- Email: [email protected]
Feasibility of 3.0 T pelvic MR imaging in the evaluation of endometriosis
European Journal of Radiology 81 (2012) 1381–1387
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Feasibility of 3.0 T pelvic MR imaging in the evaluation of endometriosis L. Manganaro a,1 , F. Fierro a,∗ , A. Tomei a,1 , D. Irimia a,1 , P. Lodise a,1 , M.E. Sergi a,1 , V. Vinci a,1 , P. Sollazzo a,1 , M.G. Porpora b,1 , R. Delfini c,1 , G. Vittori c,1 , M. Marini a,1 a b c
Umberto I Hospital, Radiological Science Department, Sapienza University of Rome, Viale R. Elena 324, 00185 Italy Clinica Ostetrica e Ginecologica, Umberto I Hospital, Viale R. Elena 324, 00185 Italy Clinica Ostetrica e Ginecologica, San Carlo di Nancy Hospital, Via Aurelia 275, 00100 Italy
a r t i c l e
i n f o
Article history: Received 14 December 2010 Accepted 15 March 2011 Keywords: Pelvic MRI 3.0 T MR Endometriosis DIE Adhesions
a b s t r a c t Introduction: Endometriosis represents an important clinical problem in women of reproductive age with high impact on quality of life, work productivity and health care management. The aim of this study is to define the role of 3 T magnetom system MRI in the evaluation of endometriosis. Materials and methods: Forty-six women, with transvaginal (TV) ultrasound examination positive for endometriosis, with pelvic pain, or infertile underwent an MR 3.0 T examination with the following protocol: T2 weighted FRFSE HR sequences, T2 weighted FRFSE HR CUBE 3D sequences, T1 w FSE sequences, LAVA-flex sequences. Pelvic anatomy, macroscopic endometriosis implants, deep endometriosis implants, fallopian tube involvement, adhesions presence, fluid effusion in Douglas pouch, uterus and kidney pathologies or anomalies associated and sacral nervous routes were considered by two radiologists in consensus. Laparoscopy was considered the gold standard. Results: MRI imaging diagnosed deep endometriosis in 22/46 patients, endometriomas not associated to deep implants in 9/46 patients, 15/46 patients resulted negative for endometriosis, 11 of 22 patients with deep endometriosis reported ovarian endometriosis cyst. We obtained high percentages of sensibility (96.97%), specificity (100.00%), VPP (100.00%), VPN (92.86%). Conclusion: Pelvic MRI performed with 3 T system guarantees high spatial and contrast resolution, providing accurate information about endometriosis implants, with a good pre-surgery mapping of the lesions involving both bowels and bladder surface and recto-uterine ligaments. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Endometriosis represents an important clinical problem in women of reproductive age with high impact on quality of life, work productivity and health care management. It is defined as the presence of epithelial tissue and endometrial stroma outside the uterus, whose prevalence is not well defined; it is estimated to occur with an incidence around 5–10%, including both symptomatic and asymptomatic patients [1–3]. The pathogenesis is still unknown, therefore a multifactor basis is supposed. Three theories of histogenesis have been proposed:
∗ Corresponding author. Tel.: +39 064456695; fax: +39 064456695. E-mail addresses: [email protected] (L. Manganaro), francescafi[email protected] (F. Fierro), [email protected] (A. Tomei), doc [email protected] (D. Irimia), [email protected] (P. Lodise), [email protected] (M.E. Sergi), [email protected] (V. Vinci), [email protected] (P. Sollazzo), [email protected] (M.G. Porpora), raffaella.delfi[email protected] (R. Delfini), [email protected] (G. Vittori), [email protected] (M. Marini). 1 Tel. +39 064456695; fax: +39 064456695. 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.03.049
a) The metastasis theory, focused on retrograde menstrual or surgical implantation, lympathic and vascular spread, better explains the ovarian and peritoneal localization. b) The metaplastic differentiation of the coelomic epithelium, which ultimately develops into endometrial tissue, would explain the deep localization. c) The induction theory proposes that undefined biochemical factors induce undifferentiated peritoneal cells which develop into endometrial tissue [4].
In the last decade several etiological factors have been evaluated, such genetic factors, environmental factors, endocrine factors and immunological factors which extent the research field. Earlier classification divided endometriosis in externa and interna, which is actually defined as adenomyosis, while the external endometriosis is simply identified as endometriosis. The anatomopathological evaluation identify microscopic foci or wider cystic endometriosis whose correct name would be endometriomas; although the two terms are equally used, it is important to underline the difference between the two type of lesions, indeed the latter represents the association of adhesion and endometrial implants. The most
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frequent sites of implantation are ovaries (76%), cul de sac (69%), broad ligaments (47%), uterosacral ligaments (36%), uterus (11%), fallopian tubes (6), sigmoid colon (4%), ureters (3%) and small intestine (0.5%) [5]. Deep endometriosis is defined as the presence of invasive endometriosis implants extended for more than 5 mm from the peritoneal surface into the nearest structures; it is often associated to fibrosis and hyperplastic muscles [6]. Symptoms comprehend chronic pelvic pain in a wide range of severity, dyspareunia, dysmenorrhea, dysuria, rectal pain and infertility. Laparoscopy represents the standard technique for the evaluation and classification of endometriosis, otherwise the wide space resolution offered by magnetic resonance (MR) allows to identify implants outside the adnexal, undetected on ultrasound (US). The radiologist therefore is often requested to characterize the lesions, contributing to define the genesis of the pain. The role of 1.5 T MRI in the evaluation of endometriosis has been widely demonstrated, but only in the last years, the 3 T magnetom system has been applied on the evaluation of the female pelvis [6–8]. To the best of our knowledge, however, there are only poor papers regarding endometriosis diagnosed by 3 T unit. The increased signal-to-noise ratio (SNR), obtained with the higher field strength, lows the acquisition time, reducing the voxel volume and obtaining images with higher resolution. In the detection and staging of endometriosis, it leads a better definition of the pelvic female anatomy, characterization of the shape, localization of the implants and visualization of the adhesion. The aim of this study is to define the role of 3 T magnetom system MRI in the evaluation of endometriosis. 2. Materials and methods The study was approved by our local board and a written informed consent was obtained from all the participating. Between February 2010 and September 2010 46 women, aged between 20 and 43 years (mean age 30.4 years) underwent an MRI 3.0 T examination. We enrolled in the study patients with transvaginal (TV) ultrasound examination positive for endometriosis, patients with chronic pelvic pain, symptomatic patients with negative ultrasound examination and infertile patients. Creatinine blood levels were requested within 2 months before the MRI examination. 17 patients were treated with combined oral contraceptive pill.
