1 Department of Radiology, Hopital Necker, 161, Rue de Sevres, 75743 Paris, Cedex 15, 2 CIERM, Hopital Bicetre, Le Kremlin-Bicetre and 3 Department of Gynecological Surgery, Clinique Universitaire Baudelocque, CHU Cochin, 123, Blvd. Port Royal, 75014 Paris, France
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Abstract |
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Key words: : endometriosis/intracavitary coils/MRI/surface coils/uterosacral ligaments
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Introduction |
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Although magnetic resonance (MR) imaging is currently used for the diagnosis of ovarian endometriosis (Togashi et al., 1991; Sugimura et al., 1992
), it has not been recommended for the primary evaluation of peritoneal endometriosis. One reason is the low sensitivity of MR imaging for superficial endometrial implants and adhesions (Arrivé et al., 1989; Bis et al., 1997
). Because no previous study evaluates the value of MR imaging in diagnosing deep endometriosis, including uterosacral ligaments, the purpose of our study is to describe MR findings of histopathologically proven deep endometriosis.
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Materials and methods |
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MR imaging
MR imaging was performed with a 1.5 T unit (Signa 4.5; GE Medical Systems, Milwaukee, WI, USA) using first either a body coil (n = 12) or a torso coil (n = 8), followed by image acquisition with an endorectal cervix receiver coil (Medrad, Pittsburgh, PA, USA). All image acquisition was monitored by a radiologist aware of the clinical and other imaging modality findings. For closer proximity to the lesions, the endorectal coil was positioned in the vagina in 17 patients and in the rectum in three patients. Axial and sagittal T2-weighted fast spin echo images [repetition time, 4000 ms; echo time, 104 ms (4000/104)] and axial T1-weighted (500/10) spin echo images were obtained with 5 mm thick contiguous sections. For images obtained with the body coil or the torso coil, two signals were acquired with a 256x192 matrix and a 2432 cm field of view. For images obtained with the endorectal coil, four signals were acquired with a 256x256 matrix and a 16x16 cm field of view. Superior saturation pulse and no-phase wrap options were used for both body coil imaging and intracavitary coil imaging. Patients with T1 hyperintense lesions underwent a fat suppressed T1-weighted spin echo sequence. Four patients with nodules in the vesico-uterine pouch underwent contrast-enhanced T1- and T2-weighted fat suppressed spin echo images.
The MR images were analysed prospectively by a board certified independent reader, who was aware of the clinical suspicion of deep endometriosis, but blinded to the results of physical examination, other imaging modality results or histopathology. The reader was asked to identify any lesion of the uterosacral ligaments, the pouch of Douglas, the rectum or the vesicouterine pouch. The following parameters were recorded for each uterosacral ligament: (a) visibility on axial and/or sagittal T2-weighted and/or axial T1-weighted images; (b) morphology: presence of a nodule, size and interface to adjacent organs; and (c) signal intensity on T2-weighted fast spin echo and T1-weighted spin echo images in reference to the myometrium.
Morphology (shape, size and margins), signal intensity on unenhanced T1- and T2-weighted images and homogeneity were recorded for all other lesions. Possible extension of the lesion into the bladder detrusor, the ureters or the muscularis propria of the rectum was noted and compared to results of surgery and histopathology. The presence of endometriomas was noted for each patient. No attempt was made to diagnose superficial implants or adhesions.
MR imaging findings were compared to clinical results, findings of other imaging modalities, such as transvaginal ultrasound, rectal echoendoscopy, cystoscopy and intravenous pyelography (IVP), when available, to the video of intraoperative gross appearance and the results of histopathology.
Lesion classification
Uterosacral ligaments were considered normal when physical examination and laparoscopic inspection and palpation were normal. Histopathological criteria of deep endometriosis were the presence of both endometriotic glands and stromal tissue infiltrating the peritoneum >5 mm in depth. Lesions in the vesicouterine pouch extending into the bladder detrusor were classified as endometriosis of the bladder.
Statistical analysis
Morphology and signal intensity on T2-weighted images were compared between normal uterosacral ligaments and uterosacral ligaments infiltrated by deep endometriosis. The statistical analysis used the 2 two-tailed test in order to evaluate if abnormal uterosacral ligaments were different from normal uterosacral ligaments. A P value of < 0.05 was considered to indicate a statistically significant difference.
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Results |
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Lesions of uterosacral ligaments (n = 12)
Laparoscopic palpation diagnosed 28 normal and 12 abnormal uterosacral ligaments. Histopathology confirmed infiltration by deep endometriosis in all 12 removed uterosacral ligaments.
T2-weighted fast spin echo images identified 86% (24/28) of normal uterosacral ligaments and 100% (12/12) of uterosacral ligaments with deep endometriosis. A markedly lateral positioned cervix (n = 2) or indistinct margins between the rectosigmoid and the cervix (n = 2) prevented us from identifying four normal uterosacral ligaments. T1-weighted SE images identified 25% (7/28) of normal uterosacral ligaments and 50% (6/12) of uterosacral ligaments with deep endometriosis; all were isointense to myometrium. Non-visualization of uterosacral ligaments on T1-weighted images was due to the presence of surrounding pelvic organs (small bowel, rectum) isointense to the uterus.
