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Original Research |
1 Department of Diagnostic Radiology, Bundang CHA General Hospital, Pochon CHA
University, 351 Yatap-dong, Bundang-gu, Sungnam-si, Kyonggi-do, 463-712,
Republic of Korea.
2 Department of Health Science, Pochon CHA University, Sungnam 463-712, Republic
of Korea.
3 Department of Obstetrics and Gynecology, Bundang CHA General Hospital, Pochon
CHA University, Sungnam 463-712, Republic of Korea.
Received September 11, 2005;
accepted after revision December 16, 2005.
Address correspondence to M. D. Kim
(mdkim{at}cha.ac.kr).
Abstract
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MATERIALS AND METHODS. The cases of all patients who underwent UAE for adenomyosis without fibroids between 1998 and 2000 were analyzed. This study was a retrospective review of a prospectively collected database. Of the 66 patients, 54 patients with a follow-up period of 3 years or longer were enrolled in the study. Twelve patients were lost to follow-up. The patients' ages ranged from 29 to 49 years (mean, 40.2 years). The mean follow-up period was 4.9 years (range, 3.5-5.8 years). The primary embolic agent was polyvinyl alcohol particles (250-710 µm). All patients underwent MRI before UAE. Long-term follow-up MRI was performed on 29 patients; 22 of these patients had undergone short-term (3.5 months) follow-up MRI. Uterine volume was calculated with MR images. Symptom status in terms of menorrhagia and dysmenorrhea was scored on a scale of 0-10, 0 being no symptoms and 10 being the baseline, or initial symptoms.
RESULTS. Thirty-one (57.4%) of the 54 women who underwent follow-up had long-term success. Four had immediate treatment failure, and 19 had relapses. Changes in mean menorrhagia and dysmenorrhea scores at long-term follow-up were -5.3 and -5.1, respectively (p < 0.001), representing significant relief of symptoms. The time between UAE and recurrence of symptoms ranged from 4 to 48 months (mean, 17.3 months). Five patients underwent hysterectomy because of symptom recurrence. Mean reduction in volume of the uterus was 26.3% at short-term follow-up and 27.4% at long-term follow-up.
CONCLUSION. We found that UAE is effective in the management of symptomatic adenomyosis and has an acceptable long-term success rate. UAE should be considered a primary treatment method for patients with symptomatic adenomyosis. However, all patients should be given an explanation of the possibility of treatment failure, recurrence, and the need for hysterectomy.
Keywords: adenomyosis • digital subtraction angiography • embolization • interventional radiology • uterine artery
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Of 66 eligible patients, 54 patients with a follow-up period of 3 years or longer were enrolled in the study. Twelve patients were lost to follow-up. The age range was 29-49 years (mean, 40.2 years). The mean follow-up period was 4.9 years (range, 3.5-5.8 years). Symptom status in terms of menorrhagia and dysmenorrhea was scored on a 0-10 scale at short-term and long-term follow-up.
Short-term follow-up consisted of an outpatient visit and MRI 3 months after UAE. Long-term follow-up began with telephone calls to patients who had undergone UAE 3 years or more years before the call. The purpose of the calls was to recommend a follow-up visit to an outpatient clinic, where a questionnaire interview was conducted and MRI was performed. Women who lived far from a clinic underwent a telephone interview only.
A score of 0 was defined as little bleeding or no pain during the menstrual period. A score of 10 was baseline, or initial symptoms of menorrhagia or pain. We asked patients to answer the question, "What is your current symptom score if the score before UAE was 10?" Changes in symptoms scores of menorrhagia and dysmenorrhea determined by subtracting long-term follow-up score from baseline score were analyzed. In terms of bulk-related symptoms at long-term follow-up, a five-category Likert-type scale was used to describe the responses: complete resolution, marked improvement, slight improvement, no change, and worse condition. Treatment failure was defined as unsuccessful embolization or no resolution of symptoms after UAE.
