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Original Research |
1 Department of Radiology, Georgetown University Medical Center, 3800 Reservoir
Rd., NW, Washington, DC 20007-2113.
2 Department of Radiology, Massachusetts General Hospital, Boston, MA.
3 Present address: Department of Radiology, Kennedy Memorial Hospital, Cherry
Hill, NJ.
4 Department of Vascular and Body Imaging, Hôpital Lariboisiere, Paris,
France.
Received August 9, 2005;
accepted after revision January 15, 2007.
Address correspondence to J. B. Spies.
Abstract
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MATERIALS AND METHODS. One hundred forty-five consecutive patients who underwent UAE were retrospectively evaluated for blood supply to the uterus via the ovarian arteries after UAE. After completion of UAE, uterine supply from the ovarian arteries was assessed by performing abdominal aortography in all patients. Selective ovarian arteriography, in addition, was performed in some patients. The criteria used to characterize ovarian artery perfusion as seen on the aortograms were vessel size compared with a 5-French catheter and visualization and extent of flow. When the ovarian arteries visibly supplied uterine tissue, a quantification system was applied as follows: the uterus was divided in 24 segments on the basis of a clock model that was superimposed over the uterine territory in the anteroposterior projection. Depending on its distance from the midpoint of the clock, perfusion segments were labeled as central, middle, distal, or peripheral for each hour of the clock resulting in a total of 24 (12 x 2) potential segments of residually perfused uterine tissue via the ovarian arteries.
RESULTS. Two hundred ninety ovarian arteries were evaluated on aortography; of these, 202 (70%) were not seen during aortography. Of the visualized ovarian arteries (n = 88), 52% (46/88) were smaller than, 25% (22/88) were equal to, and 23% (20/88) were larger than the diameter of a 5-French catheter. The aortogram revealed that 61% (54/88) of the ovarian arteries extended into the pelvis, whereas 38% (33/88 [one missing data point]) did not. Selective injections were performed in 54 ovarian arteries. Of these, 69% (37/54) of the ovarian arteries had residual fibroid perfusion from the ovarian arteries after UAE (10 left-sided, 15 right-sided, six bilateral = 37 ovarian arteries). Residual fibroid perfusion was more likely in large ovarian arteries, particularly those with rapid flow visualized extending into the pelvis. The perfusion scores ranged from one to 18 segments (< 6 segments, n= 21 ovarian arteries; 6–12 segments, n= 12; > 12 segments, n= 4). Direct communication with the uterine arteries was seen in 20 ovarian arteries, 40% (8/20) of which did not show any uterine or fibroid perfusion, suggesting that fibroid flow had been occluded by UAE.
CONCLUSION. Based on aortography, the presence of residual fibroid perfusion is more likely if the ovarian arteries are large, have rapid flow, or have flow that extends into the pelvis. Selective ovarian artery evaluation may be indicated in these cases to determine the extent of residual fibroid perfusion.
Keywords: hemodynamics • leiomyoma • oncologic imaging • pelvic imaging • uterine artery embolization • women's imaging
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We have collected evidence that incomplete fibroid infarction by UAE will result in fibroid regrowth and clinical manifestation of treatment failure with recurrence of symptoms [4]. In prior studies, investigators have described and classified the types of ovarian artery–to–uterine artery anastomoses and assessed the utility of abdominal aortography in showing ovarian artery collaterals in patients undergoing UAE [5, 6]. However, the frequency and extent of collateral uterine blood flow from the ovarian arteries after UAE have not yet been examined, to our knowledge.
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UAE was performed using a standard technique. In brief, both common femoral arteries were accessed in all but one patient. In that patient, bilateral embolization was completed from a single femoral puncture. Both uterine arteries were then selectively catheterized using a crossover technique with a 5-French Cobra catheter (Imager, Boston Scientific). A microcatheter (Renegade, Target Therapeutics/Boston Scientific) was used when vasospasm was encountered. Embolization of the uterine arteries was performed with polyvinyl alcohol (PVA) particles (Ivalon, Cook; Trufill, Cordis; or Contour, Target Therapeutics/Boston Scientific) or trisacryl microspheres (Embospheres Microspheres, Biosphere Medical).
The embolization end point when using PVA particles was near stasis of flow with slight antegrade flow in the main uterine trunk still being present, and the embolization end point when using trisacryl microspheres was defined by a truncated appearance with occlusion of the smaller branches but patency of the main uterine trunk. Arteriograms of the right and left uterine arteries were obtained simultaneously by hand injections both before and after UAE.