Uterosacral ligaments with deep endometriosis were irregular due to the presence of a proximal nodule measuring between 10 and 18 mm in largest diameter (mean 13.4 mm) (Figures 13). T2-signal intensity of the nodule was iso- (6/12), hypo- (5/12) or hyperintense to the myometrium (1/12); the nodule was isointense (6/6) when identified on T1-weighted SE imaging. Pathology showed abundant fibrosis with small clusters of endometriotic glandular tissue in uterosacral ligaments with T2 hypo- or isointensity. The T2 hyperintense uterosacral ligaments correlated with multiple clusters of endometriotic glandular tissue and minimal stromal reaction on histopathology.
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Comparison between uterosacral ligaments with and without deep endometriosis showed significant differences in nodularity (P = 0.001) and no differences in T2 signal intensity. Irregularity with presence of a proximal nodule on a uterosacral ligament was highly indicative of deep endometriosis.
Two lesions of uterosacral ligaments extended to the rectal muscularis propria. The normal hyposignal of the rectal muscularis propria was visible only in patients presenting a distended rectum, as it occurred incidentally by the intrarectal position of the receiver coil. Deep rectal wall invasion corresponded to an interruption of the hyposignal of the rectal muscular propria on T2-weighted spin echo images (Figure 1b). Extension to the rectum could not be analysed in patients with an endovaginal position of the coil due to absent rectal distension.
Comparison between MR results and physical examination showed a lower detection rate of abnormal uterosacral ligaments on physical examination (10/12) than on T2-weighted imaging (12/12). Two abnormal uterosacral ligaments were missed clinically in two patients presenting with bilateral nodules of deep endometriosis in each uterosacral ligament. None of the normal uterosacral ligaments presented with a nodule either at MR imaging or at physical examination.
Lesions of the rectum (n = 3)
Two patients complaining about tenesma presented with three nodules of deep endometriosis of the rectal wall at pathology. Preoperative diagnoses had been performed by transrectal ultrasound and confirmed by surgery and histopathology. MR imaging prospectively identified one of the three lesions. This lesion was positioned 8 cm above the anus and measured 15 mm in largest diameter. MR images showed asymmetric T2 isointense thickening of the rectal wall at 8 cm from the anus. In one patient with two rectal lesions, measuring 10 and 20 mm and located in the rectosigmoid segment, at 12 and 15 cm respectively from the anus, motility artefacts impaired accurate assessment of the rectal wall. MR images obtained with the endorectal coil could not provide interpretable images above 8 cm from the anus in both patients. Positioning of the intrarectal coil higher in the rectum, above the level of the cervix, was limited by the patient's symptoms.
Lesions of the pouch of Douglas (n = 2)
Two patients presented with a nodule in the pouch of Douglas, measuring 15 and 18 mm in largest diameter and extending either into the rectal or into the rectovaginal wall. On T2-weighted fast spin echo images the signal intensity of deep endometriosis of the pouch of Douglas was isointense to myometrium and homogeneous in one patient (Figure 4), and isointense and heterogeneous due to hyperintense spots in the other patient. Signal intensity on T1-weighted images was iso-intense and homogenous in both patients. Both lesions were suspected at physical examination.
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Discussion |
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Our study demonstrated that MR imaging was able to detect abnormal uterosacral ligaments. The sensitivity of lesion detection was significantly higher with T2-weighted images (100%) than with T1-weighted images (50%). Although the sensitivity for normal uterosacral ligament detection was low, 25 and 86% respectively for T1- and T2-weighted imaging, the purpose of our study was not to detect all uterosacral ligaments, but specifically those that will require surgical excision. Our findings do not agree with the study of Arrivé et al. (1989), who reported that endometrial implants on uterosacral ligaments were not visible on MR imaging. These differences may be due to more severe endometriosis in our study populations and a thinner section thickness of 5 versus 10 mm on T2-weighted spin echo MR images. Low T2-signal intensity correlated with abundant stromal fibrosis on pathology. Fibrosis is known to be hypointense to muscle on T2-weighted images (Ebner et al., 1988) and might be due to a long evolution of endometriosis. Our results confirm the study of Siegelman et al. (1994) describing eight solid pelvic masses caused by endometriosis as being predominantly hypointense on T2-weighted images and of intermediate signal intensity on T1-weighted images. In order to differentiate those nodules from the surrounding isointense cervical stroma or myometrium, morphological features of abnormality become a more important diagnostic argument.