ple scan planes, in particular stacks were oriented on axial, coronal and sagittal planes of the pelvis and sacral para-coronal plane. Contrast agent (gadoteric acid; Dotarem, Guerbet) was administered in 3 cases in patients affected by hydroureteronephrosis, increased endometrial thickness and suspect of pelvic inflammatory disease; by using LAVAflex sequences, after contrast agent administration (0.2 ml/kg) arterial phases (15–20 s after contrast agent injection), portal vein phase (50–60 s) and late phase (120 s) were obtained. Urographic scans were acquired in patients affected by hydroureteronephrosis (8 min after contrast injection), processed according to MIP protocol (minimum intensity projection), in order to visualize the ureteral anatomy. Total acquisition time amounts to 20 min. Patient who underwent contrast agent injection required a 30 min MRI examination, or 40 min if urographic phases needed (Figs. 1 and 2). 2.2. Imaging analysis Two radiologists, with, respectively, 10 and 5 years experience in female pelvic, evaluated in consensus the exams, using LMD Sony 2451-MD monitor (resolution of 1220 × 1920 pixels). Radiologists were asked to evaluate the following parameters: -
pelvic anatomy; macroscopic endometriosis implants; deep endometriosis implants; fallopian tube involvement; adhesions presence; fluid effusion in Douglas pouch; uterus and kidney pathologies or anomalies associated; sacral nervous routes.
2.3. Standard reference Patients underwent diagnostic and therapeutic laparoscopy. 2.4. Statistical analysis Sensibility, specificity, predictive positive value (PPV), predictive negative value (NPV) of MRI in the evaluation of endometriomas and deep endometriosis implants were calculated.
2.1. MR imaging examinations 3. Results Pelvic MRI was performed in every case with a 3 T system GE Discovery 750. Patients were asked to drink and eat normally the days before the exam. A negative superparamagnetic oral contrast agent (Ferumoxil, Lumirem 175 mg/L, Guerbet), was administered in order to reduce the signal intensity of the bowels. Patients were instructed not to urinate for at least 1 h prior the MRI scan, in order to obtain a full bladder. Hyoscine N-butylbromide (Buscopan 20 mg/mL, Boehringer Ingelheim, 20 mg) was administered either by intravenous or muscular injection to reduce the normal bowel peristaltic artifacts. Patients were introduced into the gantry “feet first” supine position with one multhichannel phased-array surface body coil (8 channels, 127.73 MHz). The common study protocol included: single shot fast spin echo sequences (matrix 384 × 224, FOV 360 × 360, FA 90◦ , TR 2000, TE 102 and slice thickness 6 mm); T2 weighted FRFSE HR sequences (matrix 448 × 256, FOV 230 × 230, FA 90◦ , TR 6279, TE 1322 and slice thickness 3 mm); T2 weighted FRFSE HR CUBE 3D sequences (matrix 256 × 256, FOV 300 × 300, FA 90◦ , TR 2540, TE 162 and slice thickness 3 mm); T1 w FSE sequences (matrix 320 × 192, FOV 240 × 240, FA 90◦ , TR 586, TE 8 and slice thickness 3 mm); LAVA-flex sequences (matrix 288 × 224, FOV 310 × 310, FA 12◦ , TR 4, TE 2 and slice thickness 4 mm). MRI images were acquired according to multi-
MRI imaging diagnosed deep endometriosis in 22/46 patients, endometriomas not associated to deep implants in 9/46 patients, 15/46 patients resulted negative for endometriosis, 11 of 22 patients with deep endometriosis reported ovarian endometriosis cyst. Regions interested by endometriosis lesions were rectovaginal septum (12 patients), posterior vaginal fornix (8 patients), serosal rectosigmoid surface (5 patients), rectouterine ligaments (right 1 patients; left 2 patients), bladder surface (2 patients). 9 patients reported adnexal endometriosis, not associated with deep endometriosis implants (3 of the right ovary, 4 of the left ovary, 2 bilateral). Endometriomas appeared hyperintense in T1 weighted sequences, with and without fat saturation, on T2 w sequences they showed variable signal intensity, known as “shading”, characteristic of the presence of degradation haemoglobin products (Fig. 1). Deep endometriosis implants were characterized by both fibrosis components with a low signal intensity in T2 and T1 w sequences associated with retroaction phenomena of the close structures, or for hyperintense foci in T1 w sequences and hypointense signal in T2 w because of the poor fibrosis component (Figs. 3 and 4). In 19/31 patients affected by endometriosis adhesions were identified, which involved the rectosigmoid tract and the posterior uterus
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Fig. 1. T1 LAVA flex axial images (a and b) show the high signal of the endometriomas in the right and left adnexal. The T2 w FRFSE images indicate the typical shading.
