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1 All authors: Department of Radiology, A-113, Albany Medical College, 47 New Scotland Ave., Albany, NY 12208.
Received October 2, 2000;
accepted after revision February 2, 2001.
Address correspondence to G. P. Siskin.
Abstract
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MATERIALS AND METHODS. A retrospective review of 15 patients with adenomyosis and menorrhagia who underwent uterine artery embolization was performed. The diagnosis of adenomyosis was based on established MR imaging criteria. Clinical response was assessed at a minimum of 3 months after embolization. Follow-up MR imaging was performed 6 months after embolization.
RESULTS. Of the 15 patients in this study, five had diffuse adenomyosis without evidence of uterine fibroids, one had focal adenomyosis without evidence of uterine fibroids, and the remaining nine had adenomyosis with one or more fibroids. At follow-up, 12 (92.3%) of the 13 patients reported significant improvement in presenting symptoms and quality of life. One patient continued experiencing menorrhagia, and one patient experienced amenorrhea during the 5 months of follow-up after embolization. MR imaging in nine patients, performed at a mean of 5.9 months after embolization, revealed significant reductions in median uterine volume (42%), median fibroid volume (71%), and mean—junctional-zone thickness (11 mm; 33%; p < 0.5). Six of the nine patients had subendometrial regions of decreased T2 signal intensity after embolization.
CONCLUSION. Uterine artery embolization is a promising nonsurgical alternative for patients with menorrhagia and adenomyosis. Significant improvement in presenting symptoms and in quality of life is associated with decreases in uterine size and junctional zone thickness. Larger prospective studies are needed to establish the safety and efficacy of this procedure for patients with adenomyosis.
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Uterine artery embolization has been shown to be an effective treatment for uterine bleeding caused by a variety of conditions, including postpartum hemorrhage, postoperative hemorrhage, cervical pregnancy, and arteriovenous malformations [6,7,8]. Recently, uterine artery embolization has emerged as a treatment option for patients with symptomatic uterine fibroids. The procedure results in the reduction of both uterine and fibroid volume and in significant improvements in associated symptoms and quality of life [9,10,11,12,13].
In our interventional radiology practice, we noted that many patients referred for uterine artery embolization on the basis of initial sonographic screening studies and clinical symptoms suggestive of fibroids were, in fact, shown to have adenomyosis on preembolization MR imaging of the pelvis. We expected this finding, given the frequent coexistence of adenomyosis and fibroids, their often similar clinical symptoms, and the potential difficulties in identifying adenomyosis at screening sonography [4]. The purpose of this study was to report the clinical response and MR imaging appearance of the uterus in patients who underwent uterine artery embolization for the treatment of menorrhagia in the presence of adenomyosis.
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To date, 224 patients have undergone uterine artery embolization for the treatment of symptomatic uterine fibroids at our institution. Our study population consisted of 15 patients who had a diagnosis of adenomyosis based on MR imaging performed before uterine artery embolization. These patients had a mean age of 46.5 years (range, 37-56 years). All patients presented with abnormal uterine bleeding, 11 (73.3%) of 15 patients presented with dysmenorrhea, and seven (46.7%) of 15 patients presented with bulk-related symptoms, including abdominal distention and bladder compression with frequent urination. Three patients (20%) underwent a trial of hormonal therapy with a gonadotropin-releasing—hormone antagonist before embolization. No patient in this study population underwent myomectomy or endometrial ablation before embolization. Twelve of 15 patients had at least one child, with seven patients reporting a minimum of one miscarriage. Of note, one patient had a history of protein S and possibly protein C deficiency that was of uncertain clinical significance.
All patients underwent preprocedural and 6-month follow-up MR imaging of the pelvis. MR imaging included axial and sagittal echo-train (fast spin-echo T2-weighted) and axial gradient T1-weighted with and without fat saturation images. Images were acquired with a Signa 1.5-T system (General Electric Medical Systems, Milwaukee, WI). A torso phased-array coil, 5-mm—thick sections with a 2.5-mm gap, a 256 x 256 matrix, and 2 excitations were used for all series. All studies were reviewed both prospectively and retrospectively by two radiologists, with a consensus report ultimately generated after formal review. Uterine and index myoma volume (length x height x width x 0.5233) were calculated for each study patient. A maximal—junctional-zone measurement was then obtained with hand calipers. Adenomyosis was considered present if any portion of the junctional zone was greater than 12 mm in thickness. The presence of myometrial high-signal foci was considered ancillary evidence of adenomyosis.
