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Original Research |
1 Department of Radiology, Georgetown University Hospital, Lombardi Cancer
Center, Washington, DC 20007.
2 Present address: Department of Radiology, Kobe University Graduate School of
Medicine, 7-5-2 Kusunokicho Chuo-ku Kobe, Hyogo 650-0017, Japan.
Received October 26, 2004;
accepted after revision February 9, 2005.
Address correspondence to Y. Kitamura.
Abstract
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SUBJECTS AND METHODS. Nineteen patients with symptomatic pure or dominant adenomyosis on MRI were referred for UAE. All 19 patients had repeat MRI 4 months after UAE. The MR images obtained before and after UAE were evaluated for maximal junctional zone thickness, junctional zone-myometrial ratio, uterine volume, and the presence of avascular regions. Patients were asked to complete a questionnaire about their symptoms before and 3 and 12 months after UAE.
RESULTS. Uterine volume decreased significantly after UAE (p < 0.01). The mean uterine volume reduction was 25.1%. Junctional zone thickness decreased significantly (p < 0.001). The junctional zone-myometrial ratio did not decrease significantly (p = 0.526). Fourteen (73.7%) of the 19 patients showed devascularized change within the adenomyotic region. Eighteen patients completed a questionnaire at 3 months. Sixteen (88.9%) of the 18 reported an improvement in symptoms, whereas the two remaining patients (11.1%) reported no change (p < 0.001). Of the 16 patients with clinical improvement, 11 had devascularized areas after UAE and five did not. Eleven of the 18 patients who completed a questionnaire 3 months after UAE also completed a questionnaire 12 months after UAE. Ten of these 11 patients still reported continued improvement, and one patient reported a worsening of symptoms.
CONCLUSION. UAE in patients with pure or dominant adenomyosis results in decreased uterine volume and regions of devascularization. Most patients reported an improvement in clinical symptoms within 3 months after UAE. Some patients reported benefit for at least 1 year; however, the long-term durability of symptomatic relief remains unknown.
Keywords: adenomyosis • embolization • MRI • pelvic imaging • women's imaging
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Since uterine artery embolization (UAE) was first described in 1995 [4] as a treatment for symptomatic fibroids, this procedure has gained popularity as a less invasive alternative to hysterectomy [5-7]. Because several studies have reported symptomatic improvement after UAE in women who have both fibroids and adenomyosis, investigators have proposed UAE for managing symptomatic adenomyosis [3, 8]. However, it is unclear from the current literature whether clinical improvement in these patients after UAE is attributed to changes associated with fibroids, adenomyosis, or both. Therefore, we undertook this study to evaluate the MRI features in patients with pure or dominant adenomyosis before and after UAE and to correlate those imaging features with clinical symptoms.
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The patients' ages ranged from 30 to 51 years (mean, 44.6 years) (Table 1). Baseline MRI was performed approximately 2 months before UAE (range, 6-324 days; mean interval, 67.2 days). Repeat MRI was performed approximately 4 months after UAE (range, 6-240 days; mean interval, 115.7 days). Eleven of 19 patients had pure adenomyosis, and eight had dominant adenomyosis. If we exclude the two patients with baseline MRI examinations performed more than 180 days before UAE (patients 3 and 16 in Table 1), the interval between baseline MRI and UAE was 6-114 days (mean interval, 40.5 days) and repeat MRI was performed approximately 3.5 months (mean) after UAE (range, 6-182 days; mean interval, 103.5 days). The mean age of the 17 patients was 44.5 years. Ten of the 17 patients had pure adenomyosis, and seven had dominant adenomyosis.
An experienced angiographer performed bilateral selective UAE using either polyvinyl alcohol (PVA) particles (Contour, Boston Scientific/Meditech; Ivalon, Cook; or Turfill, Cordis) or trisacryl gelatin microspheres (Embosphere Microspheres, Biosphere Medical). Either 355- to 500-µm PVA particles or 500- to 700-µm trisacryl gelatin microspheres were used. The institutional review board approved the entire study, and each patient gave written informed consent before undergoing the procedure.
Before UAE, all eligible patients had their symptoms reviewed by an experienced angiographer. After UAE, patients were asked to complete a questionnaire about their symptoms 3 and 12 months after UAE to assess for any change in bleeding, pain, or pressure. We did not discriminate between bleeding and pain or pressure symptoms. Symptomatic improvement was categorized as better, worse, or no change. A minority of the patients were on hormone therapy at the time of enrollment. We did not exclude them from analysis because they were sufficiently symptomatic to want to undergo UAE.
