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Correlation between three-dimensional rectosonography and magnetic resonance imaging in the diagnosis of rectosigmoid endometriosis: a preliminary study on the first fifty cases
European Journal of Obstetrics & Gynecology and Reproductive Biology 187 (2015) 35–40
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European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Correlation between three-dimensional rectosonography and magnetic resonance imaging in the diagnosis of rectosigmoid endometriosis: a preliminary study on the first fifty cases Charles-Andre´ Philip a,c,*, Christian Bisch a, Agne´s Coulon b, Pierre de Saint-Hilaire a, Rene´-Charles Rudigoz a, Gil Dubernard a,c a
Obstetric and Gynecology Department, Croix-Rousse University Hospital of Lyon, France Radiology Department, Croix-Rousse University Hospital of Lyon, 103, Grande rue de la Croix-Rousse, Lyon, 69004 France c Universite´ Claude Bernard Lyon 1, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 July 2014 Received in revised form 26 January 2015 Accepted 6 February 2015
Objectives: Deep infiltrating endometriosis (DIE) raises a number of diagnostic and therapeutic problems. Magnetic resonance imaging (MRI), the reference technique in endometriosis, is questioned for posterior pelvic lesions, especially in rectosigmoid locations. In this study, we describe a new technique called three-dimensional rectosonography (3D-RSG), which combines standard transvaginal ultrasonography (TVUS), 3-dimensional (3D) ultrasonography and the use of water for rectal contrast. We also assess the correlation between 3D-RSG and MRI in the diagnosis of rectosigmoid endometriosis. Study design: This study included 50 consecutive women with symptoms suggestive of DIE. After colorectal enema, they underwent a gynecological examination and a 3D TVUS during which 120 ml of water was injected in the rectosigmoid to improve the performance of the examination. All patients also underwent an MRI and surgery was offered to the patient if there was discordance between the two procedures. Results: Fifty women underwent 3D-RSG between May and November 2012. All procedures were well tolerated by patients. Two examinations (4%) were stopped for technical reasons. Nineteen rectosigmoid nodules were diagnosed in 18 women (36%). Eighteen of these nodules were also identified on MRI, and one (2%) nodule seen on MRI was not diagnosed by 3D-RSG. In 31 examinations (62%), neither technique identified an intestinal lesion. There was a concordance rate of 96% between the two techniques. Using MRI as the reference technique, 3D-RSG had a sensitivity of 0.95, a specificity of 0.97, a positive predictive values of 0.95, and a negative predictive value of 0.97. There was a 30.3 positive likelihood ratio and a 0.05 negative likelihood ratio. Conclusions: 3D-RSG seems an interesting new method for diagnosis of rectosigmoid endometriosis and is both feasible and well tolerated. 3D-RSG is highly concordant with MRI in this indication, although further studies are needed to confirm these primary results. ß 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Deeply infiltrating endometriosis Intestinal endometriosis Rectosonography Transvaginal ultrasonography Preoperative assessment
Introduction Deep infiltrating endometriosis (DIE) is characterized by endometriotic implants that penetrate the retroperitoneal space for a distance of 5 mm or more [1]. Although the exact prevalence of bowel endometriosis is unknown, it is estimated to occur in between 3.8 and 37% of patients with endometriosis [2]. The most
* Corresponding author at: Obstetric and Gynecology Department, Croix-Rousse University Hospital of Lyon, France. Tel.: +33 4 72 07 19 36; fax: +33 4 72 07 16 65. E-mail address: [email protected] (C.-A. Philip). http://dx.doi.org/10.1016/j.ejogrb.2015.02.006 0301-2115/ß 2015 Elsevier Ireland Ltd. All rights reserved.
frequent location is the rectum (59%), followed by the sigmoid (21%), the rest of the colon (9%), the ileocaecum (6%), and the appendix (3%) [3,4]. DIE is responsible for pain symptoms and gastrointestinal disorders, which can decrease a woman’s quality of life [5]. Although these symptoms are associated with DIE [6,7], they are not specific to the severity or location of the lesions [3,8]. As patients with intestinal endometriosis often have lesions in multiple pelvic locations, the diagnosis is particularly difficult and it is not easy to locate the precise source of complains. Imaging techniques are therefore mandatory.
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Magnetic resonance imaging (MRI), transvaginal ultrasonography (TVUS), and rectal endoscopic sonography (RES) have all been proposed to confirm intestinal infiltration by endometriosis, and MRI has been reported to be the best noninvasive examination for assessing DIE [9]. Several studies, however, have shown that RES [10] and TVUS [11–13] are superior to MRI for the diagnosis of rectosigmoid lesions. In this study, we first describe the technique of 3-dimensional rectosonography (3D-RSG), a new TVUS technique with intrarectal contrast for assessing bowel endometriosis. Our principal objective was to assess the concordance between the results of 3D-RSG and those of MRI. Our secondary objectives were the assessment of the performance of 3D-RSG using MRI as the reference technique and the evaluation of the feasibility and reproducibility of the procedure. Materials and methods Study and population Between May and November 2012, we included 50 consecutive women referred to the endometriosis center of Croix-Rousse University Hospital (Lyon, France) with clinical suspicion of endometriosis. All 50 women reported gastrointestinal symptoms suggestive of posterior DIE. The study was submitted to the SUDEST II ethics committee, which classified the treatment provided as usual care (Reference number: CAL 2013-028-2). Rectosonography protocol (3D-RSG) The 3D-RSG procedure has been published previously [14]. We obtained 2D and 3D images with the VOLUSON E8 (GE Healthcare Ultrasound, Milwaukee, WI, USA) fitted with a 3D transvaginal multifrequency transducer (2.9–10 MHz). All women had colorectal preparation by enema (Normacol1 adult rectal solution, 130 ml, 23.66 g sodium-dihydrogen phosphate/sodium monohydrogen 10.4 g, NORGINE PHARMA) twice, at 2 h and 1 h before the procedure. All procedures were performed according to the same protocol by the same operator (GD) and were interpreted in real time. First, a clinical gynecological examination was performed, followed by a standard TVUS examination looking for adenomyosis, endometrioma and DIE. During this first step, the posterior vaginal wall and posterior vaginal fornix were examined carefully to search for rectovaginal and rectosigmoid endometriotic lesions. In the second step, the patients slowly injected themselves with 120 ml of warm water into the rectum using a 60-mL syringe with conical tip. The operator then repeated the TVUS, using the distention of the bowel by water to increase the contrast and improve the quality of the rectosigmoid exploration. The anterior rectal wall was transvaginally examined, followed by the sigmoid as far as it was possible to go. The various layers of the intestinal wall were examined from outside to inside. The serosal layer appears as a thin hyperechoic line, the muscularis propria as two hypoechoic lines, and finally the submucosal and mucosal layer as a unique hyperechoic line (Figs. 1 and 2). Bowel involvement was suspected when a solid hypoechoic nodule adhered to the serosal layer and infiltrated the intestinal muscularis (Fig. 3). Each time, several 3D TVUS acquisitions of the posterior compartment were performed, especially when intestinal infiltration was suspected. The structures of interest visualized during the 3D acquisition were the uterosacral ligaments, vaginal apex, rectovaginal septum, rectosigmoid colon, and rectum. After acquisition, the multiplanar display showed a sagittal view, an axial plane and a coronal plane (Fig. 4A). The coronal plane could not have been obtained with conventional 2D sonography. Several
Fig. 1. Standard transvaginal ultrasonography (TVUS). Standard TVUS shows the normal layers of the bowel. The vaginal wall (A) hypoechoic, the serosal layer (B) hyperechoic, the muscularis mucosae (C) as two hypoechoic lines and then the submucosal and mucosal layers (D) hyperechoic.