The presence of recurrence was based on an operational definition, considered presence of recurrent symptoms after initial improvement after UAE with a greater than 4 change in symptom score (determined by subtracting short-term follow-up score from long-term follow-up score) or the patient's feeling she had a recurrence regardless of the difference in symptom score. Because the maximum difference in symptom score was 4 in the group of patients without recurrence, we designated a score of 4 the cutoff value. Patient satisfaction with UAE was assessed at long-term follow-up.
MRI Studies
MRI (1.5-T supermagnet, Magnetom Vision, Siemens Medical Solutions) of the
pelvis was performed on all patients before UAE. Long-term (mean, 4.9 ±
0.8 [SD] years) follow-up MRI was performed on 29 patients, 22 of whom had
undergone short-term (mean, 3.3 ± 1.8 months) follow-up MRI. All
patients underwent axial and sagittal fast spin-echo T2-weighted imaging
(TR/effective TE, 3,500/99; matrix size, 225 x 300; field of view, 340
x 340 mm; section thickness, 7 mm) and contrast-enhanced T1-weighted
sagittal imaging. Contrast-enhanced MRI was performed 2 minutes after IV
infusion of 10 mL of gadolinium (gadoterate dimeglumine, Dotarem, Guerbet)
with fast low-angle shot sequences (TR/TE, 117.3/4.1; flip angle, 80°;
matrix size, 140 x 256; section thickness, 5 mm). MRI diagnostic
criteria for adenomyosis were presence of poorly defined low signal intensity
of a mass with or without bright foci on T2-weighted images and greater than
12-mm thickening of the junctional zone
[12,
13].
The pattern of adenomyosis was subdivided into two categories: focal and diffuse. Focal adenomyosis, or adenomyoma, was adenomyosis localized and often presented as a rounded or oval low-signal-intensity mass. Diffuse adenomyosis was defined as showing diffuse widening of the junctional zone. Presence of necrosis was defined as the finding of low signal intensity on T2-weighted images and absence of contrast enhancement on T1-weighted images [9]. The total volume of the uterus was determined by measuring length, height, and width and calculating the volume with the equation for a prolate ellipse: length x width x height x 0.5233 [14].
Angiographic Procedure
The preparation and embolization protocol for our patients were similar to
those previously discussed in the literature
[7]. Coaxial 3-French catheters
(Tracker 18 infusion catheter, Boston Scientific) were advanced distally into
the uterine artery. The primary embolic agent was polyvinyl alcohol (PVA)
particles (Contour, Boston Scientific) mixed with 40 mL of a 1:1
saline-contrast agent mixture. Eleven of 54 patients underwent embolization
with 250- to 355-µm PVA particles. In 21 patients, 250- to 355-µm
particles were used initially and followed by 500- to 710-µm particles. In
the other 22 patients, 355- to 500-µm of PVA particles were used. We used
250- to 355-µm PVA particles with or without 500- to 710-µm particles in
the first 32 patients (1998-1999) but switched to 355- to 500-µm particles
in 2000, hoping that there would be less pain. The amounts of PVA used for
embolization were as follows: The 250- to 355-µm group received a mean of
1.7 mL (vials) (range, 1.5-2.0 mL); the group receiving the combination of
250- to 355-µm and 500- to 710-µm particles received a mean of 2.2 mL
(range, 2-2.8 mL); and the 355- to 500-µm group received a mean of 2.2 mL
(range, 2-2.5 mL).
Secondary supplemental embolization with gelatin sponge pledgets was performed in all cases. Embolization was performed until there was complete cessation of blood flow in the ascending uterine artery with residual flow in the lower uterine segment.
Statistical Analysis
The paired Student's t test, one-sample proportion test, and
one-sample test for binomial proportion were used to determine the long-term
follow-up effects of UAE. One-way analysis of variance and the chi-square test
were used to determine the effects of UAE on the basis of PVA size. The
two-sample t test and the chi-square test were used to compare
recurrence and no-recurrence groups on the basis of age, size of PVA
particles, baseline uterine volume, focal versus diffuse type of adenomyosis,
and presence of necrosis in the adenomyotic area on short-term follow-up MRI
after UAE. Differences were considered statistically significant at p
< 0.05.