MRI Technique
MRI was performed with a 1.5-T superconducting system unit (Magnetom
Vision, Siemens Medical Solutions) in 33 examinations using a standard
phased-array torso coil. The sequences performed included axial relative to
the pelvis T2-weighted single-shot fast spin-echo (TR/TE range, 4,400/64-90;
flip angle, 150-160°); T2-weighted single-shot fast spin-echo orthogonal
relative to the uterus (4,400/64-90; flip angle, 150-160°); axial
T1-weighted fat-saturated spoiled gradient echo (TR/TE, 150/4; flip angle,
80°); and sagittal T1-weighted fat-saturated spoiled gradient echo (150/4;
flip angle, 80°) before and after the administration of contrast material.
Postcontrast imaging consisted of three dynamic runs after IV infusion of
gadopentetate dimeglumine (Magnevist, Berlex Laboratories) at a dose of 0.1
mmol/kg of body weight.
Five MRI examinations (four before UAE and one after UAE) were performed on a different 1.5-T superconducting system unit (Signa, GE Healthcare). The sequences performed included sagittal pre- and postcontrast T1-weighted spin-echo (TR range/TE range, 500-700/8-10); axial, sagittal, or axial and sagittal T2-weighted fast spin-echo (TR range/effective TE range, 923-7,300/88-132; and sagittal contrast-enhanced T1-weighted fat-saturated spoiled gradient echo (8.1/4.2; flip angle, 15°).
Data Evaluation
Two experienced MRI radiologists independently analyzed the MR images for
each patient. Each reviewer was given T1-weighted, T2-weighted, and delayed
gadolinium-enhanced T1-weighted images of the uterus, both before and after
UAE. We analyzed the images for the following features: uterine volume,
junctional zone thickness, junctional zone-myometrial ratio, distribution of
adenomyosis, and enhancement before UAE.
Uterine volume was calculated using the following equation for a prolate
ellipse: (volume [cm3] = length x width x height
x 0.523) (Figs. 1A and
1B). The reduction rate in
uterine size was also calculated as a percentage as follows:
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Statistical Analysis
To assess the significance of the changes in uterine volume, junctional
zone thickness, and junctional zone-myometrial ratio, paired Student's
t tests were performed. The Mann-Whitney U test was used to
assess the significance of the changes in vascularity after UAE. It was also
used to assess the relationship between adenomyosis and myometrial enhancement
before UAE with devascularization after UAE. To assess the significance of
changes in clinical symptoms 3 months after UAE, a Wilcoxon's signed rank test
was used. Statistical analysis was performed using software (Excel 2003,
Microsoft); p values of less than 0.05 or 0.01 were considered
statistically significant.
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Nineteen Patients
Uterine volume—A significant decrease (25.1%) in the mean
uterine volume—from 438.6 cm3 before UAE to 293.4
cm3 after UAE—was shown (p < 0.01).
Junctional zone thickness and junctional zone-myometrial ratio—There was a significant decrease in the mean junctional zone thickness of 13.7% between pre- and post-UAE MRI, from 36.3 to 31.4 mm, respectively (p < 0.001). In contradistinction, the junctional zone-myometrial ratio decrease from 0.799 to 0.784 (1.9%) was not significant (p =0.526). Characteristics and changes in vascularity of adenomyosis—Before UAE, 12 of the 19 patients had an asymmetric diffuse pattern, five had a symmetric diffuse pattern, and two had a focal pattern of adenomyosis. One of the 12 patients with an asymmetric pattern also had a focal adenomyoma. Eighteen of the 19 patients received IV contrast material. All 18 patients had a homogeneous enhancement pattern. In this group, 12 had enhancement less than myometrium, two had enhancement more than myometrium, and four had enhancement equal to myometrium.
All 19 patients had a postcontrast MR examination approximately 4 months after UAE (Fig. 6). Fourteen of 19 patients showed at least one area of devascularization (hereafter referred to as the "devascularized group") within the adenomyosis (Figs. 7A, 7B, 7C, 7D, and 7E). The remaining five patients had a homogeneous enhancement pattern after contrast administration (hereafter referred to as the "not-devascularized group") (Figs. 8A, 8B, 8C, and 8D). These five patients include the one patient who did not receive IV contrast material on the MRI examination performed before UAE. The pattern of adenomyosis for each individual patient did not change after UAE. There was no significant relationship between adenomyosis enhancement relative to the myometrium before UAE and the presence of devascularized areas after UAE (p = 0.610).