3D image programs were used for off-line analysis. The virtual organ computer-aided analysis (VOCAL) mode was used to assess the volume of the DIE (Fig. 4A), and the tomographic ultrasound imaging (TUI) mode provided series of slices through any one of these planes (Fig. 4B). The TUI display was modified to provide the maximum of number of slices in the region of interest (ROI) and thus obtain a better appreciation of intestinal wall infiltration. At the end of the procedure, we used the surface mode to reconstruct the endometriotic nodule entirely, in a kind of virtual colonoscopy that allowed us to assess the intestinal stenosis caused by the nodule (Fig. 5). All 3D volumes were separately reviewed by a single operator (CAP) blinded to the results of the initial report, at least 6 month after the procedure using 4DVIEW software for PC (GE Healthcare). MRI protocol Before the procedure started, all patients underwent colorectal preparation by an enema. An antispasmodic drug was also administered at the outset of the examination to reduce bowel peristalsis. Around 50 ml of ultrasonographic gel was introduced into the vaginal canal to distend it. The images were acquired on a 1.5-T device (MAGNETOM Avanto 1.5 T, SIEMENS Healthcare,
Fig. 2. Normal 2-dimensional rectosonography (RSG). In rectosonography, the intrarectal contrast increases the visibility of the normal layers. There is the vaginal wall (A) next to the probe, followed by the serosal layer (B), the muscularis mucosae (C) and then the submucosal and mucosal layers (D). The digestive wall is easily visible thanks to the contrast in the lumen (E).
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Fig. 3. Endometriosis nodule in 2-dimensional RSG. In 2-dimensional rectosonography, a nodule appears like a heterogeneous hypoechoic lesion (A), which here expands the normal hypoechoic muscularis (D). The intrarectal contrast (C) helps to shape the luminal side of the nodule. The submucosal and the mucosal layers (B) are also thickened by inflammatory reaction but seem not invaded.
Erlangen, Germany), with a protocol including sagittal and axial fast spin-echo T2-weighted images and gradient echo T1-weighted images with and without fat suppression, both before and after injection of gadolinium. When the procedure suggested an infiltration of the intestinal wall, around 120 ml of water was introduced into the rectum with a urinary catheter.
Fig. 5. Endometriosis nodule in 3D-RSG with surface mode. In 3D rectosonography with surface mode, it is possible to achieve a sort of virtual coloscopy (A), which allows the assessment of the digestive tract stenosis due to an endometriotic nodule (white star). In this case, the stenosis reaches more than 50% of the lumen (B).
The performances of the different sequences were not compared. Each examination was interpreted according to a standardized protocol by two radiologists (A.C. and E.M.) with experience in gynecologic imaging and blinded to the results of the 3D-RSG. The diagnosis of DIE was based on the presence of either hyperintense foci on T1-weighted MRIs, or small hyperintense cavities on T2-weighted images, combined with morphologic abnormalities or areas corresponding to fibrosis. These features were evaluated at each site of posterior DIE. Rectosigmoid colon endometriosis was defined by the disappearance of the fat tissue plane lying between the uterus and the rectosigmoid, its replacement by a tissue mass, and the disappearance of the hypointense signal of the anterior wall of the rectum/sigmoid colon on T2-weighted images, with contrast enhancement on T1weighted images [12]. Surgical procedure In accordance with the guidance of our ethical committee, surgical assessment of the lesion was not systematically performed in this study. Indeed, the first-line treatments in our endometriosis center are the medical therapies. Thus a systematical surgical procedure was offered to patients only in cases of discordance between 3D-RSG and MRI findings. Statistical analysis
Fig. 4. Endometriosis nodule in 3D-RSG with triplan mode. The Triplan mode is the most common tridimensional mode; it shows the lesion in the three spatial planes. After this acquisition, the VOCAL1mode (virtual organ computer-aided analysis) (A) can be used to assess the volume of an endometriotic nodule. The TUI mode (tomographic ultrasound imaging) (B) provided series of slices which allows an extensive analysis of the nodule in the wall of the digestive tract.
