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Vascular and Interventional Radiology |
1 From the Departments of Body and Vascular Imaging (J.P.P., J.N., R.R., O.L.D.), Obstetrics and Gynecology (D.J., A.F.), and Neuroradiology (J.N., A.L.), Hôpital Lariboisière, Paris, France. Received October 24, 2003; revision requested January 13, 2004; final revision received May 16; accepted May 24. Address correspondence to J.P.P., Department of Radiology, Hôpital Ambroise Paré, 9 avenue Charles-de-Gaulle, 92104 Boulogne Cedex, France (e-mail: jean-pierre.pelage@apr.ap-hop-paris.fr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The study protocol was approved by the institutional review board, and all participants gave written informed consent. Eighteen women (mean age, 44.3 years) with symptomatic adenomyosis were treated with bilateral embolization of the uterine arteries. The diagnosis of diffuse adenomyosis was based on heterogeneous abnormal myometrial echogenicity with myometrial cysts at ultrasonography (US) or on enlarged junctional zone and myometrial cysts at magnetic resonance (MR) imaging. Focal adenomyosis was diagnosed if there was a circumscribed nodular lesion mimicking intramural fibroid. All patients with associated uterine fibroids were excluded. Embolization was offered as an alternative to hysterectomy in all women. Clinical evaluation was made at regular intervals to assess patient outcome. Follow-up US or MR imaging was performed 6 months after embolization to assess uterine volume reduction.
RESULTS: Bilateral uterine artery embolization was achieved in all but one woman by using polyvinyl alcohol particles or trisacryl microspheres. All women resumed normal menstruation after the procedure. After 6 months, 15 (94%) of 16 women reported improvement in menorrhagia. Follow-up images at 6 months depicted a slight decrease (mean, 15%) in uterine volume in 17 (94%) of 18 women. After 1 year, 11 (73%) of 15 women had improvement in menorrhagia, and eight (53%) of 15, complete resolution. After 2 years, five (56%) of nine women had complete resolution of menorrhagia. Eight (44%) of 18 women required additional treatment during follow-up for failure or recurrence; five women (28%) underwent hysterectomy.
CONCLUSION: Even if short-term results of uterine artery embolization to treat adenomyosis appear encouraging, midterm results are disappointing, with only 55% of treated patients showing clinical improvement after 2 years.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In centers where uterine artery embolization for uterine fibroids has been performed without screening with magnetic resonance (MR) imaging, failure has been attributed to the presence of undiagnosed adenomyosis (4,6,8). Other centers, however, have reported encouraging short-term clinical results in women with adenomyosis (9–12).
The purpose of our study was to prospectively evaluate the midterm results of uterine artery embolization for symptomatic adenomyosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The mean age of the women was 44.3 years ± 4.8 (standard deviation), and the age range was 35–57 years. All women included in the study were premenopausal patients who had menorrhagia (n = 17, 94%) or pelvic pain or pressure (n = 11, 61%). Mean duration of menses before embolization was 9.2 days ± 3.8 (range, 3–15 days).
In all of the women, therapy with progestogen, hemostatic agents, or gonadotrophin-releasing hormone agonists had failed. Because of the failure of medical treatment, hysterectomy was planned in all of the women. Embolization was offered as the treatment of last resort to women who sought organ-sparing therapy.
Fourteen of the women had diffuse adenomyosis, and four had focal adenomyosis (adenomyoma). The mean uterine and adenomyoma volumes before embolization were 297 and 189 cm3, respectively.