surface (5p) (Fig. 2); the isolated rectosigmoid tract, the ovary and the posterior uterus surface (3p) (Fig. 4); tube, rectum and uterus (1p), adnexal (2p), rectosigmoid tract (2p), one rectouterine ligament (1p); rectouterine ligaments and posterior vaginal fornix (3p); utero-vescica surface (1p), uterus, sigmoid colon and left ureter (1p) (Fig. 3). 17 patients showed fluid collection in Doulas space. Five patients showed sactosalpinx. Nine patients seemed to
have an involvement of the sacral nerve into the deep implant. On FSE T2 w sequences adhesions appeared well visualized as stellate or nodular hypointense areas, creating attraction of the close structures; the rectosigmoid surface showed an increased thickness; rectouterine ligaments were ticker and not homogeneous. Laparoscopy confirmed the presence of deep endometriosis in 23 patients (true positive; TP), and endometriomas in 19 patients (true
Fig. 2. T1 axial image with fat saturation, LAVA flex (a) shows on the right posterior vaginal fornix deep endometriotic implants with high signal intensity, involving the uterosacral ligament, as the arrow indicates on the T2 high resolution image FRFSE (b). The arrow on the sagittal plane (c) shows the adherence between uterus and recto-sigmoid tract.
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Fig. 3. The T1 w LAVA fat sat image (a, b and d), acquired on axial plane, show the high signal intensity foci of the deep infiltrating endometriosis, involving uterus, bladder and recto-sigmoid tract; the T2 w image better shows the adhesions (c).
Fig. 4. On the left, the T1 LAVA sequence shows two hypointense, bilateral para-adnexal structures, better visualized on the T2 FRFSE image (b), which resulted endometriotic implants.
positive; TP), 9 of them not associated with implants and 10 associated with deep implants. MRI, compared to laparoscopy, reported 1 false negative, a deep implant of the left rectouterine ligament, in a woman underwent to bilateral ovariectomy and had uterine anteflexion and anteversion (Table 1). Values of sensibility, specificity, predictive positive value (PPV), predictive negative value (NPV) are reported in Tables 2–4 4. Discussion
posed in order to identify alternative techniques able to evaluate etiology of pelvic pain and infertility and to offer a better planning management. Transvaginal and transrectal ultrasound have been matter of debate [13,14] with variable and mainly positive results as discussed by Bazot et al. Grasso et al. [1] in a recent work of 2009 compared transvaginal ultrasound 3D and MRI reaching the conclusion that US may be helpful in the first evaluation of the Table 2 Sensibility, specificity, PPV, NPV for endometriosis
Laparoscopy remains the standard technique to evaluate the endometriosis, necessary for diagnosis and treatment of both endometriosis and adhesions [9–11]. Laparoscopy is however associated with some risks for young women. Moreover in some cases, adhesions of the cul-de-sac-region make surgery difficult [12]. In the last two decades several diagnostic techniques have been proTable 1 MR vs LPS results.
MR results LPS results
DIE
IE
DIE + IE
Negatives
11 13
9 9
11 10
15 13
. Sensibility
Specificity
PPV
NPV
96.97%
100.00%
100.00%
92.86%
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Fig. 5. (a and b) T1 w LAVA axial sequences. Right adnexal region: sactosalpinx of endometriosis. The variable signal intensity depends on the presence of degradation haemoglobin products. The T2 w FRFSE sequences (c and d) show also the adhesion (arrow, d).
Fig. 6. The T1 w images, acquired on paracoronal plane, without fat suppression (T1 FSE, a) and in axial plane, with fat saturation (LAVA-FLEX, b) show the presence of endometriomas in the left adnexal; the T2 w images on axial (c) and sagittal (d) plane better show the adhesions between adnexal, uterus and recto-sigmoid tract.
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Table 3 Sensibility, specificity, PPV, NPV for deep endometriosis
. Sensibility
Specificity
PPV
NPV
96.65%
100.00%
100.00%
92.86%
woman with chronic pelvic pain, although the distance between the transducer and deep lesion may be a technical limit. Jung et al. [15] recent study evaluated feasibility and diagnostic possibilities of CT scan, demonstrating that the elevate dose of radiation does not justify its use, even if it could be useful in case of deep endometriosis as an adjunctive imaging modality. Several studies have proved the role of 1.5 T MR in the evaluation of endometriosis: Kataoka et al. established its utility in the evaluation of cul-de-sac obliteration [16]; Zanardi et al. proposed the use of MRI technique in the staging of endometriosis [17–20]. Our work demonstrated an optimal correlation between MRI and laparoscopy, with exhaustive values of sensibility and specificity, comparable to those reported on a recent paper of Hottat et al. [6]. MRI revealed to be more useful than the 1.5 T MR in the evaluation of deep implants located in the recto-vaginal septum, posterior vaginal fornix and in rectosigmoid surface, highlighting the pelvic portion between ureters and recto-uterine ligaments, sometimes not well detected with US. The protocol of study on a 3 T System, comprehends the same sequences and planes we usually apply on a 1.5 T magnetom system. The use of T1 w fat saturation sequences falls in the ordinary routine of the endometriosis evaluation and specificity would drastically reduce without its application. Fat saturation comprehends various techniques: CHESS (chemical shift saturation) and SPECIAL (spectral inversion at lipids), widely used, which are often affected by magnetic field and RF impulse inhomogeneities [8]. This effect is increases proportionally with magnetic field strength. Few studies [8] demonstrated that the application of Dixon 3D sequences may overcome this problem because less sensitive to the movement, still producing fat suppression images. It is however well known the characteristic hyperintense signal of endometriosis implants due to the hemoglobine degradation products [21]; however our experiences demonstrated the importance of the high
Table 4 Sensibility, specificity, PPV, NPV for endometriomas