After the presence of adenomyosis was diagnosed with MR imaging, therapeutic options were discussed with all patients. Embolization was included as an option because of its success at addressing identical symptoms in patients with uterine fibroids [9,10,11,12,13]. Whereas none of the patients in the study population had contraindications for surgery, they all strongly preferred avoiding surgical treatment if another option was available. After their options were reviewed, all patients selected embolization as their treatment of choice; no patient in our population with MR imaging findings consistent with adenomyosis decided to undergo hysterectomy. Written informed consent was obtained from all patients before embolization.
The technique and protocol used for embolization were the same as those used during uterine artery embolization for the treatment of symptomatic uterine fibroids. The right common femoral artery was used for arterial access in all patients. After obtaining a nonselective pelvic arteriogram (Fig. 1A), we catheterized the left uterine artery, using a 5-French Cobra Glidecatheter (Terumo; Boston Scientific, Watertown, MA) and a 0.035-inch Glidewire (Terumo; Boston Scientific). Once the catheter position was confirmed (Fig. 1B), Contour polyvinyl alcohol particles (Interventional Therapeutics, Fremont, CA) measuring 355-500 µm in diameter were injected until stasis of flow was achieved. The right uterine artery was then selectively catheterized (Fig. 1C), and additional particles were injected until the vessel was occluded. In patients in whom the Cobra catheter was flow-limiting when positioned in one or both uterine arteries, a Tracker-325 catheter (Target; Boston Scientific) was used in a coaxial fashion to deliver the polyvinyl alcohol particles. After bilateral uterine artery embolization, completion angiography was performed in all patients to document arterial occlusion and to determine if significant collateral supply to the uterus was present. Polyvinyl alcohol particles measuring 355-500 µm in diameter were selected on the basis of their effectiveness shown during uterine fibroid embolization [12].
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We performed embolization on an outpatient basis in all patients, using a protocol described previously [14]. All patients were contacted by telephone 2 or 3 times during the first 7-10 days of the immediate postprocedure recovery period. Patients were then seen in the clinic at 1 month for a follow-up appointment. At the time of follow-up imaging, a questionnaire was given to each patient to assess the changes in their presenting symptoms and quality of life. This questionnaire is used to assess the degree of clinical improvement in all patients undergoing uterine artery embolization at our institution. Patients were presented with a list of items assessing quality of life before and after embolization; variables included the ability to perform activities of daily life and to socialize outside the home, overall energy level, the degree of interest in and pain experienced during sexual intercourse, and the degree of pain or cramping experienced during menstruation. Patients were asked to rank the degree of severity or impairment, using a scale of 1-10 (with 1 representing "no severity or impairment" and 10 representing "severe severity or impairment").
We performed statistical analysis, using the Wilcoxon's rank sum test, to assess the significance of the changes in responses to the questionnaire before and several months after embolization. In addition, summary descriptive statistical tests and the Wilcoxon's sum rank test were used to assess the significance of reductions in uterine volume, fibroid volume, and junctional zone thickness after embolization.
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Bilateral uterine artery embolization was successfully performed in all patients. The mean duration of the procedure in this group of 15 patients was 60.9 min (range, 44-87 min). In four patients, embolization was performed with a 5-French Cobra Glidecatheter, and in 11 patients, a microcatheter was required because of the occlusive nature of the Cobra catheter in one or both uterine arteries. The expected postprocedure symptoms, including pelvic pain, nausea, and fever, occurred in all patients and were treated according to a previously described protocol with medications including meperidine hydrochloride (Demerol; Abbott Laboratories, Chicago, IL), ketorolac tromethamine, hydrocodone bitartrate and acetaminophen (Lortab; UCB Pharma, Atlanta, GA), and prochlorperazine (Compazine; SmithKline Beecham, Philadelphia, PA) in all patients [15].
Clinical response was assessed by a questionnaire that addressed quality-of-life variables before and after embolization. Questionnaire follow-up at a minimum of 3 months after embolization was available in 13 patients. One patient was lost to follow-up after the embolization procedure. The mean length of clinical followup was 8.2 months (range, 3-16 months) after embolization. The variables assessed on this questionnaire, the median response values before and after embolization, and the statistical significance of the responses are listed in Table 1. We noted statistically significant improvement in the ability to perform activities of daily life and to socialize outside the home, overall energy level, the degree of pain experienced during sexual intercourse, and the degree of pain or cramping experienced during menstruation when comparing the responses obtained before and after embolization (p < 0.05). No significant changes were noted in the level of interest in sexual intercourse after embolization. On the basis of data obtained from this questionnaire, we found that there was also statistically significant improvement in the number of days patients experienced bleeding during the menstrual cycle and in the amount of time between changes of sanitary napkins or tampons during the menstrual period (p < 0.05).