The concordance between 3D-RSG and MRI was defined by the sum of identical diagnoses (both positive or both negative) divided by the total number of patients. To assess the performances of 3DRSG, we calculated its sensitivity and specificity for rectosigmoid endometriotic infiltration using MRI as the reference technique. Positive predictive values (PPV), negative predictive values (NPV), and positive and negative likelihood ratios (LR+ and LR ) were also calculated to determine the performance of these tests in predicting the presence or absence of bowel disease. To determine
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the precision of the results, we also calculated 95% confidence intervals (95% CI). The Chi2 test was used to analyze the data (R Core Team1 2008 by the R Foundation for Statistical Computing). The tests were considered to be: very useful if LR+ >10 and LR <0.1; moderately useful if 5 < LR+ < 10 and 0.1 < LR < 0.2; somewhat useful if 2 < LR + < 5; and 0.2
Results Clinical examination Table 1 summarizes the women’s characteristics. The mean age was 35.3 years (range from 22 to 51). Ninety percent of the patients had been pregnant, and 60% had given birth. Twenty patients (40%) had been diagnosed as infertile and 15 (30%) had already been treated with medically assisted procreation. Feasibility and results of 3D-rectosonography All 50 women agreed to the examination after the technique was explained, and no examination was stopped at the woman’s request. Two procedures were stopped by the examiner for technical reasons: one (2%) for an inadequate bowel preparation and one (2%) because of too much water leakage to the upper sigmoid resulting in a lack of rectal contrast. In the other 48 procedures, all three layers of the digestive wall were visualized and followed to the second loop of the sigmoid (between 10 cm and 15 cm). The procedure was therefore feasible and well tolerated in 96% of cases. In 3D-RSG, nineteen rectosigmoid nodules were found in 18 patients (38%). Six (31.6%) were visualized in the rectal wall and 13 (68.4%) in the sigmoid wall. The mean diameter was 19.9 mm (SD = 7.23) for a median volume of 1.02 ml (SD = 0.9). The distance from the anus was not estimated, but all lesions were located in the upper third of the rectovaginal septum and beyond. The ‘‘blinded’’ reviewing of all 3D volumes at 6 months found the same diagnosis in all 50 cases (100%). 3D-RSG performances with MRI as the reference technique All 50 women underwent both 3D-RSG and MRI. Eighteen of the 20 intestinal nodules (90%) were diagnosed by both MRI and 3DRSG. In two cases the findings of MRI and 3D-RSG were discordant. Table 1 Characteristics of patients.
Age (years) Graviditya Paritya Infertilityb ARTc,b Age at menarche (years)a Age at first symptoms (years)a Menarche to first symptoms (years)a
35.3 0.9 0.6 20 (40%) 15 (30%) 12.7 18.7 6
Previous medical treatmentb Estrogen-progestinb Progestinb GnRH agonistb
37 27 24 10
Previous surgery for endometriosisb Endometriomab
27 (54%) 17 (34%)
a b c
Data are presented as mean (%). Data are presented as number (%). Assisted reproductive technologies (ART).
Comment To our knowledge, this is the first original study to report TVUS combining intrarectal contrast and 3D imaging in intestinal endometriosis. In this publication we describe the detailed technique of this new procedure. 3D-RSG appears feasible, reproducible and well tolerated, with only two procedures stopped for technical reasons. Twenty endometriotic nodules of the rectosigmoid were reported in this series of 50 patients. There was a 96% concordance between 3D-RSG and MRI. A blinded review at 6 months of all the 3D procedures found exactly the same results as the initial procedure combining 2D and 3D-TVUS. 3DRSG seems satisfactory using MRI as the reference technique with a sensibility, specificity, PPV and NPV of 95%, 97%, 95% and 97% respectively. It appears to be a useful technique according to the LR+ and the LR- of 30.3 and 0.05 respectively [15,16]. Our study shows that 3D-RSG is feasible and well tolerated in 96% of the cases, since no patient asked that the procedure be stopped, and only two procedures were interrupted by the operator due to technical problems. These results are not surprising since intestinal opacification is used routinely in pelvic MRI without major functional discomfort for patients. Indeed, Ferrero et al. reported that pain during TVUS with intrarectal contrast (mean VAS 4.2) was lower than during CT colonography (mean VAS 5.3) [17]. Standard TVUS is known to be an excellent technique in the diagnosis of rectosigmoid endometriosis with experienced operators [12,13,18–20]. In a meta-analysis, Hudelist et al. reported for TVUS a sensitivity of 91% and a specificity of 95% [21]. Similarly in Table 2 3D RSG & MRI concordance and 3DRSG performances using MRI as the reference technic. Procedures results (n = 50a)
Patients characteristics (n = 50) a
The two techniques concurred in finding no intestinal lesion in 31 examinations. There was a concordance rate of 96% between the two techniques. We also evaluated the 3D-RSG performance, using MRI results as the reference technique. The sensitivity, specificity, PPV and NPV were of 95%, 97%, 95% and 97% respectively. There was a 30.3 positive likelihood ratio and a 0.05 negative likelihood ratio (Table 2). In both cases with discordant diagnosis, an endometriotic lesion of the recto-sigmoid was confirmed at surgery. As the majority of other patients did not undergo surgery, the performance of 3D-RSG and MRI using surgery as the reference technique has not been estimated.
(74%) (54%) (48%) (20%)
(Range 20–51) (Range 0–3) (Range 0–3)
(Range 9–16) (Range 11–45) (Range 0–31)
Chi2 = 38.92; p < 0.0001 3D-RSG (+) 3D-RSG ( ) Total
MRI (+)
MRI ( )
18 1 19
1 31 32
Performances (CI 95%)b Global concordance Sensitivity
0.96 [0.85;0.99] 0.95 [0.68;0.97]
Specificity
PPVc
0.95 [0.68;0.97]
NPVd
LR(+)e a b c d e
30.3 [4.4;209.3]
LR( )e
The difference is related to a patient with two lesions. Confidence Interval. Positive predictive value (PPV). Negative predictive value (NPV). Likelihood ratio (LR); Positive (+); Negative ( ).