We obtained aortograms in all 145 patients enrolled in this study. Aortography was performed using a pigtail catheter (Expo, Cook) with its tip positioned just above the origin of the renal arteries. Contrast material was injected at a rate of 15 mL/s for a total volume of 30 mL. The aortograms were reviewed, and the ovarian arteries were characterized and classified using vessel size, flow visualization, and flow extent as parameters. The entire angiographic study and all angiographic data sets were reviewed. All aortograms obtained for evaluation of ovarian artery supply to the fibroids were obtained after UAE only. We believe that aortography is more sensitive for the detection of fibroid supply from the ovarian arteries after UAE because of the hemodynamic changes that occur during UAE. It may, in addition, be more specific for the evaluation of the significance of ovarian artery supply than aortography before UAE.
The presence of any of the following criteria during aortography prompted ovarian artery catheterization and injection, which occurred in 54 of the 88 (61%) visualized ovarian arteries: ovarian artery size exceeding the diameter of a 5-French catheter, rapid ovarian artery flow similar to the flow in the abdominal aorta, and ovarian artery collateral extension into the lower pelvis.
For the selective ovarian arteriograms, the following criteria were established to evaluate collateral ovarian artery perfusion to the uterus: the existence or absence of a communication between the ovarian arteries and the ipsilateral uterine artery; the size of the ovarian arteries compared with a 5-French catheter; and the type, area, and location of uterine and fibroid tissue perfused by the ovarian artery. The size of the ovarian arteries was categorized as follows: not visible or smaller than, equal to, or greater than the diameter of a 5-French catheter. Ovarian artery flow was categorized as not visualized; late, if appearing delayed with respect to abdominal aortic flow; or early, if appearing similar to abdominal aortic flow and extension of flow. Extension of flow was categorized as not visualized, reaching into the abdomen, or extending into the pelvis (Fig. 1A, 1B).
A semiquantitative scoring system was used to estimate the extent and location of the tissue supplied by the ovarian arteries after completion of UAE. For this purpose, a clock model was superimposed over the uterine territory of an angiographic image in the anteroposterior projection. The segments were labeled as central or peripheral for each hour of the clock, resulting in 24 (2 x 12) potential segments of residual ovarian artery collateral perfusion (Fig. 2). The total score for each ovarian artery was then generated by adding the number of segments that contained perfusion derived from the collateral ovarian artery supply.
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The data were collected in an Excel database (Microsoft). Because of the small numbers of women in each of the ovarian artery characteristic categories, specialized software for small sample sizes was used to analyze the data (Cytel, Cytel Software Corp.), and exact p values are reported rather than asymptotic p values. Ovarian artery size, ovarian artery flow visualization, and extension of ovarian flow were examined as potential predictors of fibroid supply in a univariate analysis using the Fisher Freeman Halton test and Fisher's exact test statistics, and the positive predictive value for each parameter based on the results of our study was determined. The same three parameters (size of ovarian arteries, visualization of ovarian artery flow, and extension of ovarian artery flow) were analyzed regarding their respective potential correlation with the number of uterine segments that were being supplied by the ovarian arteries using the Jonckheere-Terpstra and Kruskal-Wallis tests.
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Evaluation results for the three parameters—the size of the ovarian arteries compared with a 5-French catheter, visualization of the ovarian arteries during aortography, and the frequency of extension of ovarian artery flow into the pelvis—are all listed in Table 1. Univariate analysis showed that larger size of the ovarian arteries, visualization of flow, and flow extending into the pelvis were all independently significantly associated with the presence of fibroid supply from the ovarian arteries (p < 0.001, p < 0.001, and p < 0.001, respectively; Table 2).
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Selective hand injections were performed in 54 ovarian arteries. Of those, 69% (37/54) showed residual fibroid perfusion (31 patients: 10 left, 15 right, six bilateral). Perfusion scores for individual ovarian arteries ranged from one to 18 segments (n = 37 ovarian arteries). The number of segments supplied by the ovarian artery was categorized into one of four groups: none, small (< 6 segments), moderate (6–12 segments), or large (> 12 segments). In 17 selective ovarian artery injections, no fibroid perfusion was evident, and 21 ovarian artery injections showed a small number of perfused segments; 12, a moderate number; and four, a large number.
Again, increased size of ovarian arteries, high velocity of flow, and extension of flow into the pelvis were all significantly associated with the number of segments supplied by the ovarian arteries (p < 0.001).
In general, residual fibroid perfusion was more likely in large ovarian arteries, particularly those with rapid flow visualized extending into the pelvis (Table 3). Results were similar for both the left and right ovarian arteries. The size of the ovarian artery in relation to a 5-French catheter, the velocity of flow, and the extension of flow were all significantly associated with the presence of same-sided fibroid supply by the ovarian arteries after embolization (Table 4). Fifty-eight percent (14/24) of women (left ovarian artery) and 53% (16/30) of women (right ovarian artery) with visible ovarian artery flow into the pelvis had same-sided fibroid supply compared with 0% of women with flow extending only into the abdomen.