Imaging before Embolization
All women included in this study underwent transabdominal and endovaginal ultrasonography (US) (n = 6) or MR imaging (n = 12) of the pelvis. The first six patients were evaluated by using US, and the next 12 were evaluated by using MR imaging after it became available at our institution. Imaging was performed by two senior radiologists with special training in women’s imaging (J.P.P. and O.L.D., each with 10 years of experience in pelvic imaging), who worked together in consensus to confirm the diagnosis of adenomyosis, determine the uterine volume, and exclude associated conditions (ie, uterine fibroids, hydrosalpinx) and malignancy (ie, endometrial or cervical cancer). US examinations started with transabdominal real-time gray-scale evaluation of the pelvis, which was followed by transvaginal examination of the uterus and adnexa by using a US scanner (Sequoia 512; Acuson, Mountain View, Calif) equipped with transabdominal (4C1; Acuson) and transvaginal (EC-10C5; Acuson) transducers. MR imaging was performed with a 1.5-T superconducting unit (Signa; GE Medical Systems, Milwaukee, Wis) and a standard phased-array torso coil. The protocol consisted of the following sequences: sagittal and transverse T2-weighted fast spin echo (3200/80 [repetition time msec/echo time msec], 90° flip angle) and transverse T1-weighted fat-saturated spoiled gradient echo (160/1.7, 65° flip angle) for pelvic imaging, and sagittal dynamic contrast material–enhanced T1-weighted spoiled gradient echo (160/1.7, 65° flip angle) for uterine imaging immediately after and at 30, 60, and 90 seconds after administration of 0.1 mmol/kg of gadoterate meglumine (Dotarem; Laboratoires Guerbet, Aulnay-sous-Bois, France). The following criteria were used for the diagnosis of adenomyosis on the basis of US images: heterogeneous myometrial echotexture, asymmetry of the anterior and posterior uterine walls, small myometrial cysts, and poor definition of the endomyometrial junction (13). The following criteria were used for diagnosis of adenomyosis on the basis of sagittal T2-weighted images: low myometrial signal intensity, diffuse (>12 mm) or focal thickening of the junctional zone, high-signal-intensity foci corresponding to myometrial cysts, poor definition of the endomyometrial junction, and poor definition of lesion borders (14–16). With both techniques, diffuse adenomyosis and focal adenomyosis (adenomyoma) were differentiated. Volume measurements were obtained for the whole uterus in cases of diffuse adenomyosis and/or for the adenomyoma before embolization. Volumes were calculated by using the formula for an ellipsoid (length x width x depth x .52).
Procedure
Digital subtraction angiography was performed with an angiographic unit (ADAC Laboratories, Milpitas, Calif) and with access via the right or left femoral artery in all patients. Patients were treated either during conscious sedation (obtained by using midazolam and fentanyl) or during spinal anesthesia, on the basis of a preprocedural evaluation of the patient by the anesthesiologist. For spinal anesthesia, a single injection of a mixture of bupivacaine and morphine was used that had an effect lasting 6–12 hours. In case of insufficient effect, a patient-controlled analgesia pump was immediately used. Contralateral internal iliac artery angiography and selective study of the anterior arterial branch was then performed by using a 4- or 5-F cobra-type catheter (Glidecath; Terumo, Tokyo, Japan) to determine the anatomy of the uterine artery. The ipsilateral internal iliac artery and uterine artery were also accessed with the same catheter by using a modified Waltman loop technique (17,18). One of two 3-F microcatheters (GT Leggiero, Terumo; Tracker 325, Boston Scientific, La Garenne–Colombes, France) was used in tortuous, small, or spastic uterine arteries to ensure free-flow embolization. Images obtained prior to embolization were carefully evaluated, with special attention given to the presence of utero-ovarian anastomosis (19). We chose the embolization material and angiographic end point on the basis of the technique used in our daily practice at the time of the procedure. Polyvinyl alcohol particles (Contour; Boston Scientific) with a diameter of 355–500 µm or trisacryl microspheres (EmboSphere; BioSphere Medical, Louvres, France) with a diameter of 500–900 µm were introduced with free flow during fluoroscopic guidance. The choice of particle diameter was made by the interventional radiologist during the procedure (J.P.P. and O.L.D., with 15 and 10 years of experience in uterine artery embolization, respectively). The embolization was stopped when stasis or near stasis was observed in the ascending segment of the uterine artery. Pledgets of gelatin sponge (Spongel, Yamanuchi, Tokyo, Japan; Curaspon, CAPS Recherche, Saint-Cloud, France) were optionally injected, depending on operator preference, as a secondary embolic agent in our first several patients to ensure arterial occlusion.
Management and Pain Evaluation after Embolization
In all patients, embolization was followed by a hospital stay of one or two nights. After embolization, the patient was admitted to the Department of Obstetrics and Gynecology for postprocedural care. The management of postprocedural pelvic pain consisted of administration of a narcotic via a patient-controlled analgesia pump. Intravenous anti-inflammatory drugs were also administered after embolization. Pelvic pain was evaluated 6–12 hours after the procedure by using a three-level scale (no, moderate, and intense pain). Patients were discharged 1–2 days after the procedure. After discharge, pain was controlled by using nonsteroidal anti-inflammatory and analgesic therapy.
