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Genitourinary Imaging |
1 From the Departments of Nuclear Medicine and Diagnostic Imaging (M.L.K., K.T., T.Y., T.K., H.U., H.K.), Epidemiological and Clinical Research Information Management (M.R.), and Obstetrics and Gynecology (T.H., S.F.), Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Received August 26, 2003; revision requested November 4; final revision received May 7, 2004; accepted June 17. Address correspondence to M.L.K. (e-mail: milliam@kuhp.kyoto-u.ac.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Institutional review board approval was not required for this retrospective study, but informed consent was obtained from all patients. MR images obtained between January 1989 and December 2000 in 57 women (mean age, 39 years; age range, 26–52 years) with histologically confirmed endometriosis were retrospectively evaluated by four radiologists independently. All patients underwent laparotomy or laparoscopy less than 1 month after MR imaging. MR images were evaluated for the presence and location of endometrial implants and adhesions. MR images were also scored for the presence of five findings: retroflexed uterus, elevated posterior vaginal fornix, intestinal tethering or tethered appearance of rectum in direction of uterus, faint strands between uterus and intestine, and fibrotic plaque or nodule covering serosal surface of the uterus. Interobserver agreement for each of the five findings and for the overall diagnosis of cul-de-sac obliteration was calculated. Sensitivity, specificity, accuracy, positive and negative predictive values, and 
statistics were determined.
RESULTS: Laparotomy or laparoscopy revealed posterior cul-de-sac obliteration in 30 patients. Overall, the four radiologists had mean accuracies of 89.0% and 76.3% for diagnosing endometrial implants and adhesions, respectively, at MR imaging. Overall, the radiologists achieved mean sensitivity, specificity, accuracy, and positive and negative predictive values of 68.4%, 76.0%, 71.9%, 76.6%, and 68.5%, respectively, in diagnosing posterior cul-de-sac obliteration. The best accuracy (mean value, 64.5%) was obtained with the finding of fibrotic plaque in the uterine serosal surface. Readers agreed on the observations 63.2%–91.2% of the time. For the impression of the presence or absence of posterior cul-de-sac obliteration, interobserver agreement varied between substantial and moderate: Mean interobserver agreement was 78.4% (range, 70.2%–84.2%), and mean was 0.57 (range, 0.40–0.67). Mean accuracy of MR imaging for diagnosing posterior cul-de-sac obliteration was 71.9%.
CONCLUSION: These results suggest that use of the described MR imaging findings may enable diagnosis of posterior cul-de-sac obliteration.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Results of pelvic mapping with either laparoscopy or laparotomy indicate that the cul-de-sac and uterosacral ligaments are the most common pelvic sites of involvement byendometriosis (3). Results of another study indicate that the frequency of endometriosis in the posterior cul-de-sac is up to 56% (4).
Physical findings for endometriosis are nonspecific. Possible signs of endometriosis include uterosacral or cul-de-sac nodularity, localized tenderness along the uterosacral ligaments and the cul-de-sac, and adnexal masses. In more advanced disease, there is association with increased pelvic adhesions, with the uterus often fixed in a retroflexed position, reduced mobility of the ovaries and fallopian tubes, and cul-de-sac obliteration (2,5).
Endometriosis is staged at laparoscopy according to a point system that is based on the presence, size, and depth of ovarian and peritoneal endometrial implants; the presence and extent of ovarian and tubal adhesions; and the degree of posterior cul-de-sac obliteration (6). However, when dense adhesions are present, the cul-de-sac cannot be accessed or evaluated with laparoscopy (7). Because the cul-de-sac is the most common site of pelvic involvement and because it may be inaccessible in some patients, magnetic resonance (MR) imaging is potentially of use for evaluating the cause of infertility or planning the surgical approach.
The purpose of our study was to retrospectively evaluate the accuracy of MR imaging in depicting posterior cul-de-sac obliteration in patients with endometriosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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This search yielded 57 patients aged 26–52 years (mean age, 39 years); these patients formed our study group. The interval between laparotomy or laparoscopy and MR imaging was 1–29 days (mean, 10.7 days). The patients had presented with one or more of the following symptoms: dysmenorrhea (n = 21), lower abdominal pain (n = 12), infertility (n = 12), hypermenorrhea (n = 10), abnormal genital bleeding (n = 4), pollakiuria (n = 2), lower abdominal distention (n = 2), lower abdominal mass (n = 2), pain in lower back (n = 2), and pain with defecation (n = 2). Two patients had no symptoms. There were final associated diagnoses of leiomyoma (n = 20), adenomyosis (n = 8), ovarian cystadenoma (n = 4), and ovarian dermoid cyst (n = 1) (not all patients had associated disorders). For studies involving retrospective clinical research, our institutional review board does not require its approval or informed consent. However, written informed consent was obtained from all patients treated in the Department of Gynecology for review of their records, files, and images for research and educational purposes.