Our results further demonstrated that MR imaging could reliably differentiate normal from abnormal uterosacral ligaments. The comparative analysis between normal and infiltrated uterosacral ligaments showed a significant difference in the proximal morphology of the ligaments. Deep endometriosis infiltrating uterosacral ligaments differed from normal uterosacral ligaments by the presence of a proximal nodule >9 mm. Signal intensity was of no use in differentiating normal from infiltrated uterosacral ligaments as iso- or hypointense signal intensity was found in both groups. If we had applied the diagnostic criteria of `nodularity of uterosacral ligaments' to our study population, we could have yielded a maximum sensitivity and specificity of 100% for deep endometriosis of uterosacral ligaments. Our results need to be interpreted in the context of clinical suspicion of deep endometriosis occurring more frequently in patients with previously diagnosed and treated endometriosis (Chapron and Dubuisson, 1996). Indeed our high sensitivity of 100% for depiction of deep endometriosis in uterosacral ligaments is most likely overestimated due to the 30% prevalence of this type of lesion in our study population. Nevertheless, the lower sensitivity of physical examination, the difficulty of prelaparoscopic palpation and the fact that results of surgery depend on total excision of the lesion, emphasize the usefulness of MR imaging before surgery. Further prospective studies are necessary in order to confirm the excellent diagnostic results of MR imaging in deep endometriosis of uterosacral ligaments.
In the patients with rectal endometriosis or with deep endometriosis in uterosacral ligaments extending to the rectal wall, a more aggressive surgery with partial resection of the rectum is required (Coronado et al., 1990; Nezhat et al., 1992
). Staging of deep rectal involvement is therefore helpful for patient management. Our results show a low sensitivity of 33% for rectal lesion invasion by our MR imaging technique. In women with rectal endometriosis, the mobility of the endorectal coil is limited by the clinical symptoms, therefore preventing imaging levels >8 cm from the anal border. The endovaginal position of the coil was shown a higher tolerance by the patient, but did not distend the rectal wall and could not image levels above the cervix. Rectal contrast administration distending the rectal wall and use of combined pelvic phase array and endovaginal coils might represent a better technical option for detailed anatomic information on the rectal wall. Nevertheless, endorectal ultrasound combines good results, high feasibility and lower costs than MR imaging, and seems to represent a more available technique for rectal wall extension than MR imaging (Ohba et al., 1996
; Schroder et al., 1997
).
Our one-third rate of bladder endometriosis in a population with suspicion of deep endometriosis was higher than that reported in women with all types of endometriosis. Our results demonstrated that bladder endometriosis can be diagnosed on MR imaging by morphologic abnormalities, including localized or diffuse bladder wall thickening and signal intensity abnormalities. On T2-weighted images, 71% of the patients with bladder endometriosis presented with spots of high signal intensity in an abnormal thickening of the bladder wall. Our study did not address whether these signs allow differentiation from bladder cancer which usually does not occur in young women. Contrast-enhanced MR images, obtained with an endovaginal coil, allowed precise staging of bladder endometriosis by demonstrating invasion of the detrusor by an extrinsic bladder mass. Indirect diagnostic arguments in favour of bladder endometriosis were the association with ovarian endometriomas and/or other lesions of endometriosis in 71% of our patients. MR imaging of the bladder was abnormal even in the patients with normal cystoscopy results or without urinary symptoms. The high false negative rate of cystoscopy in bladder endometriosis has been reported in other studies (Savoca et al., 1996; Vercellini et al., 1996
). As endometriosis seldom invades the mucosa, lesion identification remains difficult but might be optimized by performing cystoscopy during menstruation. Indeed in two of our patients with bladder endometriosis and negative initial cystoscopy, results were positive at a subsequent cystoscopy during menstruation, performed after the MR diagnosis and only 23 weeks after the first cystoscopy. Compared to transvaginal ultrasound, MR imaging allowed more accurate localization of the nodule in the bladder wall and ruled out the diagnosis of subserosal uterine fibroid. Our results did not confirm recently reported superiority of transvaginal ultrasound over MR imaging in assessing bladder endometriosis (Fedele et al., 1997
). Technical differences, such as intravenous injection of contrast media and endovaginal receiver coils, might explain differences in MR results between studies. Intravenous pyelography was more sensitive than MR imaging in diagnosing extension of the bladder mass to the distal ureter. The different surgical treatment options for bladder endometriosis include laparoscopic or laparotomic partial bladder resection (Dubuisson et al., 1994
; Nezhat et al., 1996
) or urological endoresection during cystoscopy. Preoperative knowledge of the accurate extent of bladder endometriosis guides patient orientation to a trained referral centre. Although MR imaging is not specific for bladder endometriosis, it can detect morphological and signal abnormality of the bladder highly suggestive of endometriosis in patients that might present with other sites of extraperitoneal involvement. The advantage of MR imaging combined with intravenous pyelography is the accurate evaluation of most extraperitoneal sites of involvement, contents of a pelvic mass and lesions hidden by dense adhesions. If bladder or rectal endometriosis is suspected, the endovaginal MR imaging protocol should include intravenous contrast for lesions in the bladder and rectal contrast for lesions in the rectum. Technically, optimal and individually adapted pelvic MR imaging might contribute to better patient management.
In conclusion, MR imaging can diagnose deep endometriosis of uterosacral ligaments by demonstrating a proximal nodule. Staging of possible urinary or rectal endometriosis requires the use of intravenous or intrarectal contrast media for optimal MR imaging results. In those circumstances, preoperative MR imaging can guide laparoscopic treatment planning and might improve patient management.
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Notes |
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References |
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Submitted on May 12, 1998; accepted on December 21, 1998.