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Table 5 presents the positive predictive values of the left, right, or either ovarian artery for the presence of same-sided ovarian artery supply. The characteristic of having either a left or a right ovarian artery larger in caliber than a 5-French catheter had the best positive predictive value (80%). In this population, ovarian artery embolization was not routinely performed.
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Because there is no communication between the ovarian artery collaterals and the original uterine arteries on a macroscopic level in type II, arteries seen on a selective uterine artery angiogram should not be seen on a selective ovarian arteriogram and vice versa. In types I and III, communications between the ovarian artery and the ipsilateral uterine artery are visible and both arteries perfuse the same capillary tissue bed.
Regarding the significance of the various types of collateralization for UAE, we base our considerations on the following presumptions. If collateral flow to the fibroid uterus is present, it may cause treatment failure. If fibroid tissue is perfused by the uterine artery only, infarction after technically successful UAE should ensue. On the other hand, fibroids that are solely or partially perfused by collateral ovarian artery flow will not have complete or even partial infarction after UAE. If fibroid perfusion is provided via the branches of both the uterine and ovarian arteries, fibroid infarction may be incomplete and the initial extent of the infarcted area likely correlates with the size of the territory that derived its blood supply from the uterine artery. In that case, selective ovarian artery angiography after completed bilateral UAE will show uterine and fibroid tissue that still has perfusion. On the basis of these assumptions, we have elected to evaluate the remaining uterine perfusion from ovarian collaterals after bilateral UAE rather than before UAE. Ovarian supply may be obscured by uterine vessels overlapping if aortography is performed before embolization.
At this time, whether there is a threshold of remaining fibroid perfusion above which treatment will likely fail is not proven. However, in our recent analysis of long-term imaging outcomes after UAE, patients with incomplete fibroid infarction all showed fibroid regrowth and symptom recurrence in the long term [4]. Based on this finding, we can draw the following conclusions. Clinical failure after standard UAE is likely in patients with type II and is possible in patients with type I ovarian collateral fibroid supply, whereas those with type III may rather bear the risk of inadvertent ovarian embolization with resulting ovarian failure. Collateral ovarian supply to uterine fibroids detected during UAE should be considered clinically significant if the aortogram obtained after UAE shows ovarian arteries that are large, have rapid flow, or have flow that extends into the pelvis. In these scenarios, ovarian artery catheterization and injection may be performed.
Technically successful target embolization procedures of the identified distal ovarian artery that provides partial fibroid perfusion have been described and have sometimes been advocated in the literature previously [6, 9]. However, ovarian artery embolization should be used cautiously. The reports of ovarian artery embolization currently are limited. The procedure can be technically challenging, particularly if distal passage of the catheter is attempted. On the other hand, a proximal catheter position can result in complications. Pelage et al. [8] reported a case of particle reflux during ovarian artery embolization that led to subsequent foot ischemia. Binkert et al. [6] described three cases of women with large ovarian arteries providing collateral fibroid supply after UAE. Ovarian artery catheterization was technically completely unsuccessful in one patient and was partially unsuccessful in a second patient; in the second patient, embolization had to be performed from a catheter position proximal to the ovary with a slurry of gelatin sponge particles (Gelfoam, Upjohn) and the patient developed amenorrhea after the procedure. The third ovarian arteries embolization procedure had technical and clinical success [6]. Barth and Spies [4] have described technically successful embolization using PVA particles or trisacryl gelatin microspheres in a total of nine ovarian arteries in six patients and reported "substantial clinical improvement" in five of these patients on follow-up. Although menstruation resumed in all patients in that small series on follow-up, the authors suggest caution given the limited data available about ovary function after ovarian artery embolization.
Our current approach is to assess the extent of ovarian artery supply to fibroid tissue. When there is extensive residual flow to fibroids, we usually proceed with ovarian artery embolization, at least unilaterally. In the case of extensive bilateral flow, we usually wait to determine the outcome from UAE alone before suggesting embolization of the ovarian arteries unless we have the patient's prior consent to proceed in that circumstance.
In performing this study, we intended to establish parameters that suggest significant uterine perfusion by ovarian artery collaterals and that increase the likelihood of collateral fibroid perfusion. We have shown that an ovarian artery exceeding 5-French in diameter, rapid flow, and visible extension of flow into the pelvis are useful parameters to suspect substantial collateral flow. If these characteristics are identified on the flush aortogram, selective ovarian arteriography is indicated to further delineate the collateral supply.
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