MR Imaging
All examinations were performed with a 1.5-T MR imaging system (Signa; GE Medical Systems, Milwaukee, Wis). In 47 examinations, a body coil was used, and in 10 examinations, a phased-array torso coil was used for imaging the pelvis. Before the examination, 20 mg of hyoscine butylbromide (Buscopan; Boehringer Ingelheim, Higashine, Japan) was administered intramuscularly to reduce intestinal peristalsis.
Routine clinical sequences were used. Forty-seven patients underwent imaging performed with spin-echo techniques—specifically, intermediate- and T2-weighted double-echo sequences in the sagittal plane. The parameters for intermediate- and T2-weighted spin-echo imaging were as follows: repetition time msec/echo time msec, 2000/20 for intermediate-weighted imaging and 2000/70 for T2-weighted imaging; number of signals acquired, two; and field of view, 32 cm. The section thickness was 5 mm, with a 2.5-mm intersection gap and a 256 x 192–256 matrix. Ten patients underwent sagittal T2-weighted fast spin-echo imaging (4000–6000/86.9–135 [effective]; number of signals acquired, two or three; field of view, 26 cm) with a 512 x 256 matrix, a 5-mm section thickness, and a 2.5-mm intersection gap. All patients underwent sagittal T1-weighted spin-echo imaging (600/8–20; number of signals acquired, two or three; field of view, 24–32 cm) with a 512–256 x 192–256 matrix, a 5-mm section thickness and a 2.5-mm intersection gap. In 15 patients, T1-weighted spin-echo imaging was performed after administration of 0.1 mL per kilogram of body weight of gadopentate dimeglumine (Magnevist; Schering, Berlin, Germany), but these postcontrast images were not taken into consideration in the present study. Only one patient underwent fat-saturated T1-weighted imaging. Eight patients underwent T1-weighted or T2-weighted imaging in transverse planes.
Image Review
The MR images were retrospectively and independently reviewed by four radiologists (M.L.K., K.T., T.Y., and T.K., with 4, 18, 3, and 4 years of experience in pelvic MR image interpretation, respectively) who were aware that the patients had or were suspected of having endometriosis. The radiologists were blinded to the specific findings at laparoscopy or laparotomy. The readers specifically recorded the presence and location of endometrial implants (including ovarian endometriomas) and adhesions. The radiologists also noted the presence or absence of the following findings related to posterior cul-de-sac obliteration: (a) retroflexed uterus, (b) elevated posterior vaginal fornix, (c) intestinal tethering and/or a tethered appearance of the rectum in the direction of the uterus, (d) faint strands between the uterus and intestine, and (e) fibrotic plaque and/or nodule covering the serosal surface of the uterus (Figs 1, 2). Finally, independently from the detailed evaluation, the readers were asked for their impression about the presence or absence of posterior cul-de-sac obliteration—that is, they reported whether or not they thought posterior cul-de-sac obliteration was present.
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Endometrial implants were considered to be present when lesions had a hyperintense appearance on T1-weighted MR images, irrespective of their appearance on T2-weighted MR images (8–11). If endometrial lesions appear hypointense on both T1- and T2-weighted MR images (11), they are acute hematomas or nonpigmented lesions. Some researchers (12) have indicated that, because of the presence of hemorrhage, only pigmented lesions can be detected with nonenhanced MR imaging. We thought it would be difficult to identify nonpigmented hypointense lesions in our study, which did not involve contrast material–enhanced images. Consequently, we decided not to include these hypointense lesions as a finding indicating the presence of endometrial implants.
Ovarian endometrioma was diagnosed when a cyst that was entirely hyperintense on T1-weighted or fat-saturated T1-weighted images exhibited hypointense signal (usually mixed with hyperintense areas) on T2-weighted images ("shading") or when the lesion consisted of multiple entirely hyperintense cysts on T1-weighted or fat-saturated T1-weighted images ("multiplicity"), regardless of its signal intensity on T2-weighted images (9).