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Imaging follow-up was available in nine patients at a mean duration of 5.9 months (range, 4.25-7.25 months) after embolization. In these nine patients, the mean—uterine-volume measurement decreased from 455.4 to 230.6 cm3. The median percentage of reduction in uterine volume was 42% (range, 24.4-65.0%; p < 0.05). The mean volume of the dominant fibroid identified in the six patients with fibroids and adenomyosis on MR imaging follow-up decreased from 56.5 to 27.0 cm3. The median percentage reduction in the 11 fibroids seen in six patients was 71% (range, 18.7-100%; p < 0.05). Mean thickness of the junctional zone in the nine patients with MR imaging follow-up decreased from 31 to 20 mm. The median percentage reduction in junctional zone thickness was 33% (range, 0-60%; p < 0.05). Six patients with MR imaging follow-up showed residual areas of decreased signal on T2-weighted images in the subendometrial region of the uterus (Figs. 1A,1B,1C,1D,1E,1F and 2A,2B,2C,2D).
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One patient with diffuse adenomyosis and multiple uterine fibroids reported no significant improvement in her presenting symptoms. She presented initially with abnormal uterine bleeding and continued to experience heavy bleeding during her menstrual period 4 months after the embolization procedure and is, therefore, considered a treatment failure. To date, this patient has not undergone additional procedures to address this bleeding. A second patient, 48 years old, with diffuse adenomyosis and no evidence of fibroids, who presented initially with abnormal bleeding, has not resumed her menstrual periods in the 5 months available for follow-up after embolization.
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Clinically, the diagnosis of adenomyosis is difficult to make, as evidenced by the patient population in our study. The typical presenting symptoms, including abnormal uterine bleeding, dysmenorrhea, and uterine enlargement, are nonspecific and not easily attributed to adenomyosis. In fact, these patients are frequently diagnosed with uterine fibroids, with a definitive diagnosis obtained only after pathologic examination. The exact cause of the abnormal bleeding in adenomyosis is unknown. Ota et al. [1] theorized that adenomyosis results in an increase in the absolute number and surface area of endometrial capillaries, which leads to insufficient vasoconstriction, low resistance, and increased blood loss during menstruation.
Radiologic studies can aid in the diagnosis of patients with adenomyosis. The appearance of adenomyosis on transabdominal sonography was initially described by Walsh et al. [18] as irregular cystic spaces in the myometrium. Other findings include thickening and asymmetry of the anterior or posterior uterine walls, a heterogeneous myometrium, and uterine enlargement with preservation of normal myometrial echogenicity [19, 20]. These and other findings, including pseudo widening of the endometrium or poor definition of the endomyometrial junction, are more apparent on transvaginal sonography [4]. Pelvic MR imaging may be more accurate in diagnosing adenomyosis, with criteria including diffuse or focal widening of the junctional zone and bright foci or linear striations in the myometrium on T2-weighted images [4, 21]. On MR imaging, focal adenomyomas may appear as a localized low-signal myometrial mass with poorly defined margins that often contain high-signal foci [22].
Hysterectomy is the definitive treatment for adenomyosis, especially as the depth and degree of myometrial invasion increases [5, 19] because the endometrial islands characteristic of adenomyosis interdigitate with normal smooth muscle and do not have planes of cleavage with respect to the myometrium [17]. However, with increasing interest in nonoperative therapies for benign uterine disease, researchers have investigated the applicability of these therapies to adenomyosis has been investigated. Hormonal therapy is not reliable in patients with adenomyosis because the glands in the endometrial islands are of the basalis type, which are resistant to hormonal stimulation [23]. In fact, cyclic changes may or may not occur in the endometrial islands, depending on the number and quality of the estrogen and progesterone receptors [16]. Nonsurgical procedures, such as endometrial ablation, may represent a viable treatment option in patients in whom the extent and depth of myometrial penetration is limited [4, 19, 24].
In centers where embolization procedures are or have been performed without a screening MR examination, it is likely that this procedure has been performed in patients with undiagnosed adenomyosis because of its association with uterine fibroids. Smith et al. [25] reported a patient with menorrhagia and pelvic pain attributed to uterine fibroids, which were diagnosed on the basis of physical examination and pelvic sonography. This patient continued to experience abnormal bleeding and pelvic pain until the fifth month after the successful embolization of both uterine arteries, at which time a total vaginal hysterectomy was performed. Pathologic examination of the uterus revealed viable islands of adenomyosis and infarction of all existing fibroids. These authors attributed the failure of embolization to the presence of concurrent adenomyosis in this patient. Goodwin et al. [12] described six patients requiring hysterectomy after uterine artery embolization for symptomatic fibroids. Three of these patients had adenomyosis revealed at postoperative pathologic examination of the uterus. These initial reports have, therefore, implicated adenomyosis in the failure of uterine artery embolization to address the symptoms associated with uterine fibroids.