resolution study with T2 sequences for the evaluation of both the deep implants and adhesions, attracting and deforming the close structures. T2 w FSE sequences have a higher signal-to-noise ratio, which ensures a good quality images, with better visualization of thin structures such rectouterine ligaments or bladder and bowel surface. Moreover, FSE sequences allow the use of parallel imaging, which reduces the inter-eco space, with higher resolution due to reduction of blurring. MRI spatial resolution is easily explicated by the axial and sagittal planes which offer a good anatomical view of the Douglas space, cul-de-sac and rectouterine ligaments. Coronal plane, however, added few diagnostic information, even if a para-coronal plane has been used to evaluate the involvement of the sacral nerves radices as possible cause of chronic pelvic pain. CUBE 3D sequences allowed, in this regard, acquisition of one volume, different from the previous single voxel, in order to process on different planes space with a low slice thickness, thus leading to a reduced time and higher anatomical resolution. The efficacy of this technique enabled us to follow the sacral nerves routs throughout the pelvic space. Contrast agent does not add new information, although it might help to evaluate an acute inflammatory condition, or to analyze the anatomical ureter tract thanks to MIP processing. We used it for selected cases when a differential diagnosis was necessary or in ureteral involvment. Few authors [22] support the use of intracavitary gel, both vaginal and rectal, in order to obtain a better definition of the lesions, especially in Douglas space; even if Bazot, in one of his work of 2004 [14] demonstrate how it is possible to get the same results with a standard protocol avoiding the patient discomfort and the lenghthening procedure. 3 T MR is usually affected by an increased SAR (specific absorption rate) and radiofrequency field inhomogeneity [23]. A device of Kataoka et al. study [24], suggests to include on women’s body a dielectric pad, whose function is to absorbe and eliminate reflexes waves, reducing interference [25–27], thus obtaining quality imaging vantages. Patients referred no discomfort due to the use of the pad. Time procedure of 3 T system remains equal to 1.5 T system. Limits of our study were the heterogeneous population and the small number of patients, especially affected by deep endometriosis; by the way the radiologists were aware of the clinical condition of the patients. The small number of patients affected by deep endometriosis involving the sacral nerves did not allow us to perform a significant statistical correlation between these data and the pain. Furthermore the MR has been installed by our department just few months ago and is still in progressive implementation; the signal inhomogeneity might have affected our study (Figs. 5 and 6). 5. Conclusions Pelvic MRI performed with 3 T system guarantees high spatial and contrast resolution, providing accurate information about endometriosis implants, with a good pre-surgery mapping of the lesions involving both bowels and bladder surface and rectouterine ligaments. T2 w FSE sequences resulted useful in the evaluation of deep implants and adhesions. However, studies based on wider population and with optimal correction of technical parameters are necessary in order to increase the diagnostic possibilities. References
. Sensibility
Specificity
PPV
NPV
90%
100.00%
100.00%
92.86%
[1] Grasso RF, Di Giacomo V, Sedati P, et al. Diagnosis of deep infiltrating endometriosis: accuracy of magnetic resonance imaging and transvaginal 3D ultrasonography. Abdom Imaging 2009. Online FirstTM . [2] Halis G, Mechsner S, Ebert AD. The diagnosis and treatment of deep infiltrating endometriosis. Dtsch Arztebl Int 2010;107(25):446–56. [3] Bulun SE. Endometriosis. N Engl J Med 2009;360(January (3)):268–79. [4] Woodward PJ, Sohaey R, Mezzetti Jr TP. Endometriosis: radiologic–pathologic correlation. Radiographics 2001;21(January–February (1)):193–216, questionnaire 288–94.
L. Manganaro et al. / European Journal of Radiology 81 (2012) 1381–1387 [5] Chamiè LP, Blasbalg R, Goncalves MO, Carvalho FM, Abrao MS, de Oliveira IS. Accuracy of magnetic resonance imaging for diagnosis and preoperative assessment of deeply infiltrating endometriosis. Int J Gynaecol Obstet 2009;106(September (3)):198–201. Epub 2009 May 24. [6] Hottat N, Larrousse C, Anaf V, et al. Endometriosis: contribution of 3.0T pelvic MR imaging in preoperative assessment-initial results. Radiology 2009;253(October (1)):126–34. Epub 2009 July 7. [7] Hussain SM, van den Bos IC, Oliveto JM, Martin DR. MR Imaging of the female pelvis at 3 T. Magn Reson Imaging Clin 2007;14:537–44. [8] Cornfeld DM, Israel G, McCarthy SM, Weinreb JC. Pelvic imaging using a T1 w fat-suppressed three-dimensional dual echo Dixon technique at 3 T. J Magn Reson Imaging 2008;28:121–7. [9] Van der Wal JBC, Halm JA, Jeekel J. Chronic abdominal pain: the role of adhesions and benefit of laparoscopic adhesiolysis. Gynecol Surg 2006;3: 168–74. [10] Giannoulis H, Tantanasis T, Papathanasiou K, Loufopoulos A, Tzafettas J. Diagnostic laparoscopy, infertility, and endometriosis-5 years experience. Gynecol Surg 2008;5:231–4. [11] Endometriosis and infertility. The practice Committee of the American Society for Reproductive Medicine. Fertil Steril 2004;81(May (5)). [12] Bis KG, Vrachliotis TG, Agrawal R, Shetty AN, Maximovich A, Hricak H. Pelvic endometriosis: MR imaging spectrum with laparoscopic correlation and diagnostic pitfalls. Radiographics 1997;17:639–55. [13] Roseau G, Dumontier I, Palazzo L, et al. Rectosigmoid endometriosis: endoscopic ultrasound features and clinical implications. Endoscopy 2000;32:525–30. [14] Bazot M, Darai E, Hourani R, Thomassin I, Cortez A, Uzan J-N. Buy deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004;232:379–89. [15] Jung SI, Kim Yj, Jeon HJ, Jeong KA. Deep infiltrating endometrios: CT imaging evaluation. J Comput Assist Tomogr 2010;34:338–42. [16] Kataoka ML, Togashi K, Yamaoka T, et al. Posterior Cul-de-Sac obliteration associated with endometriosis: MR imaging evaluation. Radiology 2005;234:815–23.
