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Genitourinary Imaging |
1 From the Department of Radiology, Georgetown University Medical Center, 3800 Reservoir Road NW, Washington DC, 20007. Received August 18, 1999; revision requested October 7; revision received December 14; accepted December 21. Supported in part by grants from Siemens Medical Systems and Berlex Laboratories. Address correspondence to R.C.J. (e-mail: jhar@gunct.georgetown.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: T1- and T2-weighted and dynamic gadolinium-enhanced T1-weighted images were obtained before and 3 months after UAE in 31 patients. Up to five fibroleiomyomata (total of 125) were evaluated for volume, location, signal intensity characteristics, and vascularity. Region-of-interest curves were used to assess the vascular enhancement pattern of each fibroleiomyoma and adjacent myometrium. Each patient completed a questionnaire on symptoms 3 months after UAE.
RESULTS: UAE resulted in significant reductions in mean uterine volume (from 588.6 to 393.1 cm3) and mean fibroleiomyoma volume (from 69.4 to 41.4 cm3) (P < .005). After UAE, lesions showed signal intensity changes consistent with hemorrhagic infarction. The vascularity of fibroleiomyomata was decreased (P < .001), with no significant change in myometrial vascularity. Submucosal location was a strong positive predictor of fibroleiomyoma volume reduction (P < 001). When a reduction in vascularity was the measure of success, hypervascularity was a strong indicator of success (P < .005).
CONCLUSION: MR imaging is useful for quantitative assessment of signal intensity and morphologic changes before and after UAE. Pretreatment MR imaging findings may help predict the success of the procedure.
Index terms: Arteries, therapeutic blockade, 969.1264 • Arteries, uterine • Leiomyoma, 854.319 • Uterine neoplasms, 854.319 • Uterine neoplasms, MR, 854.121411, 854.121412, 854.121415, 854.12143 • Uterine neoplasms, therapy, 854.1264
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Transcatheter uterine arterial embolization (UAE), which is traditionally performed for management of life-threatening gynecologic hemorrhage, has recently been used to treat symptomatic uterine fibroleiomyomata (4–10). Initial results (4–10) suggest that UAE leads to substantial improvement in symptoms. Although there have been a few reports (6,11,12) of the magnetic resonance (MR) imaging findings following UAE, to our knowledge there has not been a comprehensive MR imaging assessment of the morphology, signal intensity features, and vascular enhancement pattern of fibroleiomyomata before and after UAE.
The purposes of this study were (a) to determine the changes in MR imaging signal intensity, morphology, and vascularity of 125 uterine fibroleiomyomata after UAE and (b) to identify pretreatment MR imaging features most predictive of successful UAE, as defined by volume reduction or diminished vascularity of the fibroleiomyomata. We correlated these features with changes in symptoms after UAE.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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An experienced angiographer (J.B.S.) performed bilateral selective UAE by using 500–710-µm-diameter polyvinyl alcohol particles (Contour, Boston Scientific/Medi-tech, Natick, Mass; Ivalon, Cook, Bloomington, Ind; or Trufill, Cordis, Miami, Fla). The institutional review board gave approval for the entire study, and each patient gave written informed consent.
MR imaging was performed with a 1.5-T superconducting unit (Magnetom Vision; Siemens Medical System, Iselin, NJ) and a standard phased-array torso coil. Imaging was performed before and 3 months after embolization (mean interval, 122 days). Almost all patients underwent UAE within 1 month of the initial MR examination (mean, 25 days; range, 0–74 days). Table 1 delineates the imaging parameters. Patients fasted for 4 hours prior to MR imaging. All sequences required suspended respiration, with a total patient imaging time of less than 20 minutes. Dynamic images were acquired at 30, 60, and 90 seconds after intravenous injection of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Monteville, NJ) at a dose of 0.1 mmol per kilogram body weight.
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Data Evaluation
Three readers (R.C.J., I.I., S.M.A.) independently analyzed MR images for each patient. Each reader was given T1- and T2-weighted and gadolinium-enhanced T1-weighted images of each fibroleiomyoma and composite images of the uterus, with pre- and post-UAE images presented at the same time. Images of the uterus and of up to five index fibroleiomyomata (ie, masses that were known and had been selected and measured) were analyzed (total of 125 fibroleiomyomata before UAE and 120 fibroleiomyomata after UAE, because five fibroleiomyomata were too small to characterize). In patients with more than five fibroleiomyomata, the index fibroleiomyomata were generally selected on the basis of size and conspicuity on images obtained in orthogonal planes, although an attempt was made in each patient to include fibroleiomyomata of varying location, size, and morphology. Each fibroleiomyoma was evaluated for the following features: location (submucosal, intramural, subserosal, or other), volume, signal intensity, and, on gadolinium-enhanced images, vascularity.
