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DOI: 10.1148/radiol.2441060796
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(Radiology 2007;244:291-298.)
© RSNA, 2007

Vascular and Interventional Radiology

Uterine Fibroid Embolization: The Utility of Aortography in Detecting Ovarian Artery Collateral Supply1

Amy M. White, MD, Filip Banovac, MD, Shadi Yousefi, MD, Rebecca S. Slack, MS, and James B. Spies, MD

1 From the Department of Radiology, Georgetown University Hospital, 3800 Reservoir Rd NW, CG 201, Washington, DC 20007-2113 (A.M.W., F.B., S.Y., J.B.S.); and Department of Biostatistics, Bioinformatics, and Biomathematics, Georgetown University, Washington, DC (R.S.S.). Received May 6, 2006; revision requested July 7; revision received August 7; accepted September 7; final version accepted November 15. A.M.W. supported by a Radiological Society of North America Research & Education Foundation Medical Student Departmental Program Grant. Address correspondence to J.B.S. (e-mail: spiesj{at}gunet.georgetown.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Purpose: To retrospectively determine the sensitivity of ovarian artery (OA) visualization at aortography performed after uterine fibroid embolization (UFE) and, using OA arteriography as the reference standard, compare the extent of arterial flow to the uterus at aortography with selective ovarian arteriography, to establish the utility of aortography and ovarian arteriography in the routine practice of UFE.

Materials and Methods: This study received institutional review board approval with waiver of informed consent and was HIPAA compliant. Retrospective review of 1129 consecutive UFE patients (1072 with aortograms, 57 excluded; mean age, 44 years; range, 21–60 years) was performed to identify all visible OAs. Visible OAs were independently graded by two interventional radiologists according to extent of pelvic arterial flow. If selective arteriography was performed, a second grade was assigned based on assessment of the selective study. Descriptive and summary statistics were used for assessment by the senior observer, and interobserver variability was determined.

Results: Of 1072 UFE patients, 184 (17.2%) had at least one visible OA. Ten (0.8%) patients were identified at aortography with collateral OA supply to more than 10% of the uterus. In total, 251 OAs were visualized, and 157 of these were further evaluated with selective study. Sixty-two (5.8%) patients were identified at selective arteriography as having collateral OA supply. The sensitivity of aortography was approximately 18%. Interobserver concordance was high ({kappa} values of 0.81 and 0.90 for aortography and selective study, respectively), but not perfect.

Conclusion: Aortography rarely helps identify patients with substantial residual OA supply to the uterus and is a poor predictor of the extent of that supply, and thus may be of limited utility in routine UFE.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Uterine fibroid embolization (UFE) is now recognized as one of the primary therapies available to women for the treatment of symptomatic uterine fibroids. Menorrhagia, pelvic pain, and pelvic pressure are the most common symptoms associated with fibroids. While technical success rates are generally reported in the range of 97%–100%, clinical success rates as low as 80% have been described in long-term studies (1,2). Although considerable research into the outcome of UFE has provided valuable data on symptom and imaging results (3–8), the factors that contribute to potential failure have not yet been fully defined.

Ovarian artery (OA) blood flow, supplementing or replacing uterine artery (UA) supply to the uterus, has long been identified as a potential cause of UFE failure. Several early case reports identified the role of ovarian collateral supply as a potential issue in UFE (9,10). The use of supplemental OA embolization (OAE) has also been reported with clinical success, further supporting the importance of collateral arterial supply in cases of UFE failure (11,12). However, there are few available data on the frequency and extent of OA supply to the uterus at the conclusion of UFE. Thus, the purpose of our study was to retrospectively determine the sensitivity of OA visualization at aortography performed after UFE, and, using ovarian arteriography as the reference standard, to compare the extent of arterial flow to the uterus at aortography and selective ovarian arteriography. This allows us to establish the utility of aortography and ovarian arteriography in the routine practice of UFE.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Our retrospective study was approved by the institutional review board and was compliant with the Health Insurance Portability and Accountability Act. Patient informed consent was waived.