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[17] Zanardi R, Del Frate C, Zuiani C, Del Frate G, Bazzocchi M. Staging of pelvic endometriosis using magnetic resonance imaging compared with the laparoscopic classification of the American Fertility Society: a prospective study. Radiol Med 2003;105:326–38. [18] Eskenazi B, Warner M, Bonsignore L, Olive D, Samuels S, Vercellini P. Validation study of nonsurgical diagnosis of endometriosis. Fertil Steril 2001;76: 929–35. [19] Bazot M, Bornier C, Dubernard G, Roseau G, Cortez A, Darai E. Accuracy of magnetic resonance imaging and rectal endoscopic sonography for the prediction of location of deep pelvic endometriosis. Hum Reprod 2007;22: 1457–63. [20] Del Farte c, Girometti R, Pittino M, Del Frate G, Bazzocchi M, Zuiani C. Deep retroperitoneal pelvic endometriosis: MR imaging appearance with laparoscopic correlation. Radiographics 2006;26:1705–18. [21] Stratton P, Winkel C, Premkumar A, et al. Diagnostic accuracy of laparoscopy, magnetic resonance imaging, and histopathologic examination for the detection of endometriosis. Fertil Steril 2003;79:1078–85. [22] Chassang M, Novellas S, Bloch-Marcotte C, et al. Utility of vaginal and rectal contrast medium in MRI for the detection of deep pelvic endometriosis. Eur Radiol 2010;20:1003–10. [23] Schnick F. Whole-body MRI at high field: technical limits and clinical potential. Eur Radiol 2005;15:946–59. [24] Kataoka M, Isoda H, Maetani Y, et al. MR imaging of the female pelvis at 3 Tesla: evaluation of image homogeneity using different dielectric pads. J Magn Reson Imaging 2007;26:1572–7. [25] Schmitt M, Feiweier T, Horger W, et al. Improved uniformity of RF-distribution in clinical whole body-imaging at 3 T by means of dielectric pads. In: Proceedings of the 12th Annual Meeting of ISMRM. 2004 (Abstract 197). [26] Sreenivas M, Lowry M, Gibbs P, Pickles M, Turnbull LW. A simple solution for reducing artifacts due to conductive and dielectric effects in clinical magnetic resonance imaging at 3 T. Eur J Radiol 2007;62:143–6. [27] Yang QX, Mao Wang J, et al. Manipulation of image intensity distribution at 7.0 T: passive RF shimming and focusing with dielectric materials. J Magn Reson Imaging 2006;24:197–202.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Feasibility of 3.0 T pelvic MR imaging in the evaluation of endometriosis L. Manganaro a,1 , F. Fierro a,∗ , A. Tomei a,1 , D. Irimia a,1 , P. Lodise a,1 , M.E. Sergi a,1 , V. Vinci a,1 , P. Sollazzo a,1 , M.G. Porpora b,1 , R. Delfini c,1 , G. Vittori c,1 , M. Marini a,1 a b c
Umberto I Hospital, Radiological Science Department, Sapienza University of Rome, Viale R. Elena 324, 00185 Italy Clinica Ostetrica e Ginecologica, Umberto I Hospital, Viale R. Elena 324, 00185 Italy Clinica Ostetrica e Ginecologica, San Carlo di Nancy Hospital, Via Aurelia 275, 00100 Italy
a r t i c l e
i n f o
Article history: Received 14 December 2010 Accepted 15 March 2011 Keywords: Pelvic MRI 3.0 T MR Endometriosis DIE Adhesions
a b s t r a c t Introduction: Endometriosis represents an important clinical problem in women of reproductive age with high impact on quality of life, work productivity and health care management. The aim of this study is to define the role of 3 T magnetom system MRI in the evaluation of endometriosis. Materials and methods: Forty-six women, with transvaginal (TV) ultrasound examination positive for endometriosis, with pelvic pain, or infertile underwent an MR 3.0 T examination with the following protocol: T2 weighted FRFSE HR sequences, T2 weighted FRFSE HR CUBE 3D sequences, T1 w FSE sequences, LAVA-flex sequences. Pelvic anatomy, macroscopic endometriosis implants, deep endometriosis implants, fallopian tube involvement, adhesions presence, fluid effusion in Douglas pouch, uterus and kidney pathologies or anomalies associated and sacral nervous routes were considered by two radiologists in consensus. Laparoscopy was considered the gold standard. Results: MRI imaging diagnosed deep endometriosis in 22/46 patients, endometriomas not associated to deep implants in 9/46 patients, 15/46 patients resulted negative for endometriosis, 11 of 22 patients with deep endometriosis reported ovarian endometriosis cyst. We obtained high percentages of sensibility (96.97%), specificity (100.00%), VPP (100.00%), VPN (92.86%). Conclusion: Pelvic MRI performed with 3 T system guarantees high spatial and contrast resolution, providing accurate information about endometriosis implants, with a good pre-surgery mapping of the lesions involving both bowels and bladder surface and recto-uterine ligaments. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Endometriosis represents an important clinical problem in women of reproductive age with high impact on quality of life, work productivity and health care management. It is defined as the presence of epithelial tissue and endometrial stroma outside the uterus, whose prevalence is not well defined; it is estimated to occur with an incidence around 5–10%, including both symptomatic and asymptomatic patients [1–3]. The pathogenesis is still unknown, therefore a multifactor basis is supposed. Three theories of histogenesis have been proposed:
∗ Corresponding author. Tel.: +39 064456695; fax: +39 064456695. E-mail addresses: [email protected] (L. Manganaro), francescafi[email protected] (F. Fierro), [email protected] (A. Tomei), doc [email protected] (D. Irimia), [email protected] (P. Lodise), [email protected] (M.E. Sergi), [email protected] (V. Vinci), [email protected] (P. Sollazzo), [email protected] (M.G. Porpora), raffaella.delfi[email protected] (R. Delfini), [email protected] (G. Vittori), [email protected] (M. Marini). 1 Tel. +39 064456695; fax: +39 064456695. 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.03.049
a) The metastasis theory, focused on retrograde menstrual or surgical implantation, lympathic and vascular spread, better explains the ovarian and peritoneal localization. b) The metaplastic differentiation of the coelomic epithelium, which ultimately develops into endometrial tissue, would explain the deep localization. c) The induction theory proposes that undefined biochemical factors induce undifferentiated peritoneal cells which develop into endometrial tissue [4].