Total
19 32 51a
0.97 [0.84;0.99] 0,97 [0.84;0.99] 0.05 [0.01;0.37]
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three studies, TVUS seems at least equal, if not superior, to MRI, which has sensitivity ranging from 78 to 87% and specificity ranging from 92 to 98% [12,13,22]. These results make the TVUS, for some authors, the best first-line technique line when posterior deep endometriosis is suspected [23]. In our study, the performances of 3D-RSG seem higher than those reported in the literature for standard TVUS and MRI, although this needs to be confirmed in future studies using surgery as the gold standard. The use of the MRI as the reference technique in our study can be discussed, as the gold standard commonly used in the literature is surgery in combination with histology. However, the international recommendation remains unclear about the need for surgery to assess endometriosis [24]. Indeed, as the first-line recommended treatment is medical therapy and the imaging techniques are proven to be reliable, surgery is not offered systematically in our center to patients with radiological evidence of endometriosis. Surgical assessment is reserved for patients with clinico-radiological discordance or cases resistant to medical treatment. As reported above, surgery was performed in the two patients in whom discordance between 3D-RSG and MRI was observed. We confirmed the presence of an endometriotic lesion in both of them. A larger study using surgery as the gold standard is currently ongoing. Abrao et al. reported that mechanical cleansing of the lower bowel by means of a rectal enema 1 h before TVS enables the best identification of the different bowel layers [13]. We also performed this bowel preparation twice, by two rectal enemas, before starting the procedure. The advantage of using contrast for the diagnosis of posterior DIE in MRI has been demonstrated [25]: it improves sensitivity and specificity and decreases interpretation time. In TVUS, two Italian series showed a significant trend in favor of TVUS with intrarectal contrast compared to standard TVUS and RES for the diagnosis of rectosigmoid lesions [26,27], with a 97% detection rate for digestive endometriosis. Accordingly, we believe that the use of intrarectal contrast accelerates the learning curve and plays an important role in the diagnostic accuracy of 3D-RSG. Visibility of the anterior wall was much better after contrast injection and the posterior wall of the intestine was useful for creating a kind of control mirror image (Fig. 3). Further studies comparing the performance of standard TVUS and 3D-RSG are necessary, however, to confirm the benefits of intrarectal contrast. The contribution of 3D in our study is also difficult to assess due to the lack of comparison between standard TVUS and 3D ultrasound. In 2009, Guerriero et al. first described the 3D sonography characteristics of DIE and concluded that the higher spatial resolution of 3D ultrasound could improve characterization of DIE [28]. In a series of 19 patients with surgery as the reference, Pascual et al. reported a trend toward higher sensitivity with 3D probes (94.7%) [29]. Conversely, Guerriero et al. recently reported a series of 129 patients with a higher diagnostic accuracy in favor of 3D-TVUS (but without contrast) against 2D-TVUS, in posterior DIE without digestive involvement. Surprisingly there was no significant difference between the two techniques for rectosigmoid localization [30]. In addition to its diagnostic performance, however, the main benefit of 3D-RSG is the characterization of lesions with clearer distinction between the intestinal layers, calculation of volumes with the VOCAL mode, and more useful images with the TUI and surface modes. The surface mode allows a kind of virtual colonoscopy that is valuable to assess bowel stenosis (Fig. 5) and prepare surgical management. The ability to store the 3D data seems also interesting because it allows a retrospective analysis of the volumes, which is reproducible in this study. These results allow us to propose a centralized review in ‘‘Endometriosis expertise centers’’ of 3D-RSG volumes performed by external practitioners.
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Conclusion Although further studies are needed to confirm these primary results, 3D-RSG seems satisfactory for the diagnosis of rectosigmoid endometriosis. Condensation Three-dimensional rectosonography, a new sonography technique in rectosigmoid endometriosis, seems feasible and correlated with magnetic resonance imaging after review of 50 procedures. Acknowledgments The authors would like to thank Mrs. Kelly Hess for her contribution to the English language editing. Declaration of conflicts of interest All authors report no potential conflicts of interest except Christian Bisch who performed « Septimus » formations for GE Healthcare1. References [1] Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ. Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 1991;55:759–65. [2] Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. Obstet Gynecol Surv 2007;62:461–70. [3] Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;18:157–61. [4] Chapron C, Chopin N, Borghese B, et al. Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution. Hum Reprod 2006;21:1839–45. [5] Dubernard G, Piketty M, Rouzier R, Houry S, Bazot M, Darai E. Quality of life after laparoscopic colorectal resection for endometriosis. Hum Reprod 2006;21:1243–7. [6] Chapron C, Dubuisson JB, Pansini V, et al. Routine clinical examination is not sufficient for diagnosing and locating deeply infiltrating endometriosis. J Am Assoc Gynecol Laparosc 2002;9:115–9. [7] Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Breart G. Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis. Fertil Steril 2002;78:719–26. [8] Koninckx PR, Martin D. Treatment of deeply infiltrating endometriosis. Curr Opin Obstet Gynecol 1994;6:231–41. [9] Bazot M, Darai E, Hourani R, et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004;232:379–89. [10] Chapron C, Vieira M, Chopin N, et al. Accuracy of rectal endoscopic ultrasonography and magnetic resonance imaging in the diagnosis of rectal involvement for patients presenting with deeply infiltrating endometriosis. Ultrasound Obstet Gynecol 2004;24:175–9. [11] Bazot M, Detchev R, Cortez A, Amouyal P, Uzan S, Darai E. Transvaginal sonography and rectal endoscopic sonography for the assessment of pelvic endometriosis: a preliminary comparison. Hum Reprod 2003;18:1686–92. [12] Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I, Darai E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 2009;92:1825–33. [13] Abrao MS, Goncalves MO, Dias Jr JA, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Hum Reprod 2007;22:3092–7. [14] Philip CA, Bisch C, Coulon A, et al. Three-dimensional (3D) rectosonography: description of a new 3D transvaginal ultrasonography technique with intrarectal contrast to assess colorectal endometriosis. Ultrasound Obstet Gynecol 2015;45:233–5. [15] Jaeschke R, Guyatt GH, Sackett DL. Users’ guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group. J Am Med Assoc 1994;271:703–7. [16] Nendaz MR, Perrier A. [Bayes theorem and likelihood ratios. Rev Mal Respir 2004;21:394–7. [17] Ferrero S, Biscaldi E, Morotti M, et al. Multidetector computerized tomography enteroclysis vs. rectal water contrast transvaginal ultrasonography in determining the presence and extent of bowel endometriosis. Ultrasound Obstet Gynecol 2011;37:603–13.