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Of the 14 patients in the devascularized group, the distribution of adenomyosis before and after UAE included 10 patients with asymmetric diffuse adenomyosis, three patients with symmetric diffuse adenomyosis, and one patient with an adenomyoma. One of the 10 patients with asymmetric diffuse pattern had a concomitant adenomyoma that also had regions of devascularization after UAE.
Of the five patients in the not-devascularized group, the distribution of adenomyosis before and after UAE included two patients with asymmetric diffuse adenomyosis, another two patients with symmetric diffuse adenomyosis, and one patient with a focal adenomyoma.
Clinical changes—Eighteen of the 19 patients completed symptom questionnaires 3 months after UAE (Fig. 9). Sixteen of these patients reported an improvement in symptoms, and two patients reported no change in symptomatology (p < 0.001). Of the 16 patients with clinical improvement, the distribution pattern of adenomyosis was asymmetric diffuse in nine patients, symmetric diffuse in five patients, and focal adenomyosis in two patients. In these same patients, regions of devascularization after UAE were observed in seven patients, three patients, and one patient, respectively. The two patients without clinical improvement had an asymmetric diffuse pattern of adenomyosis and devascularized regions after UAE.
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Overall, of the 16 patients with clinical improvement, 11 had regions of devascularization and the two patients without change in symptoms also had regions of devascularization.
Eleven patients completed symptom questionnaires 12 months after UAE (Fig. 10). All 11 had also completed symptom questionnaires 3 months after UAE. Ten women reported clinical improvement; this includes nine women with continued improvement compared with their 3-month questionnaire and one patient, a patient who had reported no change in symptoms at 3 months after UAE, now reporting clinical improvement. Of these 10 women with clinical improvement, the distribution pattern of adenomyosis was asymmetric diffuse in seven patients, symmetric diffuse in two patients, and focal adenomyosis in one patient. In these same patients, regions of devascularization were observed in six, two, and zero patients, respectively. One patient reported worsening of symptoms at 12 months after UAE compared with clinical improvement 3 months after UAE. This patient had symmetric diffuse adenomyosis with regions of devascularization after UAE.
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There was no statistically significant difference in clinical symptoms between the two groups (devascularized and not devascularized) at both 3 and 12 months after UAE (p = 0.366 and p = 0.637, respectively).
Seventeen Patients
Uterine volume—A significant decrease (23.4%) in the mean
uterine volume—from 441.4 cm3 before UAE to 298.4
cm3 after UAE—was shown (p < 0.05).
Junctional zone thickness and junctional zone-myometrial ratio—There was a significant decrease in the mean junctional zone thickness of 13.3%: from 37.0 mm before UAE to 32.1 mm after UAE (p < 0.005). In contradistinction, the junctional zone-myometrial ratio decrease (0.13%) from 0.796 before UAE to 0.795 after UAE was not significant (p = 0.978).
Characteristics and changes in vascularity of adenomyosis—Before UAE, 11 of 17 patients had an asymmetric diffuse pattern, four had a symmetric diffuse pattern, and two had a focal pattern of adenomyosis. One of the 11 patients with an asymmetric pattern also had a focal adenomyoma. Sixteen of the 17 patients received IV contrast material. All 16 patients had a homogeneous enhancement pattern. In this group, 11 had enhancement less than myometrium, two had enhancement more than myometrium, and three had enhancement equal to myometrium.
All 17 patients had a postcontrast MR examination approximately 3.5 months after UAE. Twelve of the 17 patients showed at least one area of devascularization (devascularized group) within the adenomyosis (Figs. 7A, 7B, 7C, 7D, and 7E). The remaining five patients had homogeneous enhancement pattern after contrast administration (not-devascularized group) (Figs. 8A, 8B, 8C, and 8D). These five patients included the one patient who did not receive IV contrast material on the pre-UAE MRI examination. The pattern of adenomyosis for each individual patient did not change after UAE. There was no significant relationship between adenomyosis enhancement relative to the myometrium before UAE and the presence of devascularized areas after UAE (p = 0.657).