Patients
Between December 2000 and June 2005, 1129 consecutive women who underwent UFE for the treatment of symptomatic uterine fibroids at a large metropolitan academic teaching hospital (Georgetown University) were identified. Patient presentation was typical of fibroid-related symptoms and most commonly included prolonged or excessive menstrual bleeding, dysmenorrhea, pelvic pain, pelvic pressure, or urinary symptoms. The diagnosis of uterine fibroids was confirmed in all patients prior to UFE with magnetic resonance (MR) imaging. Postembolization aortography became part of our routine procedure after the first 100 patients, to exclude additional collateral arterial supply to the fibroids that would become apparent after UFE.

Fifty-seven patients undergoing repeat embolization or in whom aortography after embolization was not performed were excluded; two had renal insufficiency, in whom contrast agent use was minimized, and 55 underwent UFE prior to our instituting aortography as part of routine UFE, leaving a final cohort of 1072 women (mean age, 44 years; range, 21.8–60.9 years).

Embolization Procedure
Informed consent was obtained from each patient after all risks associated with the procedure were explained. Each patient underwent embolization performed by one of two experienced operators (J.B.S., 15 years of angiographic experience; additional operator, 11 years of angiographic experience). Bilateral femoral access was obtained and selective hypogastric catheterization was completed with use of a 5-F hydrophilic catheter (Cobra 2 Glidecath; Terumo/Boston Scientific, Natick, Mass). A 3-F microcatheter (Renegade Hi-Flow, Target Therapeutics/Boston Scientific; or Embocath, Biosphere Medical, Rockland, Md) was used in 24 of 50 procedures prior to our instituting microcatheter use in all UFE procedures. Uterine arteriography was performed in all patients. Bilateral UA embolization was performed in all but 14 patients. In these patients, unilateral embolization was performed owing to the absence of a second UA or inability to catheterize one UA. Embolization was performed by using either 355–500-µm polyvinyl alcohol particles (Contour; Boston Scientific) or 500–700- and/or 700–900-µm tris-acryl gelatin microspheres (Embospheres; Biosphere Medical), as determined by the performing interventional radiologist. The rate of embolization was always controlled to avoid reflux into the OAs with the endpoint defined by the angiographic appearance of a patent main UA with proximal or distal occlusion of its main branches as determined by the type of embolic material being used as in a previously published report (13). The embolization technique was not altered regardless of identified OA communication at initial arteriography. Subsequent OAE was selectively performed based on the extent of OA supply, consent status, and the desire for future fertility.

Postembolization Arteriography
To minimize radiation dose to the patient, a filming rate of 1 frame every second was used for postembolization abdominal aortography to image from the pubic symphysis extending superiorly, collimated from side to side to include the common femoral arteries. Nonionic contrast medium (various manufacturers) was injected at a rate of 20 mL/sec for 2 seconds. Criteria for evaluation of OAs visualized at aortography by using selective arteriography included a visualized OA down to the level of the ovaries and/or rapid OA flow comparable to flow in other vessels visualized on the aortogram. In some patients with ovarian arteriography indicated for one side, the contralateral OA was catheterized inadvertently while searching for the target OA, secondary to the proximity of the OA origins to one another. At contrast material injection, the catheterized contralateral artery was recognized to have increased flow toward the ovary, indicating the need for further arteriographic evaluation in nine patients to exclude supplemental blood supply to the uterus. Selective ovarian arteriography was performed by using hand injection of contrast medium, with imaging to include the entire length of the OA. Of 1072 patients, 123 underwent selective ovarian arteriography (Fig 1).


Figure 1
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  		Figure 1: Flow diagram describes number of patients satisfying inclusion or exclusion criteria for postembolization aortography and subsequent selective ovarian arteriography.

 
Image Evaluation
Postembolization aortograms were each initially reviewed by one observer (J.B.S.) for the presence of a visible OA. Angiographic studies for the first 639 patients included in this study were stored at the hospital and were available for review. The remaining 433 studies were filed at a document storage facility. Our protocol for these studies was to report OA visualization and the extent of flow. Patient angiographic images were retrieved from the storage facility for review if OA visualization was documented in the procedure note or if no comment was reported on the visualization, or lack of visualization of the OAs. One hundred eight patients met these criteria. Fourteen patients with documented OA visualization were identified with angiographic studies that could not be retrieved. Therefore, we evaluated all 1072 aortograms by means of image review and/or review of the procedure report, with 747 evaluated directly and 325 reviewed by using the procedure report. Of those 325 patients, 311 were identified as having a noted absence of visible OAs, and 14 had visible OAs, but we were unable to retrieve those 14 aortograms for assessment of the visible OAs.

