in whom the illness itself causes organs to stick to each other. While fusion imaging technology has been available for some time 9 28, it has not yet been used for pelvic imaging. To the best of our knowledge, this is the first description of advanced image fusion of real-time ultrasound with MRI in pelvic endometriosis. Although the results from our study are promising, several limitations must be considered. First, pathological/surgical correlations of our findings were not available for most patients. Therefore, the diagnostic performance of fusion imaging, as compared with that of ultrasound and/or MRI, could not be evaluated. However, this was not our primary objective and we did not aim to demonstrate any improvement in diagnosis of DIE, which explains why we did not include a control group. Our aim was to evaluate the feasibility of this new technique and assess its ability to improve visualization of the main anatomical sites of endometriosis, whether or not these sites were affected. To illustrate, normal USL cannot be identified routinely by ultrasound, unless there is surrounding fluid 34 bordering the usually thin ligament; at MRI, normal USL are always visualized 21. Fusion imaging, in combining ultrasound with MRI, was able to visualize these structures in all cases. Second, our study included only a small number of cases. Further studies with surgical and anatomopathological correlations will be necessary to evaluate the clinical benefit of this new technique for the management of patients with endometriosis. Additional studies are also required to evaluate the benefit of fusion imaging in other endometriotic-focused lesions, such as adnexal injuries, hydrosalpinges and adenomyosis. More generally, it would be of interest to evaluate fusion imaging in the follow-up of pelvic diseases, compared with the current use of repeat MRI examinations. Finally, this study was performed by only one operator, who was highly experienced in imaging of endometriosis. Future studies should include a larger sample of operators, including junior doctors, to assess the impact of this technique on the learning curve of endometriotic diagnostics. In conclusion, fusion imaging, which combines the advantages of both MRI and ultrasound for pelvic imaging, is feasible and well suited to locating and assessing the anatomical sites involved in DIE. Multimodality fusion imaging could facilitate diagnoses and provide a more reliable means of follow-up for pelvic anomalies, although more robust studies are required to confirm this. Larger prospective studies are necessary to standardize this new technique and rate conclusively its additional value. REFERENCES 1. 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