Of the 12 patients in the devascularized group, the distribution of adenomyosis before and after UAE included nine patients with asymmetric diffuse adenomyosis, two patients with symmetric diffuse adenomyosis, and one patient with an adenomyoma. One of the nine patients with asymmetric diffuse pattern had a concomitant adenomyoma that also had regions of devascularization after UAE.
Of the five patients in the not-devascularized group, the distribution of adenomyosis before and after UAE included two patients with asymmetric diffuse adenomyosis, another two patients with symmetric diffuse adenomyosis, and one patient with a focal adenomyoma.
Clinical changes—Sixteen of the 17 patients completed symptom questionnaires 3 months after UAE. Fifteen of these patients reported an improvement in symptoms and one patient reported no change in symptoms (p < 0.001). Of the 15 patients with clinical improvement, the distribution pattern of adenomyosis was asymmetric diffuse in nine patients, symmetric diffuse in four patients, and focal adenomyosis in two patients. In these same patients, regions of devascularization after UAE were observed in seven patients, two patients, and one patient, respectively. The one patient without clinical improvement had an asymmetric diffuse pattern of adenomyosis and devascularized regions after UAE.
Overall, of the 15 patients with clinical improvement, 10 had regions of devascularization, whereas the remaining one patient without change in symptoms also had regions of devascularization.
Ten patients completed a questionnaire about their symptoms 12 months after UAE. All 10 had also completed symptom questionnaires 3 months after UAE. All 10 women reported clinical improvement. This includes nine women with continued improvement compared with their 3-month questionnaire and one patient, a patient who had reported no change in symptoms at 3 months after UAE, now reporting clinical improvement. Of these 10 women with clinical improvement, the distribution pattern of adenomyosis was asymmetric diffuse in seven patients, symmetric diffuse in two patients, and focal adenomyosis in one patient. In these same patients, regions of devascularization were observed in six, two, and zero patients, respectively.
Overall, of the 10 patients with clinical improvement, eight had regions of devascularization after UAE.
There was no statistically significant difference in clinical symptoms
between the two groups (devascularized vs not devascularized) at 3 and 12
months after UAE (p = 0.500 and p = 
,
respectively).
No major complications have been reported as a result of UAE in our patient groups.
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The exact cause of bleeding in adenomyosis is still unclear. Current hypotheses include increased cavitary surface resulting from uterine hypertrophy and decreased myometrial contraction due to intramural fibrosis resulting in compromised or insufficient venous flow during menstruation [1, 2, 12]. Ota et al. [12] reported that vascularization during the proliferative phase is increased markedly in terms of number and the total surface area of capillaries in patients with adenomyosis and speculated that these vessels are unable to contract completely, resulting in an increased volume of bleeding.
The definitive treatment for adenomyosis is still hysterectomy. Hormonal therapy or ablation may be helpful in some patients, but neither is durable [2]. Furthermore, although UAE has gained popularity as a minimally invasive treatment for symptomatic fibroids, coexisting adenomyosis was initially considered a contraindication for UAE because of the potential for uncontrollable bleeding [13]. Several studies, however, have reported no untoward effects after UAE in women with both fibroids and adenomyosis. For example, in a retrospective review by Siskin et al. [8], nine of 13 patients with both conditions underwent UAE without complication and most patients reported an improvement in symptoms. Similarly, in a retrospective review by Jha et al. [3], 27 of 30 patients with fibroids and adenomyosis underwent successful UAE and reported symptomatic improvement. However, in these two studies of women with both fibroids and adenomyosis, it is unclear which condition (or both) was symptomatic and was therefore effectively treated by UAE. Neither study described the relative proportions of adenomyosis or fibroids in the patients studied. Therefore, we restricted our study group to symptomatic women with a junctional zone width of greater than 12 mm, women with coexisting fibroids of less than 4 cm in diameter, or women with both.
We showed that both uterine volume and junctional zone thickness decreased significantly after UAE: 25.1% and 13.7% for 19 patients and 23.4% and 13.3% for 17 patients, respectively. Significant reduction in uterine size after UAE in women with both conditions has also been reported by Siskin et al. [8] and Jha et al. [3], 42% and 40%, respectively. The fact that uterine volume reduction was greater in these other series as compared with ours may be a function of large (> 4 cm) concomitant fibroids that accounted for the bulk of uterine volume decrease. Similarly, a significant decrease in junctional zone thickness was also reported by Siskin et al. and Jha et al. (33% and 22-33%, respectively). It is certainly possible that a greater reduction in junctional zone width may have been seen in these patients if there were fibroids embedded within the regions of adenomyosis that shrank markedly after successful UAE.