In the last decade several etiological factors have been evaluated, such genetic factors, environmental factors, endocrine factors and immunological factors which extent the research field. Earlier classification divided endometriosis in externa and interna, which is actually defined as adenomyosis, while the external endometriosis is simply identified as endometriosis. The anatomopathological evaluation identify microscopic foci or wider cystic endometriosis whose correct name would be endometriomas; although the two terms are equally used, it is important to underline the difference between the two type of lesions, indeed the latter represents the association of adhesion and endometrial implants. The most
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frequent sites of implantation are ovaries (76%), cul de sac (69%), broad ligaments (47%), uterosacral ligaments (36%), uterus (11%), fallopian tubes (6), sigmoid colon (4%), ureters (3%) and small intestine (0.5%) [5]. Deep endometriosis is defined as the presence of invasive endometriosis implants extended for more than 5 mm from the peritoneal surface into the nearest structures; it is often associated to fibrosis and hyperplastic muscles [6]. Symptoms comprehend chronic pelvic pain in a wide range of severity, dyspareunia, dysmenorrhea, dysuria, rectal pain and infertility. Laparoscopy represents the standard technique for the evaluation and classification of endometriosis, otherwise the wide space resolution offered by magnetic resonance (MR) allows to identify implants outside the adnexal, undetected on ultrasound (US). The radiologist therefore is often requested to characterize the lesions, contributing to define the genesis of the pain. The role of 1.5 T MRI in the evaluation of endometriosis has been widely demonstrated, but only in the last years, the 3 T magnetom system has been applied on the evaluation of the female pelvis [6–8]. To the best of our knowledge, however, there are only poor papers regarding endometriosis diagnosed by 3 T unit. The increased signal-to-noise ratio (SNR), obtained with the higher field strength, lows the acquisition time, reducing the voxel volume and obtaining images with higher resolution. In the detection and staging of endometriosis, it leads a better definition of the pelvic female anatomy, characterization of the shape, localization of the implants and visualization of the adhesion. The aim of this study is to define the role of 3 T magnetom system MRI in the evaluation of endometriosis. 2. Materials and methods The study was approved by our local board and a written informed consent was obtained from all the participating. Between February 2010 and September 2010 46 women, aged between 20 and 43 years (mean age 30.4 years) underwent an MRI 3.0 T examination. We enrolled in the study patients with transvaginal (TV) ultrasound examination positive for endometriosis, patients with chronic pelvic pain, symptomatic patients with negative ultrasound examination and infertile patients. Creatinine blood levels were requested within 2 months before the MRI examination. 17 patients were treated with combined oral contraceptive pill.
ple scan planes, in particular stacks were oriented on axial, coronal and sagittal planes of the pelvis and sacral para-coronal plane. Contrast agent (gadoteric acid; Dotarem, Guerbet) was administered in 3 cases in patients affected by hydroureteronephrosis, increased endometrial thickness and suspect of pelvic inflammatory disease; by using LAVAflex sequences, after contrast agent administration (0.2 ml/kg) arterial phases (15–20 s after contrast agent injection), portal vein phase (50–60 s) and late phase (120 s) were obtained. Urographic scans were acquired in patients affected by hydroureteronephrosis (8 min after contrast injection), processed according to MIP protocol (minimum intensity projection), in order to visualize the ureteral anatomy. Total acquisition time amounts to 20 min. Patient who underwent contrast agent injection required a 30 min MRI examination, or 40 min if urographic phases needed (Figs. 1 and 2). 2.2. Imaging analysis Two radiologists, with, respectively, 10 and 5 years experience in female pelvic, evaluated in consensus the exams, using LMD Sony 2451-MD monitor (resolution of 1220 × 1920 pixels). Radiologists were asked to evaluate the following parameters: -
pelvic anatomy; macroscopic endometriosis implants; deep endometriosis implants; fallopian tube involvement; adhesions presence; fluid effusion in Douglas pouch; uterus and kidney pathologies or anomalies associated; sacral nervous routes.
2.3. Standard reference Patients underwent diagnostic and therapeutic laparoscopy. 2.4. Statistical analysis Sensibility, specificity, predictive positive value (PPV), predictive negative value (NPV) of MRI in the evaluation of endometriomas and deep endometriosis implants were calculated.