Adhesions were diagnosed when there was obliteration of fat planes with a lack of a clear interface between adjacent organs, spiculated low-signal-intensity stranding between the organs, and/or angulation and distortion of adjacent bowel loops. At evaluation of the images for findings related to posterior cul-de-sac obliteration, a tethered appearance of the rectum was diagnosed when the rectum had a teardrop shape, with its acute angle pointed toward the adhesion plane of the two ovaries (8,13). The posterior vaginal fornix was considered to be elevated when its upper level was superior to the level of the uterine isthmus, when its contour was angulated, and/or when its contour was subject to traction in the upper direction and stretching the vaginal wall.
The following MR imaging characteristics were considered to indicate the presence of nodules or plaques: areas of low to intermediate signal intensity with internal foci of high signal intensity on T1-weighted images, areas of uniform low signal intensity on T2-weighted images, and areas of enhancement corresponding to the abundant fibrous tissue seen in these lesions at histologic examination (14,15).
Obliteration without a definable mass, as opposed to obliteration in conjunction with implants or a mass in the cul-de-sac, indicates that the cul-de-sac is not accessible from the peritoneal space—that is, it is not accessible with an anterior approach at laparoscopy or laparotomy—owing to the presence of adhesions. The imaging findings that suggest the presence of obliteration without a definable mass are those that indicate the adhesion of bowel loops to the uterus; these findings are detailed among the five findings described earlier in the Image Review section.
Comparisons
MR imaging findings were compared with the results of laparoscopy in four patients and with laparotomy findings in the other 53 patients. The comparisons were performed by a radiologist (M.L.K.).
For comparison of MR imaging and surgical findings regarding the sites of involvement, the pelvis was divided into five regions: the right ovary, the left ovary, the serosal surface of the uterus, the posterior cul-de-sac, and "other."
Statistical Analysis
A site-by-site comparison of the presence or absence of endometriosis according to each of the four readers was performed so that we could calculate sensitivity, specificity, positive predictive values (PPVs), negative predictive values (NPVs), and accuracy. Mean values represent values averaged across the four readers.
With regard to posterior cul-de-sac obliteration, the sensitivity, specificity, PPV, NPV, and accuracy were assessed for each of the five findings and for the overall diagnosis of posterior cul-de-sac obliteration. Mean values represent values averaged across the four readers.
Sensitivity, specificity, PPV, NPV, and accuracy were also calculated for each combination of two, three, four, and five findings of posterior cul-de-sac obliteration for each reader. Images were considered to be positive for a combination of findings if each of the combined findings was present. The results with these combinations were compared with the results of the analyses described in the immediately preceding paragraph.
Interobserver agreement for each of the evaluated findings of posterior cul-de-sac obliteration was expressed for each pair of reviewers as a percentage of agreement and by using the statistic. The statistic is used to estimate the proportion of interobserver agreement beyond that expected by chance. Values were interpreted as follows: Values less than 0.00 represented poor, values between 0.00 and 0.20 represented slight, values between 0.21 and 0.40 represented fair, values between 0.41 and 0.60 represented moderate, values between 0.61 and 0.80 represented substantial, and values between 0.81 and 1.00 represented almost perfect agreement (16). The values were compared with zero (which indicates agreement by chance only) to assess their statistical significance.
A P value of less than .05 was considered to indicate a statistically significant difference. Data were analyzed with the DAG_Stat statistical software system (17).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Performance values achieved by the radiologists in diagnosing endometriosis are presented in Table 1. Overall, for the diagnosis of endometrial implants, the four radiologists achieved a mean sensitivity of 93.1%, a mean specificity of 54.1%, and a mean accuracy of 89.0%. Overall, for the diagnosis of adhesion, the radiologists achieved a mean sensitivity of 77.8%, a mean specificity of 50.0%, and a mean accuracy of 76.3%. Overall, for the diagnosis of posterior cul-de-sac obliteration, the radiologists achieved a mean sensitivity, specificity, accuracy, PPV, and NPV of 68.4%, 76.0%, 71.9%, 76.6%, and 68.5%, respectively.