Clinical Follow-up
Each woman was interviewed by telephone 1 week after the procedure to elicit reports of incidents such as pelvic pain, groin hematoma, abnormal bleeding, or infection (J.P.P., O.L.D.). Office visits were planned at 6 and 12 months after embolization with the interventional radiologist and the gynecologist (J.P.P., O.L.D., D.J., A.F.). A telephone interview or office visit also was completed every year thereafter. The women were asked to evaluate the changes in their symptoms after the procedure. Improvement in menorrhagia was scored by using the following six-point scale, which is routinely used at our institution: complete resolution of symptoms (+3), marked improvement (+2), slight improvement (+1), unchanged symptoms (0), slight worsening of symptoms (–1), or worsening of symptoms (–2). The reason is that, at the time of this study, no standardized questionnaire for fibroid-related symptoms was available in the literature. Duration of menses (in days) was also recorded before and after embolization. Pelvic pain and pressure were evaluated as still present or resolved after embolization.
Complications also were recorded prospectively, with special emphasis on menstrual irregularity, amenorrhea, and pelvic infection.
Imaging Follow-up
Follow-up US and/or MR imaging was performed at 6 months by the same radiologists who performed the initial examinations. Measurements for the calculation of volume were obtained for the whole uterus in cases of diffuse adenomyosis and/or for the adenomyoma. Volume was calculated by using the ellipsoid formula and was compared with volume prior to embolization.
Only one postprocedural imaging examination was planned, but some patients also underwent US at 12 months and 24 months after embolization to determine whether any additional reduction in uterine volume or any abnormality, including pelvic abscess or hydrosalpinx, was present.
Statistical Analysis
Summary descriptive statistics were used for demographic parameters and uterine and adenomyoma volumes before and after embolization. Nonparametric tests were used to compare volumes before and after embolization, because of the small pool of data. The Wilcoxon test was used to assess the statistical significance of uterine and adenomyoma shrinkage. Null hypotheses were rejected at a P level of less than .05. Statistical analysis was carried out by using software (StatView; SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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A total volume of 4.4 mL ± 1.9 (range, 2–8 mL) of the microsphere-containing embolization material was used per procedure. The amount of polyvinyl alcohol particle–containing embolization material used (two or three vials) varied among procedures. In three women, the secondary embolization agent (gelatin sponge pledgets) was used.
Postprocedural Pain
Sixteen (89%) women experienced severe postprocedural pain. Only two women experienced moderate pain after embolization. One woman had recurrent severe cramping pain 4 days after embolization, and she was subsequently evaluated with pelvic MR imaging (Fig 1). Myometrial ischemia was observed, but the patient experienced a full resolution of pain with the aid of oral analgesia.
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The first postprocedural evaluation was performed 5.3 months ± 1.1 after embolization in 17 women. The remaining woman, who had a continuation of symptoms of menorrhagia and pelvic pressure, underwent hysterectomy 3.9 months after embolization, because of treatment failure. Fifteen (94%) of 16 women with abnormal bleeding experienced improvement in menorrhagia, and resolution was complete in eight women (50%). Mean bleeding improvement score was 1.7. Mean duration of menses was 6.2 days ± 3.1 (range, 3–15 days; median, 8 days), which was shorter than that before embolization (P = .002, Wilcoxon test). Pelvic pain and pressure were improved in eight (80%) of 10 women.
Sixteen women completed 12-month follow-up. Hysterectomy was performed in one woman for recurrent symptoms 9 months after embolization. Eleven (73%) of 15 women with abnormal bleeding had improvement in menorrhagia, with complete resolution in eight (53%) of 15 women. The mean bleeding improvement score was 1.4. Mean duration of menses was 6.5 days ± 2.3 (range, 3–12 days; median, 8 days), which was shorter than that before embolization (P = .002, Wilcoxon test). Pelvic pain and pressure were improved in six (60%) of 10 women.
Nine women completed 24-month follow-up. Hysterectomy was performed in one woman for recurrent symptoms 13 months after embolization. Five (56%) of the nine women had complete resolution of abnormal bleeding, including the patient with unilateral embolization. The mean bleeding improvement score was 1.25. Mean duration of menses was 5.8 days (range, 3–8 days), which was shorter than that before embolization (P = .002, Wilcoxon test). Pelvic pain and pressure were improved in three (50%) of six women.
Hysterectomy for recurrence was performed in two women at 25 and 27 months, respectively, after embolization. Two women still had improvement in symptoms at the last follow-up visit, 73 and 72 months after embolization, but required either additional medical treatment or endometrial balloon thermocoagulation for recurrence.