OAs visualized at aortography were independently graded by two interventional radiologists with experience performing UFE (J.B.S., >1500 procedures; F.B., approximately 50 procedures).

The grading system has already been published (13). Grades were assigned according to the extent of arterial flow into the pelvis by using the following scale: grade 0, OA not visualized; grade 0+, OA visible, normal in size, with flow extending no further than the ovary; grade 1, arterial flow visible to the edge of the uterus but does not appear to provide any uterine flow; grade 2, minor crescentic arterial supply to the margin of the uterus supplying less than 10% of the ipsilateral half of the uterus; grade 3, moderate supply to the uterus, providing flow to 10%–50% of the ipsilateral half of the uterus; grade 4, flow to more than 50% of the ipsilateral half of the uterus; grade 5, replacement of the UA by the OA (Figs 2 and 3). If selective ovarian arteriography was performed, then a second grade was independently assigned by each of the radiologists on the basis of the extent of arterial flow, with this grade based on the selective ovarian studies. Thus, two data sets were obtained from each radiologist: a grade for each OA as assessed at aortography; and a grade for each OA as assessed at selective ovarian arteriography when selective studies were available.


Figure 2A
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  		Figure 2a: Anteroposterior fluoroscopic angiographic images obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show bilateral OA (arrows). Both right and left OA assessed as grade 0+. (c) Selective right ovarian arteriogram shows minor crescentic flow (arrows) to less than 10% of the ipsilateral half of the uterus and was assessed as grade 2. (d) Selective left ovarian arteriogram shows flow (arrow) to level of the uterus and was assessed as grade 1 (arrow).

 

Figure 2B
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  		Figure 2b: Anteroposterior fluoroscopic angiographic images obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show bilateral OA (arrows). Both right and left OA assessed as grade 0+. (c) Selective right ovarian arteriogram shows minor crescentic flow (arrows) to less than 10% of the ipsilateral half of the uterus and was assessed as grade 2. (d) Selective left ovarian arteriogram shows flow (arrow) to level of the uterus and was assessed as grade 1 (arrow).

 

Figure 2C
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  		Figure 2c: Anteroposterior fluoroscopic angiographic images obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show bilateral OA (arrows). Both right and left OA assessed as grade 0+. (c) Selective right ovarian arteriogram shows minor crescentic flow (arrows) to less than 10% of the ipsilateral half of the uterus and was assessed as grade 2. (d) Selective left ovarian arteriogram shows flow (arrow) to level of the uterus and was assessed as grade 1 (arrow).

 

Figure 2D
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  		Figure 2d: Anteroposterior fluoroscopic angiographic images obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show bilateral OA (arrows). Both right and left OA assessed as grade 0+. (c) Selective right ovarian arteriogram shows minor crescentic flow (arrows) to less than 10% of the ipsilateral half of the uterus and was assessed as grade 2. (d) Selective left ovarian arteriogram shows flow (arrow) to level of the uterus and was assessed as grade 1 (arrow).

 

Figure 3A
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  		Figure 3a: Anteroposterior fluoroscopic angiographic imaged obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show right OA (arrows). Flow observed to margin of uterus was assessed as grade 1. (c) Selective right ovarian arteriogram shows OA branches (arrowheads) supplying ipsilateral half of the uterus. No UA was identified during angiography, defining grade 5 OA.

 

Figure 3B
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  		Figure 3b: Anteroposterior fluoroscopic angiographic imaged obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show right OA (arrows). Flow observed to margin of uterus was assessed as grade 1. (c) Selective right ovarian arteriogram shows OA branches (arrowheads) supplying ipsilateral half of the uterus. No UA was identified during angiography, defining grade 5 OA.