The volumes of the uterus and of each index fibroleiomyoma were measured by using a prolate ellipse equation (length x width x height x 0.523). The reduction in uterine and fibroleiomyoma volume was calculated and expressed as a percentage, as follows: 100 x [Volumepre - Volumepost]/Volumepre], where Volumepre and Volumepost are the volumes before and after UAE, respectively.
The signal intensity of index fibroleiomyomata on nonenhanced T1-weighted and T2-weighted images was categorized as hyperintense, isointense, or hypointense to myometrium. T2-weighted images were also assessed for heterogeneity of fibroleiomyoma signal intensity.
Two methods of assessing vascularity were used. First, each examiner qualitatively assigned the degree of enhancement (hypervascular, isovascular, or hypovascular) of each fibroleiomyoma on images obtained before and after UAE. The enhancement of a fibroleiomyoma was compared with that of the myometrium at 30, 60, and 90 seconds after injection of contrast material. Second, for a quantitative assessment of vascularity, regions-of-interest (ROI) curves were generated from the dynamic data obtained during gadolinium enhancement (0, 30, 60, and 90 seconds after injection). The largest ROI that would encompass the index fibroleiomyoma was used, and an ROI was also placed on the adjacent normal-appearing myometrium. Another ROI was placed over the musculature of the anterior abdominal wall or paraspinal region to act as a standard, and a fourth was ROI placed in the background for the purpose of determining the contribution of noise from the MR imager (Figs 1, 2). An attempt was made to draw ROIs of similar size for the myometrium, paraspinal muscle, and background on pre- and post-UAE images for any given fibroleiomyoma. In five patients (20 index fibroleiomyomata) in whom 1-year follow-up MR images were available, a repeat analysis was performed.
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Interrater reliability among the three readers was determined with the 
statistic, an index of agreement corrected for chance that can take values of 0 or less for poor agreement, 0.01–0.40 for slight to fair agreement, 0.41–0.60 for moderate agreement, 0.61–0.80 for substantial agreement, and 0.81–1.00 for excellent agreement (13). The significance of changes in uterine volume from before to after UAE was assessed by using the Wilcoxon signed rank test. Changes in categoric variables were assessed by using the McNemar test.
Multiple fibroleiomyomata were sampled from each patient, which resulted in clustering of fibroleiomyomata within patients. We accounted for this clustering by using a random-effects analysis of variance or Huber-corrected estimates of the standard error (StataCorp, College Station, Tex). Means, standard errors, and t tests for reduction in fibroleiomyoma volume and vascularity were obtained from the results of the random-effects analysis of variance. A paired Student t test was used to assess changes in ROIs selected before and after UAE. To examine changes in ROI signal intensity for fibroleiomyomata, the myometrium, the paraspinal muscle, and background, we used a random-effects analysis of variance to model the effects of gadolinium enhancement (on images obtained 0, 30, 60, 90 seconds after injection), period (on pre- and post-UAE images), and the interaction between the two.
To identify pre-UAE variables that might help predict the success of UAE, we conducted backward stepwise multiple linear regression analyses to predict percentage reductions in fibroleiomyoma volume and vascularity. To account for the clustering within patients, we used Huber-corrected estimates of the standard error.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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values that describe the interrater reliability among the three readers for location, gadolinium-enhancement pattern, T1- and T2-weighted signal intensity, and T2-weighted signal intensity heterogeneity. All values were greater than 0.75, which reflected substantial agreement among the three readers.
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Changes in Signal Intensity Characteristics
The majority of fibroleiomyomata showed a change in T1-weighted signal intensity (Figs 1–3): Before UAE, eight (6%) of 125 lesions had high signal intensity, after embolization 68 (57%) of 120 lesions had high signal intensity. On T2 weighted images, the overwhelming majority of fibroleiomyomata had low signal intensity both before (116 [93%] of 125) and after (113 [94%] of 120) UAE. After UAE, however, 78 (65%) of 120 fibroleiomyomata showed a homogeneous decrease in T2-weighted signal intensity (Fig 3b), as compared with 56 (45%) of 125 fibroleiomyomata before UAE (P < .001).
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Quantitative changes in vascularity.—There was no significant difference in the sizes of the ROIs used for the myometrium (t = 1.55, P = .23), paraspinal muscle (t = 0.18, P = .861), and background (t = 0.80, P = .424). ROIs used for the fibroleiomyoma did change, however, as the fibroleiomyoma decreased in size (t = 5.26, P < .001).