No statistically significant difference was found between patients in whom embolization was performed with nonspherical polyvinyl alcohol particles and those in whom calibrated microspheres were used, or between patients with focal adenomyosis and those with diffuse adenomyosis.
Failures and Complications
In all of the women, regular menstrual cycles resumed after embolization. At 1 week after embolization, four women still had moderate cramping pain, two had mild vaginal discharge, and one had pelvic pain without hematoma. All of these symptoms spontaneously resolved.
In total, five women (28%) underwent hysterectomy: one woman, for early treatment failure (3.9 months after embolization), and four others, for recurrence of symptoms at 9, 13, 25, and 27 months after embolization and initial relief of symptoms. At pathologic analysis of five tissue specimens from hysterectomy, areas of necrosis were seen, but viable foci of adenomyosis were also identified in all five. Three other women who experienced initial improvement after embolization required additional medical treatment (two women) or endometrial balloon thermocoagulation (one woman).
In total, eight (44%) of 18 women required additional therapy after embolization because of failure or recurrence.
No severe vaginal discharge, pelvic infection, or definitive amenorrhea was observed after embolization in our patients.
Follow-up US and MR Imaging
Follow-up imaging was performed at an average of 5.3 months ± 1.3 after embolization in 16 women. The mean uterine volume had decreased significantly, by 15% ± 18% (P = .009, Wilcoxon test) (Fig 2). The mean adenomyoma volume decreased by 25% ± 19%, but this difference was not statistically significant (P = .679, Wilcoxon test) (Fig 3) (Table).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Symptoms related to adenomyosis are nonspecific and are similar to those encountered in other nonmalignant conditions, such as endometriosis and leiomyoma (1–3). In particular, differentiation of adenomyosis from leiomyoma is critical because this is the most frequently encountered pitfall and the therapeutic options differ. Uterus-preserving therapy, including myomectomy and uterine artery embolization, is possible for leiomyoma, whereas hysterectomy is often considered the definitive treatment for debilitating adenomyosis (3).
Therefore, the diagnosis of adenomyosis should be established with imaging (13–16,20). Imaging is also performed to determine the type and the extent of myometrial invasion. It has been suggested that transvaginal US allows the diagnosis of adenomyosis with a high accuracy, even when associated disorders such as fibroids are present (13). In our study, US was used in the first six women. Adenomyosis was considered present if abnormal myometrial echogenicity, poor definition of the endomyometrial junction, and/or myometrial cysts were present (13,16). However, several studies have shown MR imaging to be highly accurate, with sensitivity and specificity of more than 90% (13–16,20). When MR imaging was used, adenomyosis was considered present if the junctional zone was greater than 12 mm, with or without myometrial foci of high signal intensity on sagittal T2-weighted MR images (14–16). Imaging features that favor adenomyoma instead of leiomyoma were focal thickening of the junctional zone, poorly defined margins, and minimal mass effect (20).
Uterine artery embolization is a very effective procedure to treat uterine fibroids, and it has been successful in large numbers of patients (4–7). Because of the usefulness of uterine artery embolization for treating a variety of uterine bleeding disorders (eg, postpartum hemorrhage, vascular malformations, and uterine fibroids), we offered embolization to patients who were seeking a nonsurgical alternative for adenomyosis-related symptoms.
In the literature, four studies of women who underwent uterine artery embolization for adenomyosis have been reported, but the study populations differed from ours (9–12). In a study that included 15 women, Siskin et al (9) reported that only six women had adenomyosis without associated fibroids. Similarly, Jha et al (12) reported a study of 30 patients, among whom adenomyosis without fibroids was diagnosed in only three patients. In the other two articles, the percentage of women who manifested both uterine fibroids and adenomyosis was not reported (10,11). When uterine fibroids occur in association with adenomyosis, it is virtually impossible to differentiate the symptoms of one disorder from the other. This is why we specifically addressed adenomyosis-related symptoms. Since pure adenomyosis is a relatively rare condition, however, our study population was limited.