 

Figure 3C
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  		Figure 3c: Anteroposterior fluoroscopic angiographic imaged obtained after bilateral UA embolization. (a) Early and (b) late arterial phase abdominal aortograms show right OA (arrows). Flow observed to margin of uterus was assessed as grade 1. (c) Selective right ovarian arteriogram shows OA branches (arrowheads) supplying ipsilateral half of the uterus. No UA was identified during angiography, defining grade 5 OA.

 
Data Analysis
The frequency of OA visualization and distribution of OA grades was determined by using OA grades and patients' higher artery grades based on assessment by the senior observer (J.B.S.). Cross tabulations were created for aortography versus selective ovarian arteriography. Selective ovarian arteriography was considered the reference standard in determining the distribution of OA grades when calculating the sensitivity of aortography in identifying OA grades 3, 4, and 5. Sensitivity, specificity, and positive and negative predictive values for aortography were reported with Blythe-Still-Casella binomial 95% confidence intervals as calculated by using StatXact (StatXact4 for Windows; Cytel Software, Cambridge, Mass) (14,15).

A Cohen's weighted {kappa} statistic was calculated to describe the concordance of OA grade assessment at both aortography and selective ovarian arteriography between observers (J.B.S. and F.B.) with 95% confidence intervals, as calculated with StatXact.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
OA Visualization
Of 1072 consecutive women who underwent UFE with postembolization aortography, 184 (17.2%) patients (mean age, 45 years; range, 25.3–58.4 years) had at least one visible OA at postembolization aortography, and 67 (6%) patients had bilateral OA visualization. In total, 251 OAs were visualized with slightly more right (n = 143) than left (n = 108) arteries identified. The majority of OAs that were visible (Table 1) were graded as 0+ or 1, with 197 (78%) of all visible OAs in this category, indicating no supply to the uterus itself. Only 14 arteries, found in 10 (0.87%) patients, were graded as 3, 4, or 5, indicating supply to more than 10% of the ipsilateral half of the uterus at aortography.


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  		Table 1. Summary of Aortography Findings for 1072 Patients*

 
Of the 251 visualized OAs, 157 were further evaluated with selective ovarian arteriography, with an additional nine OAs further evaluated after contralateral catheterization and visualization of increased flow as described above. The 94 arteries that were visualized but not further studied were predominately (96.0%) grade 0+ or 1. The distribution of OA grades changes (Table 2) based on assessment of selective ovarian arteriographic findings, with more OAs being identified as providing supply to the uterus itself and only one OA downgraded. For example, of the 40 OAs assessed as grade 2 at aortography, three were not evaluated with selective ovarian arteriography, 12 were assessed similarly as grade 2 on selective study, 14 were upgraded to grade 3 on selective study, three were upgraded to grade 4, and eight were upgraded to grade 5. Thus, of 40 grade 2 arteries, 37 (93%) were evaluated and 25 (63%) were upgraded.


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  		Table 2. Grade Distribution of 157 OAs Visualized at Aortography and Assessed with Selective Ovarian Arteriography*

 
Selective ovarian arteriography helped identify 67 arteries, found in 62 (5.8%) patients identified as grade 3, 4, or 5, compared with the 14 arteries identified at aortography as having this degree of arterial flow. It should be noted that one of these arteries was not visualized at aortography but was upgraded to grade 3 after contralateral catheterization demonstrated increased arterial flow, as described above. With selective ovarian arteriography as the reference standard for identifying patients with a grade 3, 4, or 5 OA, the sensitivity of aortography as a screen for these patients was 18% (12 of 67; 95% confidence interval, 10%, 28%), and the specificity was 99% (98 of 99; 95% confidence interval, 95%, 99.95%). In this population who underwent selective ovarian arteriography, the positive predictive value of identifying collateral OA supply at aortography was 92% (12 of 13; 95% confidence interval, 67%, 99.6%) and the negative predictive value was 64% (98 of 153; 95% confidence interval, 56%, 71%).