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The values for interrater agreement between each pair of readers (readers 1 and 2, readers 1 and 3, readers 1 and 4, readers 2 and 3, readers 2 and 4, and readers 3 and 4) are summarized in Tables 4 and 5.
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Statistics for each pair of readers ranged between 0.29 and 0.83 (P < .05), indicating variable agreement.
For the radiologists’ impression of the presence or absence of posterior cul-de-sac obliteration, interrater agreement varied between substantial ( = 0.62– 0.67) and moderate ( = 0.40 and 0.45) (Table 5). The percentage agreement ranged from 70.2% to 84.2% (mean, 78.4%), and values varied between 0.40 and 0.67 (mean, 0.57).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Complete obliteration of the posterior pelvic cul-de-sac in women with endometriosis was first described by Cullen (21) and is identified when the rectosigmoid colon adheres across the posterior portion of the cervix, usually with fusion of the rectal wall to the uterosacral ligaments. This presentation of endometriosis is considered to be the most severe form of the disease and is the most difficult to treat surgically because of the presence of invasive endometriosis hidden under the area of obliteration. The association of severe dysmenorrhea with cul-de-sac adhesions has been observed in previous studies (22,23).
Unfortunately, however, imaging (with MR, computed tomography, or ultrasonography) is limited in its ability to depict adhesions, although it is excellent for identifying hemorrhagic masses. The literature regarding imaging in endometriosis gives importance to the detection of hemorrhagic masses and implants, especially with fat-saturated images. The detection of adhesions with MR imaging is difficult and is achieved with reference to secondary findings (8).
In this study, we evaluated the ability of MR imaging to enable diagnosis of endometrial implants and adhesions, with a particular focus on posterior cul-de-sac obliteration.
Our evaluation of the diagnosis of posterior cul-de-sac obliteration at MR imaging revealed that MR imaging performs well (mean accuracy, 71.9%). The images obtained in the sagittal plane were particularly useful for evaluating the cul-de-sac and rectum. Endometriosis is staged laparoscopically in terms of the "degree of posterior cul-de-sac obliteration," but, with MR imaging, we could not classify the degree of obliteration as partial or complete. Consequently, our classification was an all-or-nothing phenomenon. It is possible that kinematic studies might be better for evaluating the degree of obliteration, but further investigation is necessary to confirm this.
Among the findings present in cul-de-sac obliteration, we chose the ones that we considered most representative on the basis of our clinical experience, and we obtained the highest mean specificity, PPV, and accuracy with the finding of fibrotic plaque in the uterine serosal surface (84.3%, 76.8%, and 64.5%, respectively).
On the basis of our results, we propose that the major criteria for diagnosing cul-de-sac obliteration should consist of intestinal tethering and/or a tethered appearance of the rectum in the direction of the uterus (finding 3), strands between the uterus and intestine (finding 4), and a fibrotic plaque covering the serosal surface of the uterus (finding 5) because of their good specificity. The presence of a retroflexed uterus and elevation of the posterior vaginal fornix can be considered minor criteria because they should be combined with other findings to obtain good specificity in the diagnosis of obliteration.
In this study, we included all retroflexed uteri, but remember that retroflexion can be a normal variation of position. To increase the specificity of this finding, it is better to consider only those retroflexed uteri that seem distorted or beaked—that is, those with irregular configuration or shortening of the posterior surface of the uterus indicating a tethered appearance of the uterine wall itself.
The readers’ impression of cul-de-sac obliteration had a better performance than that obtained by combining all five findings assessed in the diagnosis of cul-de-sac obliteration. This was probably the case because, when the readers were asked for their impression, they considered not only the combination of findings present but also the severity of the assessed findings, in addition to considering the presence of other findings, such as endometrial cysts located inside or outside the posterior cul-de-sac.
For agreement regarding the five findings evaluated in the diagnosis of cul-de-sac obliteration, the statistic ranged from 0.29 to 0.83, indicating variable agreement. For impression of the presence or absence of posterior cul-de-sac obliteration, interobserver agreement was substantial ( = 0.62–0.67) to moderate ( = 0.40 and 0.45). Perhaps more training may improve the identification of abnormal findings.