Given the frequent occurrence of adenomyosis with uterine fibroids, we believe that it is likely that several patients in earlier published studies on uterine fibroid embolization had fibroids and possibly adenomyosis. This statement can be made because MR imaging was not frequently used as a screening test in several of the earlier studies describing the success of this procedure [9, 10, 12]. This finding provided us with the initial rationale for offering the procedure to women with adenomyosis (with or without fibroids), who were not considering hysterectomy as the definitive treatment for this condition. More important, however, the ability of uterine artery embolization to successfully address menorrhagia in patients with uterine fibroids [9,10,11,12,13] potentially supported the use of this procedure in these patients, all of whom were seeking a nonsurgical alternative for the same presenting symptoms. Whereas the rationale for offering this procedure to our earliest patients consisted of these two points, the success seen in the early patients gave additional support to the remaining patients in the study population. Even though cases of treatment failure after embolization were reported in association with adenomyosis, we believed it was likely that patients with menorrhagia and adenomyosis still had the potential to benefit from this procedure.
The results of our study show the potential for embolization to successfully address the symptoms of patients with adenomyosis alone or in association with uterine fibroids. In this setting, symptoms cannot often be definitively attributed to either of these conditions. However, the often dramatic improvement noted in the presenting symptoms of our patients after embolization clearly merits its consideration as a nonoperative treatment option for these patients. In addition, whereas concurrent adenomyosis may still prove to be a factor in patients in whom embolization fails to treat the symptoms associated with uterine fibroids, the results of this study show that this conclusion is not foregone. Instead, this study and the preliminary results from two other studies [26, 27] suggest that patients diagnosed with adenomyosis on the basis of MR imaging, with or without the presence of uterine fibroids, have the potential to benefit from uterine artery embolization in terms of significant improvement in presenting symptoms.
After embolization, pathologic examination of the uterus and uterine fibroids revealed that embolization initiates infarction, necrosis, and ultimately hyaline degeneration in existing fibroids [28]. It is this response that is likely responsible for the long-term clinical benefits afforded to patients undergoing the embolization procedure. Theoretically, the diffuse nature of adenomyosis makes it unlikely that this mechanism plays a significant role in the changes induced by embolization. Instead, the polyvinyl alcohol particles, which are presumably directed toward the low-resistance vessels in the regions of the uterus affected by adenomyosis, likely lead to slow flow, a foreign body reaction, and eventual thrombosis [29]. The residual islands of decreased T2 signal in the subendometrial region of the uterus seen in many of our patients may represent regions of infarcted smooth muscle hypertrophy, occurring as a result of arterial thrombosis. The potential for collateral flow and luminal recanalization of the embolized vessels provide possible explanations for the continued viability of the islands of adenomyosis and the failure of embolization to work in this setting, but these are also possible explanations for the failure of uterine artery embolization in patients with uterine fibroids. Without the benefit of pathologic examination, the true mechanism of action of uterine artery embolization in patients with adenomyosis will remain unproven.
The small size of our study population prevents us from making any definitive conclusions regarding the risk of complications or treatment failure in patients with adenomyosis on the basis of whether focal or diffuse adenomyosis is present alone or with uterine fibroids. In our study, the two observed complications included treatment failure (manifested by continued bleeding during the months after embolization) and amenorrhea for 5 months after the procedure. The patient reporting the failure of embolization had both adenomyosis and uterine fibroids, whereas the patient reporting amenorrhea had diffuse adenomyosis without evidence of fibroids. Future studies, specifically focusing on the three distinct populations identified in this study, namely those with diffuse adenomyosis and no evidence of fibroids, those with focal adenomyosis and no evidence of fibroids, and those with diffuse or focal adenomyosis with uterine fibroids, would be valuable in determining if different considerations should be given to each type of patient when evaluating the use of embolization and the risk of complications. Our inability to divide patients into these three groups, because of the small size of the study population, does represent a significant limitation of this study.
In conclusion, our preliminary experience with uterine artery embolization for patients with adenomyosis (with or without uterine fibroids) was successful, with symptomatic improvement noted in 12 (92.3%) of 13 patients at 3-month follow-up. These results show that uterine artery embolization may be a promising nonsurgical treatment option for menorrhagia related to adenomyosis and that patients with uterine fibroids and adenomyosis should not automatically be excluded from undergoing uterine artery embolization. In addition, the potential benefit for patients with adenomyosis makes it clear that future prospective studies, with larger patient populations, need to be performed before definitive recommendations are made.
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