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In terms of bulk-related symptoms in 23 patients before UAE, complete resolution was achieved in eight (34.8%) of the patients, marked resolution in 11 (47.8%), and no change in four (17.4%). Two patients (ages, 41 and 44 years) had amenorrhea immediately after UAE. Menopause occurred in nine patients (mean age, 48.3 years; range, 44-51 years) during follow-up. Mean time to menopause after UAE was 2.9 years (range, 1-4 years).
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MR images at long-term follow-up revealed three common patterns: persistent atrophy and necrosis of the uterus in 10 patients (Figs. 1A, 1B, 1C, and 1D), marked enlargement of the uterus (> 10% increase in uterine volume compared with uterine volume at short-term follow-up) with or without aggravated adenomyosis in seven patients, and necrotic areas detected at short-term follow-up MRI after UAE no longer visualized and replaced by viable tissue in 10 (76.9%) of 13 patients (Figs. 2A, 2B, 2C, 2D, and 2E). Short-term follow-up showed complete necrosis in 65.2% of cases of the focal type of adenomyosis and partial necrosis in 68.8% of cases of diffuse adenomyosis (none of the patients had complete necrosis of diffuse adenomyosis).
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Three of the five patients who achieved uneventful intrauterine pregnancies carried to term; two underwent elective abortion because of unwanted pregnancy. Two infants were delivered vaginally, and one was delivered by elective cesarean section. The indication for the elective cesarean delivery was previous cesarean section. The average weight of neonates was 3.2 kg (range, 3.1-3.4 kg). Deliveries were uneventful, and Apgar scores of 8 and 9 (1 and 5 minutes, respectively) were recorded for the two infants. There was no evidence of uteroplacental vascular insufficiency or abnormal uterine contraction during labor or post partum.
With regard to patient satisfaction with the procedure and its outcome, 35 (70%) of 50 patients were satisfied at long-term follow-up (64.8% when failures are included). This satisfaction rate was relatively high in light of the recurrence rate of 38%.
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Contrast-enhanced MRI is currently considered the most accurate imaging technique for the diagnosis of adenomyosis [17-19]. On T2-weighted MR images, bright foci are seen in areas of abnormally low signal intensity within the myometrium in approximately 50% of patients with adenomyosis. These foci correspond to islands of heterotopic endometrial tissue, cystic dilatation of heterotopic glands, or hemorrhagic foci. Junctional zone thickening and low signal intensity of myometrial masses with ill-defined margins are other characteristic MRI findings.
Although minimally invasive therapies have been used to manage adenomyosis, hysterectomy is considered the only procedure that definitively cures the disease. Hormonal treatments have been used to decrease junctional zone thickness and provide symptomatic relief. The effects are temporary, however, or treatment is unsuccessful in the acute setting, or drug side effects occur, and symptoms tend to recur within 1 year of treatment cessation [15, 20]. Reports of UAE for adenomyosis have described mainly short-term results. Some authors [10, 11] suggested that UAE resulted in treatment failures; others [8, 9] advocated use of UAE to manage symptomatic adenomyosis.
In view of the short-term results, Siskin et al. [8] described significant symptom resolution in 12 of 13 patients with adenomyosis with or without concomitant fibroids. In other reports, including a study by Jha et al. [9] and our previous reports of short-term results [7], most patients with pure or dominant adenomyosis had a positive outcome after UAE with respect to clinical symptoms and junctional zone thickness.
According to the results of a study by Pelage [21] et al., only five (56%) of nine patients who underwent UAE for pure adenomyosis and clinical follow-up for longer than 24 months had complete resolution of abnormal bleeding. The authors considered the midterm results of UAE for adenomyosis performed according to their protocol disappointing and concluded that the indications for embolization were limited. We have no exact explanation for this discrepancy compared with our findings. Aside from small sample sizes, one reason for the difference may be the embolic agent. Pelage and colleagues used trisacryl microspheres with a diameter of 500-900 µm, whereas we used PVA particles measuring 250-355 µm (alone or in combination with 500- to 710-µm particles) or 355-500 µm. Another explanation may be the end point of embolization. Pelage et al. considered the end point "embo light," in which flow to the uterus was maintained at the end of embolization.