2.1. MR imaging examinations 3. Results Pelvic MRI was performed in every case with a 3 T system GE Discovery 750. Patients were asked to drink and eat normally the days before the exam. A negative superparamagnetic oral contrast agent (Ferumoxil, Lumirem 175 mg/L, Guerbet), was administered in order to reduce the signal intensity of the bowels. Patients were instructed not to urinate for at least 1 h prior the MRI scan, in order to obtain a full bladder. Hyoscine N-butylbromide (Buscopan 20 mg/mL, Boehringer Ingelheim, 20 mg) was administered either by intravenous or muscular injection to reduce the normal bowel peristaltic artifacts. Patients were introduced into the gantry “feet first” supine position with one multhichannel phased-array surface body coil (8 channels, 127.73 MHz). The common study protocol included: single shot fast spin echo sequences (matrix 384 × 224, FOV 360 × 360, FA 90◦ , TR 2000, TE 102 and slice thickness 6 mm); T2 weighted FRFSE HR sequences (matrix 448 × 256, FOV 230 × 230, FA 90◦ , TR 6279, TE 1322 and slice thickness 3 mm); T2 weighted FRFSE HR CUBE 3D sequences (matrix 256 × 256, FOV 300 × 300, FA 90◦ , TR 2540, TE 162 and slice thickness 3 mm); T1 w FSE sequences (matrix 320 × 192, FOV 240 × 240, FA 90◦ , TR 586, TE 8 and slice thickness 3 mm); LAVA-flex sequences (matrix 288 × 224, FOV 310 × 310, FA 12◦ , TR 4, TE 2 and slice thickness 4 mm). MRI images were acquired according to multi-
MRI imaging diagnosed deep endometriosis in 22/46 patients, endometriomas not associated to deep implants in 9/46 patients, 15/46 patients resulted negative for endometriosis, 11 of 22 patients with deep endometriosis reported ovarian endometriosis cyst. Regions interested by endometriosis lesions were rectovaginal septum (12 patients), posterior vaginal fornix (8 patients), serosal rectosigmoid surface (5 patients), rectouterine ligaments (right 1 patients; left 2 patients), bladder surface (2 patients). 9 patients reported adnexal endometriosis, not associated with deep endometriosis implants (3 of the right ovary, 4 of the left ovary, 2 bilateral). Endometriomas appeared hyperintense in T1 weighted sequences, with and without fat saturation, on T2 w sequences they showed variable signal intensity, known as “shading”, characteristic of the presence of degradation haemoglobin products (Fig. 1). Deep endometriosis implants were characterized by both fibrosis components with a low signal intensity in T2 and T1 w sequences associated with retroaction phenomena of the close structures, or for hyperintense foci in T1 w sequences and hypointense signal in T2 w because of the poor fibrosis component (Figs. 3 and 4). In 19/31 patients affected by endometriosis adhesions were identified, which involved the rectosigmoid tract and the posterior uterus
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Fig. 1. T1 LAVA flex axial images (a and b) show the high signal of the endometriomas in the right and left adnexal. The T2 w FRFSE images indicate the typical shading.
surface (5p) (Fig. 2); the isolated rectosigmoid tract, the ovary and the posterior uterus surface (3p) (Fig. 4); tube, rectum and uterus (1p), adnexal (2p), rectosigmoid tract (2p), one rectouterine ligament (1p); rectouterine ligaments and posterior vaginal fornix (3p); utero-vescica surface (1p), uterus, sigmoid colon and left ureter (1p) (Fig. 3). 17 patients showed fluid collection in Doulas space. Five patients showed sactosalpinx. Nine patients seemed to
have an involvement of the sacral nerve into the deep implant. On FSE T2 w sequences adhesions appeared well visualized as stellate or nodular hypointense areas, creating attraction of the close structures; the rectosigmoid surface showed an increased thickness; rectouterine ligaments were ticker and not homogeneous. Laparoscopy confirmed the presence of deep endometriosis in 23 patients (true positive; TP), and endometriomas in 19 patients (true
Fig. 2. T1 axial image with fat saturation, LAVA flex (a) shows on the right posterior vaginal fornix deep endometriotic implants with high signal intensity, involving the uterosacral ligament, as the arrow indicates on the T2 high resolution image FRFSE (b). The arrow on the sagittal plane (c) shows the adherence between uterus and recto-sigmoid tract.
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Fig. 3. The T1 w LAVA fat sat image (a, b and d), acquired on axial plane, show the high signal intensity foci of the deep infiltrating endometriosis, involving uterus, bladder and recto-sigmoid tract; the T2 w image better shows the adhesions (c).
Fig. 4. On the left, the T1 LAVA sequence shows two hypointense, bilateral para-adnexal structures, better visualized on the T2 FRFSE image (b), which resulted endometriotic implants.
positive; TP), 9 of them not associated with implants and 10 associated with deep implants. MRI, compared to laparoscopy, reported 1 false negative, a deep implant of the left rectouterine ligament, in a woman underwent to bilateral ovariectomy and had uterine anteflexion and anteversion (Table 1). Values of sensibility, specificity, predictive positive value (PPV), predictive negative value (NPV) are reported in Tables 2–4 4. Discussion
posed in order to identify alternative techniques able to evaluate etiology of pelvic pain and infertility and to offer a better planning management. Transvaginal and transrectal ultrasound have been matter of debate [13,14] with variable and mainly positive results as discussed by Bazot et al. Grasso et al. [1] in a recent work of 2009 compared transvaginal ultrasound 3D and MRI reaching the conclusion that US may be helpful in the first evaluation of the Table 2 Sensibility, specificity, PPV, NPV for endometriosis
Laparoscopy remains the standard technique to evaluate the endometriosis, necessary for diagnosis and treatment of both endometriosis and adhesions [9–11]. Laparoscopy is however associated with some risks for young women. Moreover in some cases, adhesions of the cul-de-sac-region make surgery difficult [12]. In the last two decades several diagnostic techniques have been proTable 1 MR vs LPS results.