Note that all criteria (except fibrotic plaques) used in this study are consequences of adhesions. Besides endometriosis, there are other causes of adhesion formation: pelvic inflammatory disease, trauma (including that caused by invasive surgical procedures), and neoplasms (24,25). However, identification of endometrial implants and fibrotic plaque along the posterior uterine surface strongly favors the diagnosis of endometriosis as a cause of the adhesion. MR imaging can be used to noninvasively disclose these findings on the basis of their signal intensity. The ability to enable a diagnosis on the basis of signal intensity is the advantage that MR imaging has over many other imaging modalities. It is important to characterize cul-de-sac obliteration because it has been clinically implicated as a probable cause of infertility and severe dysmenorrhea. If the cul-de-sac is obliterated, then, unless one attempts to free up the region at laparoscopy, the extent of disease actually present in this region will only be apparent at MR imaging.
The MR imaging–based diagnosis of cul-de-sac obliteration has at least two important clinical implications. First, a new endoscopic technique called transvaginal hydrolaparoscopy is contraindicated because a complete evaluation of all pelvic organs is not possible with this condition (26–28). Transvaginal hydrolaparoscopy involves the exploration of the pelvic structures with a mini-endoscope. Access is gained vaginally by using a needle puncture technique and saline for distention (26–28). Second, it has previously been reported that, in patients with complete obliteration of the cul-de-sac associated with endometriosis, the incidence of intestinal involvement is 82% and the incidence of rectal involvement is 73% (29). The surgical treatment that ensures good relief of the symptoms of complete obliteration of the cul-de-sac associated with endometriosis requires complete removal of all disease, which entails bowel resection in most patients (29). Therefore, a preoperative imaging finding of obliteration of the cul-de-sac must be taken as a warning of likely rectal involvement, and surgeons must be prepared to perform intestinal surgery.
Although laparoscopy is the standard of reference for the diagnosis of endometriosis, MR imaging has been shown to have advantages for characterizing endometriotic cysts and in the evaluation of extraperitoneal lesions and lesions hidden by dense adhesions that cannot be evaluated with laparoscopy (7). Our study results also indicate that the use of MR imaging may have advantages for identifying cul-de-sac obliteration when findings based on both morphology and signal intensity, such as the presence of fibrotic plaques and endometrial implants, are used. All of this information is essential for surgical planning and therefore makes important clinical contributions.
Several relatively recent articles have detailed the ability of kinematic MR imaging to depict motion, and consequently adhesions, among pelvic organs when a half-Fourier single-shot technique is used (30). The use of both kinematic and static MR imaging may provide further clues in the evaluation of adhesions.
Many authors have attempted to demonstrate the potential value of MR imaging in the diagnosis of endometriosis. In a study described recently (31), the sensitivity of MR imaging for detection of biopsy-proved endometriosis in any woman was 69% while the specificity was 75%; in that study, the utility of fat-saturated MR imaging in diagnosing implants was evaluated but, unfortunately, no attempt was made to diagnose adhesions. In a recent study (32), a staging system for pelvic endometriosis that was based on MR imaging features that were in turn based on the characteristics of endometriomas and implants yielded classifications that had a high level of agreement (96.8%) with laparoscopic classifications; this demonstrates a further advantage to the use of MR imaging in the preoperative staging of endometriosis.
For the evaluation of accuracy in the diagnosis of posterior cul-de-sac obliteration, we included only patients with confirmed endometriosis. It is possible that the gynecologists decided to perform laparoscopy or laparotomy in these patients after confirming the presence of positive MR imaging findings. This was a potential limitation of our study. The unavailability of fat-saturated images in many patients, the fact that a body coil was used in 47 patients, and the fact that the included cases were obtained during more than a decade, during which time technology changed, were other limitations. Also, all patients had endometriosis, and the radiologists knew that the patients were, at a minimum, suspected of having this disease.
In conclusion, MR imaging can be used as a noninvasive alternative for the diagnosis of posterior cul-de-sac obliteration, although it cannot replace laparoscopy in terms of accuracy.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, M.L.K., K.T.; study concepts and design, M.L.K., K.T., H.K.; literature research, M.L.K., H.U.; clinical studies, M.L.K., T.H., S.F.; data acquisition, M.L.K., K.T.; data analysis/interpretation, M.L.K., T.Y., T.K.; statistical analysis, M.L.K., M.R.; manuscript preparation and editing, M.L.K., K.T.; manuscript definition of intellectual content, M.L.K., K.T., H.K.; manuscript revision/review and final version approval, all authors
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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