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European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Correlation between three-dimensional rectosonography and magnetic resonance imaging in the diagnosis of rectosigmoid endometriosis: a preliminary study on the first fifty cases Charles-Andre´ Philip a,c,*, Christian Bisch a, Agne´s Coulon b, Pierre de Saint-Hilaire a, Rene´-Charles Rudigoz a, Gil Dubernard a,c a
Obstetric and Gynecology Department, Croix-Rousse University Hospital of Lyon, France Radiology Department, Croix-Rousse University Hospital of Lyon, 103, Grande rue de la Croix-Rousse, Lyon, 69004 France c Universite´ Claude Bernard Lyon 1, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 July 2014 Received in revised form 26 January 2015 Accepted 6 February 2015
Objectives: Deep infiltrating endometriosis (DIE) raises a number of diagnostic and therapeutic problems. Magnetic resonance imaging (MRI), the reference technique in endometriosis, is questioned for posterior pelvic lesions, especially in rectosigmoid locations. In this study, we describe a new technique called three-dimensional rectosonography (3D-RSG), which combines standard transvaginal ultrasonography (TVUS), 3-dimensional (3D) ultrasonography and the use of water for rectal contrast. We also assess the correlation between 3D-RSG and MRI in the diagnosis of rectosigmoid endometriosis. Study design: This study included 50 consecutive women with symptoms suggestive of DIE. After colorectal enema, they underwent a gynecological examination and a 3D TVUS during which 120 ml of water was injected in the rectosigmoid to improve the performance of the examination. All patients also underwent an MRI and surgery was offered to the patient if there was discordance between the two procedures. Results: Fifty women underwent 3D-RSG between May and November 2012. All procedures were well tolerated by patients. Two examinations (4%) were stopped for technical reasons. Nineteen rectosigmoid nodules were diagnosed in 18 women (36%). Eighteen of these nodules were also identified on MRI, and one (2%) nodule seen on MRI was not diagnosed by 3D-RSG. In 31 examinations (62%), neither technique identified an intestinal lesion. There was a concordance rate of 96% between the two techniques. Using MRI as the reference technique, 3D-RSG had a sensitivity of 0.95, a specificity of 0.97, a positive predictive values of 0.95, and a negative predictive value of 0.97. There was a 30.3 positive likelihood ratio and a 0.05 negative likelihood ratio. Conclusions: 3D-RSG seems an interesting new method for diagnosis of rectosigmoid endometriosis and is both feasible and well tolerated. 3D-RSG is highly concordant with MRI in this indication, although further studies are needed to confirm these primary results. ß 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Deeply infiltrating endometriosis Intestinal endometriosis Rectosonography Transvaginal ultrasonography Preoperative assessment
Introduction Deep infiltrating endometriosis (DIE) is characterized by endometriotic implants that penetrate the retroperitoneal space for a distance of 5 mm or more [1]. Although the exact prevalence of bowel endometriosis is unknown, it is estimated to occur in between 3.8 and 37% of patients with endometriosis [2]. The most
* Corresponding author at: Obstetric and Gynecology Department, Croix-Rousse University Hospital of Lyon, France. Tel.: +33 4 72 07 19 36; fax: +33 4 72 07 16 65. E-mail address: [email protected] (C.-A. Philip). http://dx.doi.org/10.1016/j.ejogrb.2015.02.006 0301-2115/ß 2015 Elsevier Ireland Ltd. All rights reserved.
frequent location is the rectum (59%), followed by the sigmoid (21%), the rest of the colon (9%), the ileocaecum (6%), and the appendix (3%) [3,4]. DIE is responsible for pain symptoms and gastrointestinal disorders, which can decrease a woman’s quality of life [5]. Although these symptoms are associated with DIE [6,7], they are not specific to the severity or location of the lesions [3,8]. As patients with intestinal endometriosis often have lesions in multiple pelvic locations, the diagnosis is particularly difficult and it is not easy to locate the precise source of complains. Imaging techniques are therefore mandatory.
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Magnetic resonance imaging (MRI), transvaginal ultrasonography (TVUS), and rectal endoscopic sonography (RES) have all been proposed to confirm intestinal infiltration by endometriosis, and MRI has been reported to be the best noninvasive examination for assessing DIE [9]. Several studies, however, have shown that RES [10] and TVUS [11–13] are superior to MRI for the diagnosis of rectosigmoid lesions. In this study, we first describe the technique of 3-dimensional rectosonography (3D-RSG), a new TVUS technique with intrarectal contrast for assessing bowel endometriosis. Our principal objective was to assess the concordance between the results of 3D-RSG and those of MRI. Our secondary objectives were the assessment of the performance of 3D-RSG using MRI as the reference technique and the evaluation of the feasibility and reproducibility of the procedure. Materials and methods Study and population Between May and November 2012, we included 50 consecutive women referred to the endometriosis center of Croix-Rousse University Hospital (Lyon, France) with clinical suspicion of endometriosis. All 50 women reported gastrointestinal symptoms suggestive of posterior DIE. The study was submitted to the SUDEST II ethics committee, which classified the treatment provided as usual care (Reference number: CAL 2013-028-2). Rectosonography protocol (3D-RSG) The 3D-RSG procedure has been published previously [14]. We obtained 2D and 3D images with the VOLUSON E8 (GE Healthcare Ultrasound, Milwaukee, WI, USA) fitted with a 3D transvaginal multifrequency transducer (2.9–10 MHz). All women had colorectal preparation by enema (Normacol1 adult rectal solution, 130 ml, 23.66 g sodium-dihydrogen phosphate/sodium monohydrogen 10.4 g, NORGINE PHARMA) twice, at 2 h and 1 h before the procedure. All procedures were performed according to the same protocol by the same operator (GD) and were interpreted in real time. First, a clinical gynecological examination was performed, followed by a standard TVUS examination looking for adenomyosis, endometrioma and DIE. During this first step, the posterior vaginal wall and posterior vaginal fornix were examined carefully to search for rectovaginal and rectosigmoid endometriotic lesions. In the second step, the patients slowly injected themselves with 120 ml of warm water into the rectum using a 60-mL syringe with conical tip. The operator then repeated the TVUS, using the distention of the bowel by water to increase the contrast and improve the quality of the rectosigmoid exploration. The anterior rectal wall was transvaginally examined, followed by the sigmoid as far as it was possible to go. The various layers of the intestinal wall were examined from outside to inside. The serosal layer appears as a thin hyperechoic line, the muscularis propria as two hypoechoic lines, and finally the submucosal and mucosal layer as a unique hyperechoic line (Figs. 1 and 2). Bowel involvement was suspected when a solid hypoechoic nodule adhered to the serosal layer and infiltrated the intestinal muscularis (Fig. 3). Each time, several 3D TVUS acquisitions of the posterior compartment were performed, especially when intestinal infiltration was suspected. The structures of interest visualized during the 3D acquisition were the uterosacral ligaments, vaginal apex, rectovaginal septum, rectosigmoid colon, and rectum. After acquisition, the multiplanar display showed a sagittal view, an axial plane and a coronal plane (Fig. 4A). The coronal plane could not have been obtained with conventional 2D sonography. Several
Fig. 1. Standard transvaginal ultrasonography (TVUS). Standard TVUS shows the normal layers of the bowel. The vaginal wall (A) hypoechoic, the serosal layer (B) hyperechoic, the muscularis mucosae (C) as two hypoechoic lines and then the submucosal and mucosal layers (D) hyperechoic.