Figure 4 shows the mean ROI curves measured before (Fig 4a) and after (Fig 4b) UAE. The pre-UAE fibroleiomyoma ROI curves differed from the post-UAE curves (P < .001), whereas the myometrium, and paraspinal muscle ROI curves did not change as a function of UAE. No change in noise from the MR system was seen over the course of the study.
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Reduction in volume.—The final prognostic model for percentage reduction in fibroleiomyoma volume is shown in Table 3. The model explained 25% of the variance in fibroleiomyoma reduction and included three variables.
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A negative predictor of success in this model was increasing age (P = .03). For every decade increase in patient age, the volume reduction decreased by 13%. Increasing pretreatment uterine volume also was associated with a negative prognosis (P = .02). With every 100-cm3 increment in initial uterine volume, volume reduction after UAE decreased by 20%.
A small number (n = 7) of fibroleiomyomata manifested with high signal intensity before UAE. The mean reduction in volume in these lesions was 22.4%, as compared with the 41.9% mean reduction in the remainder of the fibroleiomyomata. This difference was significant (P < .001)
Reduction in vascularity.—The final prognostic model for percentage change in vascularity is displayed in Table 4. This model explained 13% of the variance in vascularity changes with the use of two variables.
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Follow-up Imaging Features
At 1-year follow-up in five patients, 19 of 20 index fibroleiomyomata were seen, although one was too small to characterize. Table 5 shows the percentage reduction in pre-UAE uterine volume at 3 months and at the 1-year follow-up. For all five patients, uterine reduction continued or remained stable after the 3-month assessment. The reduction in fibroleiomyoma volume was also continued past the 3-month assessment. The mean percentage reduction in fibroleiomyoma volume at 3 months was 40.42% ± 35.18%, and that at 1 year was 64.06% ± 30.30%. Of the 20 fibroleiomyomata, 16 showed a greater volume reduction at 1 year than at 3 months.
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Correlation between MR Imaging and Clinical Results
No significant correlation between improvement in symptoms and imaging findings was identified. Most (26 of 31) women reported improvement in symptoms as compared with symptoms at presentation. Five patients reported a lack of improvement in either bleeding or pain symptoms. Of these, four had presented with both symptoms. One patient reported worsened bleeding and no change in pain. This patient had a large uterus and multiple fibroleiomyomata. Spasm during UAE was reported, and subsequent hysterectomy revealed more than 20 fibroleiomyomata. Three of the five patients reported improvement in one symptom but no change in the other. Of these, two patients had concomitant adenomyosis.
One patient had symptoms related to bleeding alone that did not improve with UAE. This patient had a large cervical fibroleiomyoma (745 cm3 before UAE, 634 cm3 after UAE) that distorted the lower uterus. The lesion did not change in vascularity according to ROI data (fibroleiomyoma-to-myometrial ROI ratio = 0.8 before and after UAE). At hysterectomy, multiple parasitized pelvic branches were identified feeding the fibroleiomyoma.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Our results also showed that the reduction in fibroleiomyoma volume was less in older patients than in younger patients. This may be a function of decreasing levels of female hormones in older patients. The results of kinetics studies have firmly established that estrogen causes vasodilatation and increased blood flow in the uterine vasculature. It is known that fibroleiomyoma pathogenesis is estrogen dependent. In a study by Cirkel et al (15), immunohistochemical estrogen and progesterone-receptor analysis of a gonadotropin-releasing hormone analogue revealed that there is a substantial correlation between myoma shrinkage and estrogen-receptor content. This suggests that the extent of fibroleiomyoma diminution may be related to an increasing number of estrogen-receptor–positive cells within the investigated tissue. As patient age increases, the baseline reduction in estrogen levels may, at a histologic level, produce vascular effects similar to those of embolization. However, the fibroleiomyomata in older patients in our study were not significantly smaller than those in the younger patients. This result may be clarified in a study with a larger number of patients.
Many patients with fibroleiomyomata have symptoms of abnormal bleeding and anemia. These symptoms may be related to the degree of vascularity of these lesions. When we used diminished vascularity as the criterion for success, we found that a hypervascular fibroleiomyoma was a strong predictor of success. This result is consistent with embolization theory; namely, embolic particles are delivered to regions of greater blood supply, where the particles produce the greatest effect. The regions of hypervascularity, in principle, should have lower impedance to blood flow and thus act as a sink for UAE particles.