MR results LPS results
DIE
IE
DIE + IE
Negatives
11 13
9 9
11 10
15 13
. Sensibility
Specificity
PPV
NPV
96.97%
100.00%
100.00%
92.86%
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Fig. 5. (a and b) T1 w LAVA axial sequences. Right adnexal region: sactosalpinx of endometriosis. The variable signal intensity depends on the presence of degradation haemoglobin products. The T2 w FRFSE sequences (c and d) show also the adhesion (arrow, d).
Fig. 6. The T1 w images, acquired on paracoronal plane, without fat suppression (T1 FSE, a) and in axial plane, with fat saturation (LAVA-FLEX, b) show the presence of endometriomas in the left adnexal; the T2 w images on axial (c) and sagittal (d) plane better show the adhesions between adnexal, uterus and recto-sigmoid tract.
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Table 3 Sensibility, specificity, PPV, NPV for deep endometriosis
. Sensibility
Specificity
PPV
NPV
96.65%
100.00%
100.00%
92.86%
woman with chronic pelvic pain, although the distance between the transducer and deep lesion may be a technical limit. Jung et al. [15] recent study evaluated feasibility and diagnostic possibilities of CT scan, demonstrating that the elevate dose of radiation does not justify its use, even if it could be useful in case of deep endometriosis as an adjunctive imaging modality. Several studies have proved the role of 1.5 T MR in the evaluation of endometriosis: Kataoka et al. established its utility in the evaluation of cul-de-sac obliteration [16]; Zanardi et al. proposed the use of MRI technique in the staging of endometriosis [17–20]. Our work demonstrated an optimal correlation between MRI and laparoscopy, with exhaustive values of sensibility and specificity, comparable to those reported on a recent paper of Hottat et al. [6]. MRI revealed to be more useful than the 1.5 T MR in the evaluation of deep implants located in the recto-vaginal septum, posterior vaginal fornix and in rectosigmoid surface, highlighting the pelvic portion between ureters and recto-uterine ligaments, sometimes not well detected with US. The protocol of study on a 3 T System, comprehends the same sequences and planes we usually apply on a 1.5 T magnetom system. The use of T1 w fat saturation sequences falls in the ordinary routine of the endometriosis evaluation and specificity would drastically reduce without its application. Fat saturation comprehends various techniques: CHESS (chemical shift saturation) and SPECIAL (spectral inversion at lipids), widely used, which are often affected by magnetic field and RF impulse inhomogeneities [8]. This effect is increases proportionally with magnetic field strength. Few studies [8] demonstrated that the application of Dixon 3D sequences may overcome this problem because less sensitive to the movement, still producing fat suppression images. It is however well known the characteristic hyperintense signal of endometriosis implants due to the hemoglobine degradation products [21]; however our experiences demonstrated the importance of the high
Table 4 Sensibility, specificity, PPV, NPV for endometriomas
resolution study with T2 sequences for the evaluation of both the deep implants and adhesions, attracting and deforming the close structures. T2 w FSE sequences have a higher signal-to-noise ratio, which ensures a good quality images, with better visualization of thin structures such rectouterine ligaments or bladder and bowel surface. Moreover, FSE sequences allow the use of parallel imaging, which reduces the inter-eco space, with higher resolution due to reduction of blurring. MRI spatial resolution is easily explicated by the axial and sagittal planes which offer a good anatomical view of the Douglas space, cul-de-sac and rectouterine ligaments. Coronal plane, however, added few diagnostic information, even if a para-coronal plane has been used to evaluate the involvement of the sacral nerves radices as possible cause of chronic pelvic pain. CUBE 3D sequences allowed, in this regard, acquisition of one volume, different from the previous single voxel, in order to process on different planes space with a low slice thickness, thus leading to a reduced time and higher anatomical resolution. The efficacy of this technique enabled us to follow the sacral nerves routs throughout the pelvic space. Contrast agent does not add new information, although it might help to evaluate an acute inflammatory condition, or to analyze the anatomical ureter tract thanks to MIP processing. We used it for selected cases when a differential diagnosis was necessary or in ureteral involvment. Few authors [22] support the use of intracavitary gel, both vaginal and rectal, in order to obtain a better definition of the lesions, especially in Douglas space; even if Bazot, in one of his work of 2004 [14] demonstrate how it is possible to get the same results with a standard protocol avoiding the patient discomfort and the lenghthening procedure. 3 T MR is usually affected by an increased SAR (specific absorption rate) and radiofrequency field inhomogeneity [23]. A device of Kataoka et al. study [24], suggests to include on women’s body a dielectric pad, whose function is to absorbe and eliminate reflexes waves, reducing interference [25–27], thus obtaining quality imaging vantages. Patients referred no discomfort due to the use of the pad. Time procedure of 3 T system remains equal to 1.5 T system. Limits of our study were the heterogeneous population and the small number of patients, especially affected by deep endometriosis; by the way the radiologists were aware of the clinical condition of the patients. The small number of patients affected by deep endometriosis involving the sacral nerves did not allow us to perform a significant statistical correlation between these data and the pain. Furthermore the MR has been installed by our department just few months ago and is still in progressive implementation; the signal inhomogeneity might have affected our study (Figs. 5 and 6). 5. Conclusions Pelvic MRI performed with 3 T system guarantees high spatial and contrast resolution, providing accurate information about endometriosis implants, with a good pre-surgery mapping of the lesions involving both bowels and bladder surface and rectouterine ligaments. T2 w FSE sequences resulted useful in the evaluation of deep implants and adhesions. However, studies based on wider population and with optimal correction of technical parameters are necessary in order to increase the diagnostic possibilities. References
. Sensibility
Specificity
PPV
NPV
90%
100.00%
100.00%
92.86%
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