3D image programs were used for off-line analysis. The virtual organ computer-aided analysis (VOCAL) mode was used to assess the volume of the DIE (Fig. 4A), and the tomographic ultrasound imaging (TUI) mode provided series of slices through any one of these planes (Fig. 4B). The TUI display was modified to provide the maximum of number of slices in the region of interest (ROI) and thus obtain a better appreciation of intestinal wall infiltration. At the end of the procedure, we used the surface mode to reconstruct the endometriotic nodule entirely, in a kind of virtual colonoscopy that allowed us to assess the intestinal stenosis caused by the nodule (Fig. 5). All 3D volumes were separately reviewed by a single operator (CAP) blinded to the results of the initial report, at least 6 month after the procedure using 4DVIEW software for PC (GE Healthcare). MRI protocol Before the procedure started, all patients underwent colorectal preparation by an enema. An antispasmodic drug was also administered at the outset of the examination to reduce bowel peristalsis. Around 50 ml of ultrasonographic gel was introduced into the vaginal canal to distend it. The images were acquired on a 1.5-T device (MAGNETOM Avanto 1.5 T, SIEMENS Healthcare,
Fig. 2. Normal 2-dimensional rectosonography (RSG). In rectosonography, the intrarectal contrast increases the visibility of the normal layers. There is the vaginal wall (A) next to the probe, followed by the serosal layer (B), the muscularis mucosae (C) and then the submucosal and mucosal layers (D). The digestive wall is easily visible thanks to the contrast in the lumen (E).
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Fig. 3. Endometriosis nodule in 2-dimensional RSG. In 2-dimensional rectosonography, a nodule appears like a heterogeneous hypoechoic lesion (A), which here expands the normal hypoechoic muscularis (D). The intrarectal contrast (C) helps to shape the luminal side of the nodule. The submucosal and the mucosal layers (B) are also thickened by inflammatory reaction but seem not invaded.
Erlangen, Germany), with a protocol including sagittal and axial fast spin-echo T2-weighted images and gradient echo T1-weighted images with and without fat suppression, both before and after injection of gadolinium. When the procedure suggested an infiltration of the intestinal wall, around 120 ml of water was introduced into the rectum with a urinary catheter.
Fig. 5. Endometriosis nodule in 3D-RSG with surface mode. In 3D rectosonography with surface mode, it is possible to achieve a sort of virtual coloscopy (A), which allows the assessment of the digestive tract stenosis due to an endometriotic nodule (white star). In this case, the stenosis reaches more than 50% of the lumen (B).
The performances of the different sequences were not compared. Each examination was interpreted according to a standardized protocol by two radiologists (A.C. and E.M.) with experience in gynecologic imaging and blinded to the results of the 3D-RSG. The diagnosis of DIE was based on the presence of either hyperintense foci on T1-weighted MRIs, or small hyperintense cavities on T2-weighted images, combined with morphologic abnormalities or areas corresponding to fibrosis. These features were evaluated at each site of posterior DIE. Rectosigmoid colon endometriosis was defined by the disappearance of the fat tissue plane lying between the uterus and the rectosigmoid, its replacement by a tissue mass, and the disappearance of the hypointense signal of the anterior wall of the rectum/sigmoid colon on T2-weighted images, with contrast enhancement on T1weighted images [12]. Surgical procedure In accordance with the guidance of our ethical committee, surgical assessment of the lesion was not systematically performed in this study. Indeed, the first-line treatments in our endometriosis center are the medical therapies. Thus a systematical surgical procedure was offered to patients only in cases of discordance between 3D-RSG and MRI findings. Statistical analysis
Fig. 4. Endometriosis nodule in 3D-RSG with triplan mode. The Triplan mode is the most common tridimensional mode; it shows the lesion in the three spatial planes. After this acquisition, the VOCAL1mode (virtual organ computer-aided analysis) (A) can be used to assess the volume of an endometriotic nodule. The TUI mode (tomographic ultrasound imaging) (B) provided series of slices which allows an extensive analysis of the nodule in the wall of the digestive tract.