Because increased endometrial cavity size contributes to bleeding with adenomyosis [1, 2], reduction in total uterine size with an associated reduction in endometrial size after UAE may explain, in part, alleviation of symptoms. In addition, decrease in junctional zone thickness may play an equally important role in symptom reduction because the increased microvessel density associated with adenomyosis is observed mainly in the junctional zone-myometrium [14]. After UAE, there was no significant change in the junctional zone-myometrial ratio. This is similar to the experience in women with adenomyosis who were treated with gonadotropin-releasing hormone analog [15].
In our series, 14 of 19 patients and 12 of 17 patients showed regions of partial or total devascularization within the site of adenomyosis after UAE. Ten (71.4%) of those 14 patients and nine (75%) of those 12 patients had the asymmetric diffuse pattern of adenomyosis. It is unclear why areas of devascularization tend to be associated more frequently with the asymmetric diffuse pattern. Based on our literature search, there have been no documented differences in the appearance or the distribution of vessels for the different patterns of adenomyosis (e.g., asymmetric diffuse, symmetric diffuse, or focal). Interestingly, the five patients with no detectable devascularized areas on follow-up MRI still reported an improvement in symptoms. This suggests that the extent of grossly visible devascularization may not be a factor or may not be the only factor affecting symptom improvement after UAE. (It is possible that clinical improvement after UAE may depend on the secondary changes related to infarction at the microvessel level and may not be a function of visible devascularization and overall uterine volume reduction.) That is, sheer reduction in uterine size and hence myometrium may affect symptoms because four of the five patients had a decrease in uterine volume. The relationship between gross infarction and clinical symptoms is further complicated by noting that two patients with devascularized regions after UAE reported no clinical improvement. Again, this finding underscores that devascularization is likely not the only factor affecting clinical symptoms.
Our most dramatic result was the 88.9% and 94.4% improvement in symptoms 3 months after UAE in 19 and 17 patients, respectively. Symptom improvement was not related to the pattern of adenomyosis before UAE or the presence of visible devascularized regions after UAE. Only 11 of 18 patients in the 19-patient analysis completed a symptom questionnaire 12 months after UAE. The fact that one patient's symptoms recurred approximately 12 months after UAE, coupled with the small number of respondents, makes the long-term durability of UAE for symptom relief unknown.
Our study has several limitations. First, there were a small number of patients despite nearly 4 years of recruitment. Therefore, conclusions about what type of adenomyosis may respond best to UAE and the implications of devascularized areas after UAE remain unknown. A second limitation is that we did not take menstrual cycle into consideration for evaluating the thickness of the junctional zone and the size of the uterus. Although menstrual cycle changes could affect uterine volume, the effect on junctional zone width is less pronounced because the junctional zone width is relatively refractory to the different cycles of the menses. Furthermore, we did not exclude patients on endocrine therapy, believing that they were symptomatic enough, despite hormone treatment, to want to undergo UAE. Third, although we focused on pure or dominant adenomyosis, the fact that some patients had fibroids, even small ones, may have affected our results. A fourth limitation is the absence of long-term follow-up in all cases, so we cannot comment on the long-term durability of UAE in patients with pure or dominant adenomyosis. However, the fact that slightly more than half of our patients reported symptomatic improvement up to 1 year after the procedure suggests that UAE may offer temporary symptomatic relief for women with adenomyosis. The possibility of repeat UAE in women with adenomyosis who have had symptom recurrence is an interesting one, although to date we have not performed repeat UAEs in this patient group.
In conclusion, UAE in patients with pure or dominant adenomyosis results in decreased uterine volume and junctional zone width. These changes may also be accompanied by devascularized areas in the adenomyosis. Three months after UAE, nearly all patients with pure or dominant adenomyosis reported an improvement in symptoms regardless of enhancement pattern. Of the respondents who completed symptom questionnaires 1 year after UAE, slightly more than half of the original 19 patients reported continued improvement of clinical symptoms. UAE may be beneficial in patients with pure or dominant adenomyosis for at least 1 year. The long-term durability of UAE in this patient population remains unknown, and without data to determine that durability, embolization cannot yet be recommended as an alternative to surgery for long-term symptom control.
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