The mean duration of clinical follow-up reported in published studies ranges from 5 to 8.2 months (9–12). However, midterm evaluation is crucial because different authors have implicated adenomyosis in the failure of uterine fibroid embolization (4,6,8). Our study has confirmed this trend with disappointing midterm results of uterine artery embolization for adenomyosis. Most patients reported initial clinical improvement, but the percentage of improvement decreased with time, and only 56% of women still experienced improvement after 2 years. Our study shows minimal uterine volume reduction, compared with that obtained after embolization for uterine fibroids (4–7). The usefulness of contrast-enhanced MR imaging during follow-up of treated patients is emphasized in a recent article (12). Devascularization of regions of adenomyosis may be useful for predicting the long-term success of embolization. In our study, all women undergoing hysterectomy for treatment failure had viable areas of adenomyosis, a fact that lends support to the hypothesis that only infarction of areas of adenomyosis may lead to durable clinical improvement.
Intense postprocedural pain was observed after embolization in most patients, probably because of myometrial ischemia induced by the embolization technique used (21,22). As initially reported with uterine fibroid embolization, the technique of embolization here consisted of complete occlusion (stasis or near stasis) of both uterine arteries (4,6). Since the use of small particles (<300 µm in diameter) in uterine artery embolization may lead to extensive myometrial necrosis and to unintended ovarian artery embolization through a patent utero-ovarian anastomosis, only large particles were used in this study (21,23). However, adenomyosis differs from fibroids, and it may be hypothesized that small particles may be more effective for devascularization of adenomyosis foci. Although a case of expulsion of an infected adenomyoma was reported recently (24), no major complications were observed in the group of women in that study.
There are limitations to this study. Follow-up examinations involved US or MR imaging without contrast enhancement, except examinations for uterine volume measurements, which involved contrast-enhanced MR imaging. In addition, the small sample size precludes more extensive statistical analysis, particularly to compare clinical outcomes of focal and diffuse types of adenomyosis. To the best of our knowledge, however, this is the largest study of patients with isolated adenomyosis.
In conclusion, our data demonstrate initial resolution of symptoms after uterine artery embolization for adenomyosis. Mid- and long-term results, however, seem disappointing. In view of our limited experience, we believe that embolization should only be offered to women with realistic expectations regarding the duration of clinical improvement.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, J.P.P., D.J.; study concepts and design, J.P.P.; literature research, J.P.P., D.J., A.F., O.L.D.; clinical studies, J.P.P., D.J., A.F., O.L.D.; data acquisition, J.P.P., D.J., J.N., A.L.; data analysis/interpretation, J.P.P., A.L., J.N.; statistical analysis, A.L., J.P.P.; manuscript preparation, J.P.P., D.J.; manuscript definition of intellectual content, J.P.P., R.R., O.L.D.; manuscript editing, J.P.P.; manuscript revision/review, J.P.P., A.F., R.R., O.L.D.; manuscript final version approval, all authors
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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This article has been cited by other articles:
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  G. Tropeano, S. Amoroso, and G. Scambia Non-surgical management of uterine fibroids Hum. Reprod. Update, May 1, 2008; 14(3): 259 - 274. [Abstract] [Full Text] [PDF]
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 A. Van Langendonckt, J. Donnez, S. Defrere, G. A.J. Dunselman, and P. G. Groothuis Antiangiogenic and vascular-disrupting agents in endometriosis: pitfalls and promises Mol. Hum. Reprod., May 1, 2008; 14(5): 259 - 268. [Abstract] [Full Text] [PDF]
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 M. D. Kim, S. Kim, N. K. Kim, M. H. Lee, E. H. Ahn, H. J. Kim, J. H. Cho, and S. H. Cha Long-Term Results of Uterine Artery Embolization for Symptomatic Adenomyosis Am. J. Roentgenol., January 1, 2007; 188(1): 176 - 181. [Abstract] [Full Text] [PDF]
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 S. Chopra, A. S. Lev-Toaff, F. Ors, and D. Bergin Adenomyosis:common and uncommon manifestations on sonography and magnetic resonance imaging. J. Ultrasound Med., May 1, 2006; 25(5): 617 - 627. [Abstract] [Full Text] [PDF]
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 J.-P. Pelage, J. Cazejust, E. Pluot, O. L. Dref, A. Laurent, J. B. Spies, S. Chagnon, and P. Lacombe Uterine Fibroid Vascularization and Clinical Relevance to Uterine Fibroid Embolization RadioGraphics, October 1, 2005; 25(suppl_1): S99 - S117. [Abstract] [Full Text] [PDF]
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 J. Goldberg, J.-P. Pelage, D. Jacob, and O. L. Dref Uterine Artery Embolization for Adenomyosis: Looking at the Glass Half Full * Dr Pelage and colleagues respond: Radiology, September 1, 2005; 236(3): 1111 - 1112. [Full Text] [PDF]
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