The concordance between 3D-RSG and MRI was defined by the sum of identical diagnoses (both positive or both negative) divided by the total number of patients. To assess the performances of 3DRSG, we calculated its sensitivity and specificity for rectosigmoid endometriotic infiltration using MRI as the reference technique. Positive predictive values (PPV), negative predictive values (NPV), and positive and negative likelihood ratios (LR+ and LR ) were also calculated to determine the performance of these tests in predicting the presence or absence of bowel disease. To determine
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the precision of the results, we also calculated 95% confidence intervals (95% CI). The Chi2 test was used to analyze the data (R Core Team1 2008 by the R Foundation for Statistical Computing). The tests were considered to be: very useful if LR+ >10 and LR <0.1; moderately useful if 5 < LR+ < 10 and 0.1 < LR < 0.2; somewhat useful if 2 < LR + < 5; and 0.2
Results Clinical examination Table 1 summarizes the women’s characteristics. The mean age was 35.3 years (range from 22 to 51). Ninety percent of the patients had been pregnant, and 60% had given birth. Twenty patients (40%) had been diagnosed as infertile and 15 (30%) had already been treated with medically assisted procreation. Feasibility and results of 3D-rectosonography All 50 women agreed to the examination after the technique was explained, and no examination was stopped at the woman’s request. Two procedures were stopped by the examiner for technical reasons: one (2%) for an inadequate bowel preparation and one (2%) because of too much water leakage to the upper sigmoid resulting in a lack of rectal contrast. In the other 48 procedures, all three layers of the digestive wall were visualized and followed to the second loop of the sigmoid (between 10 cm and 15 cm). The procedure was therefore feasible and well tolerated in 96% of cases. In 3D-RSG, nineteen rectosigmoid nodules were found in 18 patients (38%). Six (31.6%) were visualized in the rectal wall and 13 (68.4%) in the sigmoid wall. The mean diameter was 19.9 mm (SD = 7.23) for a median volume of 1.02 ml (SD = 0.9). The distance from the anus was not estimated, but all lesions were located in the upper third of the rectovaginal septum and beyond. The ‘‘blinded’’ reviewing of all 3D volumes at 6 months found the same diagnosis in all 50 cases (100%). 3D-RSG performances with MRI as the reference technique All 50 women underwent both 3D-RSG and MRI. Eighteen of the 20 intestinal nodules (90%) were diagnosed by both MRI and 3DRSG. In two cases the findings of MRI and 3D-RSG were discordant. Table 1 Characteristics of patients.
Age (years) Graviditya Paritya Infertilityb ARTc,b Age at menarche (years)a Age at first symptoms (years)a Menarche to first symptoms (years)a
35.3 0.9 0.6 20 (40%) 15 (30%) 12.7 18.7 6
Previous medical treatmentb Estrogen-progestinb Progestinb GnRH agonistb
37 27 24 10
Previous surgery for endometriosisb Endometriomab
27 (54%) 17 (34%)
a b c
Data are presented as mean (%). Data are presented as number (%). Assisted reproductive technologies (ART).
Comment To our knowledge, this is the first original study to report TVUS combining intrarectal contrast and 3D imaging in intestinal endometriosis. In this publication we describe the detailed technique of this new procedure. 3D-RSG appears feasible, reproducible and well tolerated, with only two procedures stopped for technical reasons. Twenty endometriotic nodules of the rectosigmoid were reported in this series of 50 patients. There was a 96% concordance between 3D-RSG and MRI. A blinded review at 6 months of all the 3D procedures found exactly the same results as the initial procedure combining 2D and 3D-TVUS. 3DRSG seems satisfactory using MRI as the reference technique with a sensibility, specificity, PPV and NPV of 95%, 97%, 95% and 97% respectively. It appears to be a useful technique according to the LR+ and the LR- of 30.3 and 0.05 respectively [15,16]. Our study shows that 3D-RSG is feasible and well tolerated in 96% of the cases, since no patient asked that the procedure be stopped, and only two procedures were interrupted by the operator due to technical problems. These results are not surprising since intestinal opacification is used routinely in pelvic MRI without major functional discomfort for patients. Indeed, Ferrero et al. reported that pain during TVUS with intrarectal contrast (mean VAS 4.2) was lower than during CT colonography (mean VAS 5.3) [17]. Standard TVUS is known to be an excellent technique in the diagnosis of rectosigmoid endometriosis with experienced operators [12,13,18–20]. In a meta-analysis, Hudelist et al. reported for TVUS a sensitivity of 91% and a specificity of 95% [21]. Similarly in Table 2 3D RSG & MRI concordance and 3DRSG performances using MRI as the reference technic. Procedures results (n = 50a)
Patients characteristics (n = 50) a
The two techniques concurred in finding no intestinal lesion in 31 examinations. There was a concordance rate of 96% between the two techniques. We also evaluated the 3D-RSG performance, using MRI results as the reference technique. The sensitivity, specificity, PPV and NPV were of 95%, 97%, 95% and 97% respectively. There was a 30.3 positive likelihood ratio and a 0.05 negative likelihood ratio (Table 2). In both cases with discordant diagnosis, an endometriotic lesion of the recto-sigmoid was confirmed at surgery. As the majority of other patients did not undergo surgery, the performance of 3D-RSG and MRI using surgery as the reference technique has not been estimated.
(74%) (54%) (48%) (20%)
(Range 20–51) (Range 0–3) (Range 0–3)
(Range 9–16) (Range 11–45) (Range 0–31)
Chi2 = 38.92; p < 0.0001 3D-RSG (+) 3D-RSG ( ) Total
MRI (+)
MRI ( )
18 1 19
1 31 32
Performances (CI 95%)b Global concordance Sensitivity
0.96 [0.85;0.99] 0.95 [0.68;0.97]
Specificity
PPVc
0.95 [0.68;0.97]
NPVd
LR(+)e a b c d e
30.3 [4.4;209.3]
LR( )e
The difference is related to a patient with two lesions. Confidence Interval. Positive predictive value (PPV). Negative predictive value (NPV). Likelihood ratio (LR); Positive (+); Negative ( ).