In our study, there was a significant reduction in mean uterine and fibroleiomyoma volumes. The degree of uterine volume reduction improvement was comparable to the 35%–55% range reported in other studies (5–7,10), while the range of fibroleiomyoma volume reduction is approximately 45%–65% (4,5, 10,11). However, most other investigators have relied on physical examination or ultrasonographic (US) findings for quantitative assessment, and these may not be as accurate as MR imaging findings. Bradley et al (6) used MR imaging to measure uterine volume changes after UAE and reported a 49.5% volume reduction in seven patients. Burn et al (11) reported a mean decrease of 43% in mean fibroleiomyoma volume in 14 patients. The further reduction in the volume both of the uterus and of fibroleiomyomata at 1 year is an encouraging result that is suggestive of the durability of UAE, particularly as compared with the results of current medical treatments. Stable reductions in fibroleiomyoma volume were reported by Ravina et al (4) in 12 patients who were followed up for 12 months.
The majority of fibroleiomyomata showed a similar change in signal intensity after UAE; namely, increased signal intensity on T1-weighted MR images and homogeneous decreased signal intensity on T2-weighted images. These signal intensity changes are typical of blood products and are suggestive of hemorrhagic infarction. Furthermore, fibroleiomyomata with high signal intensity on T1-weighted images prior to UAE had a significantly lower reduction in volume and vascularity (Fig 3). Burn et al (11) reported similar results and hypothesized that fibroleiomyomata with high signal intensity on pre-UAE T1-weighted images have already undergone hemorrhagic degeneration and loss of vascular supply and, as such, do not change markedly after embolization.
The reduction in vascularity of fibroleiomyomata after UAE was not unexpected: The end point of the procedure is sluggish or no flow in the uterine arteries, which are the vessels that typically supply large feeding branches to fibroleiomyomata. The results of a Doppler US study (16) supports the concept of devascularization of fibroleiomyomata as the cause of improvement in patients treated with gonadotropin-releasing hormone analogues. Specifically, reductions in the volumes of the uterus and fibroleiomyoma in these patients are associated with an increase in vascular impedance to flow (16). Likewise, in our study, there was a significant reduction in fibroleiomyoma vascularity (qualitative and quantitative) after UAE (Fig 4). Often, the treated fibroleiomyoma had the appearance of a "bag of blood-products," that is, high signal intensity on T1-weighted images, homogeneous low signal intensity on T2-weighted images, and no detectable enhancement after injection of gadopentetate dimeglumine (Figs 2, 3).
The effect of UAE on myometrial vascularity is a relevant clinical issue. Because nonlysable material was used for embolization, it is possible that the overall flow to the myometrium may have been compromised. Our results with quantitative assessment of gross vascularity based on ROI curves of the myometrium showed no significant change in the vascular enhancement pattern after UAE (Fig 4). This may be related to the particle size. Aziz et al (8) showed that 150–250-µm-diameter polyvinyl alcohol particles used for UAE 1 day prior to hysterectomy lodge in arteries with a diameter of 1–2 mm but never in arterioles. We used even larger particles, and these presumably also lodged in arteries, particularly in the vascular siphon created by a hypervascular fibroleiomyoma. Thus, the arterioles that supply the layers of the myometrium should be spared from the direct effects of polyvinyl alcohol particles. Results of a recent study (12) in which the MR imaging changes in myometrial perfusion were assessed in two patients after UAE support our finding: Specifically, an immediate reduction in perfusion to the myometrium occurs within 5 hours after UAE, but perfusion recovers to near normal levels 1 month later, while leiomyoma perfusion remains low.
UAE is emerging as a viable alternative to traditional forms of treatment for fibroleiomyomas. MR imaging of the uterus in these patients enabled a precise quantitative assessment of the response to therapy. We showed the utility of MR imaging for the assessment of UAE-related alterations in the vascularity of the uterus and myometrium. UAE is most successful in the treatment for submucosal and hypervascular fibroleiomyomata and is less successful in treating older patients and those with a large uterus. These features may be helpful for selection of appropriate candidates for UAE and for determination of a prognosis. If UAE is to become the standard treatment, continued research is needed to evaluate the long-term effects on uterine and lesion volume, as well as to assess revascularization of fibroleiomyomata.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, R.C.J.; study concepts and design, R.C.J., S.M.A.; definition of intellectual content, S.M.A., R.C.J.; literature research, I.I., R.C.J.; clinical studies, R.C.J., S.M.A.; data acquisition, I.I., J.B.S.; data analysis, R.C.J., S.M.A., I.I.; manuscript preparation and review, R.C.J.; manuscript editing, S.M.A., I.I., J.B.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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), myometrium (
), paraspinal muscle (
), and background (
). (a) Before UAE, the ROI curve for fibroleiomyomata parallels that for the myometrium. The ROI curve for the paraspinal muscle shows mild enhancement. There was no change in background signal intensity. (b) After UAE, the ROI curve for fibroleiomyomata shows a significant change (P < .001) and is now flat. The curve for the myometrium indicates that perfusion is maintained.