Interobserver Variability
The weighted {kappa} statistic describing the concordance of OA assessment suggests that although there is substantial and highly significant concordance (0.81 and 0.90 for aortography and selective ovarian arteriography, respectively), it is not perfect (Table 3). The frequencies of concordance between the two observers at aortography and selective ovarian arteriography indicate a very strong concordance (Table 4, Table 5).


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  		Table 3. Concordance between Observers for Aortography and Selective Ovarian Arteriography Findings

 

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  		Table 4. Frequencies for Concordance of OA Assessment of Aortography Findings between Observers

 

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  		Table 5. Frequencies for Concordance of OA Assessment of Selective Ovarian Arteriography Findings between Observers

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
The role of residual OA supply to the uterus is a well-known cause of potential failure of UFE (9–12,16–18). Several reports have indicated that uterine perfusion from ovarian collateral circulation may occur in 5%–10% of women (18–20). Supplemental OAE has been described in several reports with successful clinical outcomes (11,12). The largest of these reports, by Barth and Spies (11), documented clinical and imaging outcomes in six patients with substantial uterine perfusion from OA circulation. Five of those six patients reported substantial symptom improvement, and one patient underwent subsequent hysterectomy due to persistent symptoms. Follow-up MR images for successfully treated patients demonstrated complete fibroid infarction, indicating potential benefit of supplemental OAE in some patients with substantial uterine perfusion from OA circulation. Therefore, there is value in knowing when residual uterine blood supply from the OAs is present.

The extent of OA supply to the uterus can be assessed with flush pelvic aortography either before or after UFE. Visualization of an OA often indicates an enlarged vessel since the normal OA generally has a diameter less than 1 mm, frequently making angiographic detection difficult (17). Among all primary UFE patients, our study identified fewer than 20% with a visible OA at aortography, consistent with previous reports (17). OAs are most likely clinically important when they provide arterial flow to a substantial portion of the fibroid-uterus. We may be able to define this potentially substantial flow as an OA supplying more than 10% of the ipsilateral half of the uterus, defining a grade 3, 4, or 5. If we use this definition to identify women who would potentially benefit from supplemental OAE, postembolization aortography helps identify fewer than 1% of primary UFE patients as meeting these criteria, a very low yield. Our study indicates that selective ovarian arteriography helps identify fewer than 6% of primary UFE patients with potentially substantial supply. Using selective ovarian arteriography as the reference standard, these numbers suggest the sensitivity of postembolization aortography for accurate detection of substantial residual OA supply is only 18%.

We acknowledge limitations of our study. First, UA embolization may alter pelvic arterial flow patterns to an uncertain extent and thereby alter the appearance of OA circulation at aortography. Second, assessment with selective arteriography may reflect nonphysiologic over-injection, again potentially altering the appearance of arterial supply to the pelvis. Third, the grading system is subject to both anatomic variation of the uterus and subjective assessment by the observer, although our study showed strong but imperfect concordance between observers. Fourth, our calculated sensitivity, specificity, and positive and negative predictive values are based on a select subgroup of patients who underwent ovarian arteriography. However, to obtain reliable positive and negative predictive values, as well as false negatives for OAs not visualized at aortography for sensitivity and specificity estimates, all patients would need to undergo selective ovarian arteriography which is not clinically feasible.

Our study suggests that substantial collateral OA circulation to the uterus occurs in few patients, and that postembolization aortography is of limited value in identifying residual fibroid perfusion. This calls into question the value of aortography in routine UFE, given that there are risks of additional patient radiation exposure and contrast material administration when performing additional imaging. We believe that further investigations regarding the clinical or angiographic factors associated with the development of collateral OA supply (eg, previous pelvic surgery, a substantially enlarged uterus, or a disproportionately small UA) will help identify patients who will receive the most benefit from screening aortography.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE
 References
 


   IMPLICATIONS FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
References
 


   FOOTNOTES
 

Abbreviations: OA = ovarian artery • OAE = OA embolization • UA = uterine artery • UFE = uterine fibroid embolization

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, J.B.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, A.M.W., J.B.S.; clinical studies, F.B., J.B.S.; statistical analysis, R.S.S.; and manuscript editing, A.M.W., F.B., J.B.S.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 

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