Total
19 32 51a
0.97 [0.84;0.99] 0,97 [0.84;0.99] 0.05 [0.01;0.37]
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three studies, TVUS seems at least equal, if not superior, to MRI, which has sensitivity ranging from 78 to 87% and specificity ranging from 92 to 98% [12,13,22]. These results make the TVUS, for some authors, the best first-line technique line when posterior deep endometriosis is suspected [23]. In our study, the performances of 3D-RSG seem higher than those reported in the literature for standard TVUS and MRI, although this needs to be confirmed in future studies using surgery as the gold standard. The use of the MRI as the reference technique in our study can be discussed, as the gold standard commonly used in the literature is surgery in combination with histology. However, the international recommendation remains unclear about the need for surgery to assess endometriosis [24]. Indeed, as the first-line recommended treatment is medical therapy and the imaging techniques are proven to be reliable, surgery is not offered systematically in our center to patients with radiological evidence of endometriosis. Surgical assessment is reserved for patients with clinico-radiological discordance or cases resistant to medical treatment. As reported above, surgery was performed in the two patients in whom discordance between 3D-RSG and MRI was observed. We confirmed the presence of an endometriotic lesion in both of them. A larger study using surgery as the gold standard is currently ongoing. Abrao et al. reported that mechanical cleansing of the lower bowel by means of a rectal enema 1 h before TVS enables the best identification of the different bowel layers [13]. We also performed this bowel preparation twice, by two rectal enemas, before starting the procedure. The advantage of using contrast for the diagnosis of posterior DIE in MRI has been demonstrated [25]: it improves sensitivity and specificity and decreases interpretation time. In TVUS, two Italian series showed a significant trend in favor of TVUS with intrarectal contrast compared to standard TVUS and RES for the diagnosis of rectosigmoid lesions [26,27], with a 97% detection rate for digestive endometriosis. Accordingly, we believe that the use of intrarectal contrast accelerates the learning curve and plays an important role in the diagnostic accuracy of 3D-RSG. Visibility of the anterior wall was much better after contrast injection and the posterior wall of the intestine was useful for creating a kind of control mirror image (Fig. 3). Further studies comparing the performance of standard TVUS and 3D-RSG are necessary, however, to confirm the benefits of intrarectal contrast. The contribution of 3D in our study is also difficult to assess due to the lack of comparison between standard TVUS and 3D ultrasound. In 2009, Guerriero et al. first described the 3D sonography characteristics of DIE and concluded that the higher spatial resolution of 3D ultrasound could improve characterization of DIE [28]. In a series of 19 patients with surgery as the reference, Pascual et al. reported a trend toward higher sensitivity with 3D probes (94.7%) [29]. Conversely, Guerriero et al. recently reported a series of 129 patients with a higher diagnostic accuracy in favor of 3D-TVUS (but without contrast) against 2D-TVUS, in posterior DIE without digestive involvement. Surprisingly there was no significant difference between the two techniques for rectosigmoid localization [30]. In addition to its diagnostic performance, however, the main benefit of 3D-RSG is the characterization of lesions with clearer distinction between the intestinal layers, calculation of volumes with the VOCAL mode, and more useful images with the TUI and surface modes. The surface mode allows a kind of virtual colonoscopy that is valuable to assess bowel stenosis (Fig. 5) and prepare surgical management. The ability to store the 3D data seems also interesting because it allows a retrospective analysis of the volumes, which is reproducible in this study. These results allow us to propose a centralized review in ‘‘Endometriosis expertise centers’’ of 3D-RSG volumes performed by external practitioners.
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Conclusion Although further studies are needed to confirm these primary results, 3D-RSG seems satisfactory for the diagnosis of rectosigmoid endometriosis. Condensation Three-dimensional rectosonography, a new sonography technique in rectosigmoid endometriosis, seems feasible and correlated with magnetic resonance imaging after review of 50 procedures. Acknowledgments The authors would like to thank Mrs. Kelly Hess for her contribution to the English language editing. Declaration of conflicts of interest All authors report no potential conflicts of interest except Christian Bisch who performed « Septimus » formations for GE Healthcare1. References [1] Koninckx PR, Meuleman C, Demeyere S, Lesaffre E, Cornillie FJ. Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 1991;55:759–65. [2] Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. Obstet Gynecol Surv 2007;62:461–70. [3] Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;18:157–61. [4] Chapron C, Chopin N, Borghese B, et al. Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution. Hum Reprod 2006;21:1839–45. [5] Dubernard G, Piketty M, Rouzier R, Houry S, Bazot M, Darai E. Quality of life after laparoscopic colorectal resection for endometriosis. Hum Reprod 2006;21:1243–7. [6] Chapron C, Dubuisson JB, Pansini V, et al. Routine clinical examination is not sufficient for diagnosing and locating deeply infiltrating endometriosis. J Am Assoc Gynecol Laparosc 2002;9:115–9. [7] Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Breart G. Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis. Fertil Steril 2002;78:719–26. [8] Koninckx PR, Martin D. Treatment of deeply infiltrating endometriosis. Curr Opin Obstet Gynecol 1994;6:231–41. [9] Bazot M, Darai E, Hourani R, et al. Deep pelvic endometriosis: MR imaging for diagnosis and prediction of extension of disease. Radiology 2004;232:379–89. [10] Chapron C, Vieira M, Chopin N, et al. Accuracy of rectal endoscopic ultrasonography and magnetic resonance imaging in the diagnosis of rectal involvement for patients presenting with deeply infiltrating endometriosis. Ultrasound Obstet Gynecol 2004;24:175–9. [11] Bazot M, Detchev R, Cortez A, Amouyal P, Uzan S, Darai E. Transvaginal sonography and rectal endoscopic sonography for the assessment of pelvic endometriosis: a preliminary comparison. Hum Reprod 2003;18:1686–92. [12] Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I, Darai E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 2009;92:1825–33. [13] Abrao MS, Goncalves MO, Dias Jr JA, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Hum Reprod 2007;22:3092–7. [14] Philip CA, Bisch C, Coulon A, et al. Three-dimensional (3D) rectosonography: description of a new 3D transvaginal ultrasonography technique with intrarectal contrast to assess colorectal endometriosis. Ultrasound Obstet Gynecol 2015;45:233–5. [15] Jaeschke R, Guyatt GH, Sackett DL. Users’ guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group. J Am Med Assoc 1994;271:703–7. [16] Nendaz MR, Perrier A. [Bayes theorem and likelihood ratios. Rev Mal Respir 2004;21:394–7. [17] Ferrero S, Biscaldi E, Morotti M, et al. Multidetector computerized tomography enteroclysis vs. rectal water contrast transvaginal ultrasonography in determining the presence and extent of bowel endometriosis. Ultrasound Obstet Gynecol 2011;37:603–13.
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