We embolized the uterine arteries to near stasis with PVA particles and then completely occluded flow with gelatin sponge pledgets in all cases. Our results suggest that UAE with PVA particles and secondary embolization until complete cessation of flow may be better for management of symptomatic adenomyosis. We believe that secondary embolization with an absorbable gelatin sponge (Gelfoam, Upjohn) can help to prevent recanalization of the uterine arteries and ensure enough time for ischemia of adenomyosis. Some reports [22-24] describe recanalization of vessels embolized with PVA alone. Worthington-Kirsch et al. [25] reported that 17 of 18 uterine arteries remained occluded when embolization with PVA was supplemented with gelatin sponges. Because the only definitive management of symptomatic adenomyosis is hysterectomy, we believe our findings show it is acceptable to attempt UAE before resorting to hysterectomy.
With respect to PVA size, our results show that use of the combination of 250- to 355-µm and 500- to 710-µm PVA particles gave a better embolization effect than use of 250- to 355-µm or 355- to 500-µm particles alone. Presence of necrosis at short-term follow-up MRI correlated significantly with absence of recurrence at long-term follow-up. The combination of 250- to 355-µm and 500- to 710-µm PVA particles theoretically should not outperform 250- to 355-µm particles alone in embolization effect. The observations may be flawed because of small sample size or the smaller amount of PVA used for embolization in the 250- to 355-µm group (mean, 1.7 mL) than in the combination group (mean, 2.2 mL).
Angiography shows the vascular structure of adenomyosis is quite different from that of uterine fibroids. The arteries of adenomyosis are not as large as those of fibroids. Our results support the hypothesis that more vigorous embolization seems to be needed for adenomyosis than for fibroids: use of a smaller size of PVA, complete embolization until cessation of uterine flow (no flow for 10 cardiac beats), and secondary embolization with gelatin sponges.
In terms of our embolization technique, two (3.7%) of the patients had amenorrhea immediately after UAE. The most commonly reported rates of amenorrhea after UAE range between 2% and 7% [10, 26-29]. Long-term follow-up showed that nine patients had reached menopause. Their menstrual periods might have continued if they had not undergone UAE. In general, the mean age at natural menopause, which depends on many factors such as race and smoking, is 46.7-51.3 years [30-32]. The mean age of the nine menopausal patients in our study was 48.3 years. All nine of these patients were satisfied with UAE, and the resolution of symptoms had persisted until menopause, so these findings were considered a favorable long-term outcome. We do not believe UAE played an important role in menopause in our study.
An interesting observation in our study was the relatively high satisfaction rate of 70% despite a recurrence rate of 38%. Seven of the 19 patients with recurrences were satisfied, giving the following reasons: less severe symptoms, pregnancy, long symptom-free period, and delay of hysterectomy.
With regard to MR images, we frequently found that necrotic areas visualized at short-term follow-up were replaced by ill-defined masses of low signal intensity on T2-weighted images. We believe these areas might have been viable adenomyotic tissue, but there was no pathologic correlation for proof.
A few limitations of this study must be acknowledged. First, use of the symptom score 10 as a baseline before UAE might have led to bias. It would have been theoretically ideal to compare absolute symptom scores before UAE with those after UAE, but it is not easy for patients to define the absolute value of symptoms, especially menorrhagia, before UAE. We had to compare relative symptom scores because they are more intuitive. Second, we did not have 100% follow-up because some of the patients moved to unknown addresses. Another limitation of this study was the small sample size. We recognize that the results must be validated with ongoing research.
We found that UAE is an effective treatment for symptomatic adenomyosis with a reasonable long-term success rate. However, given a more than 40% rate of treatment failure and recurrence, all patients should be counseled before the procedure about the possibility of treatment failure and need for hysterectomy. We believe UAE can be used as the primary treatment and as an alternative to hysterectomy in this setting, despite the possibility of symptom recurrence. A low complication rate, short hospital stay, and rapid recovery time are other favorable features of UAE. Further studies are necessary to confirm our findings.
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