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1 Departments of Magnetic Resonance Imaging and Academic Obstetrics and
Gynaecology, Interventional MR Unit, St Mary's Hospital London and Imperial
College School of Medicine, Praed St., London W2 1NY, England.
2 Departments of Obstetrics and Gynaecology and Reproductive Biology and
Radiology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA
02115.
3 Department of Radiology and Obstetrics and Gynaecology, Sheba Medical Centre,
Tel-Hashomer 91120, Israel.
4 Department of Radiology, Johns Hopkins School of Medicine, Baltimore, MD
21287.
5 Department of Radiology and Obstetrics and Gynaecology, Mayo Clinic,
Rochester, MN 55905.
6 Department of Radiology, Charité Medical Centre and Humboldt
University, Virchow Clinic Campus, Berlin D-13353, Germany.
7 Department of Radiology, Hadassah Medical Centre, Jerusalem 52621,
Israel.
Received February 23, 2004;
accepted after revision May 15, 2004.
Address correspondence to W. Gedroyc
(w.gedroyc{at}imperial.ac.uk).
Abstract
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MATERIALS AND METHODS. Patients presenting with symptomatic uterine fibroids who attained a minimal symptom severity score and who would otherwise have been offered a hysterectomy were recruited. Thermal lesions were created within target fibroids using an MRI-guided focused ultrasound therapy system. The developing lesion was monitored using real-time MR thermometry, which was used to assess treatment outcome in real time to change treatment parameters and achieve the desired outcome.
Fibroid volume, fibroid symptoms, and quality-of-life scores were measured before treatment and 6 months after treatment. Adverse events were actively monitored and recorded.
RESULTS. In this study, 79.3% of women who had been treated reported a significant improvement in their uterine fibroid symptoms on follow-up health-related quality-of-life questionnaires, which supports our hypothesis. The mean reduction in fibroid volume at 6 months was 13.5%, but nonenhancing volume (mean, 51 cm3) remained within the treated fibroid at 6 months.
CONCLUSION. This early description of MRI-guided focused ultrasound therapy treatment of fibroids includes follow-up data and shows that, although the volume reduction is moderate, it correlates with treatment volume and the symptomatic response to this treatment is encouraging.
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Ultrasound energy propagates harmlessly through tissue with small amounts of energy being absorbed; this energy is deposited as heat but is dissipated by the cooling effects of perfusion and conduction. If, however, the ultrasound beam carries a high level of energy and is brought to a tight focus, energy carried by the beam is rapidly converted into heat and a rise in temperature is observed [2]. If the temperature at the target spot can be raised to more than 55°C, protein denaturation occurs, resulting in cell death and the creation of a cigar-shaped lesion of coagulative necrosis in the direction of the ultrasound beam [3]. The tissue in the path of the ultrasound beam but away from the focus is warmed, but not to lethal temperatures, avoiding tissue damage except at the focus.
The possibility that focused ultrasound therapy might be developed as a result of controlling these heating phenomena was introduced by Lynn et al. [4] in the middle of the last century. Their work was closely followed by the first descriptions of focused ultrasound therapy as a noninvasive surgical technique in the brain [5]. These early uses of focused ultrasound therapy for Parkinson's disease were quickly super-seded by drug therapies, and further development of this technology was delayed until a resurgence in the 1990s [6]. In recent years, focused ultrasound therapy has been used in urology for the treatment of benign prostatic hyperplasia [7, 8] and in the management of cancer of the prostate [9, 10]. There has been an increase in interest in the use of focused ultrasound therapy in the central nervous system [11], and reports of soft-tissue tumors of the liver and kidney being treated with focused ultrasound therapy are encouraging [12].
The use of focused ultrasound therapy has been hampered by the difficulty in precise targeting of the ultrasound beam and in receiving feedback regarding the thermal damage created. Ultrasound guidance has been used to target the ultrasound energy, but its thermal sensitivity is limited and therefore real-time thermometry is problematic.
MRI guidance of focused ultrasound therapy has been explored during the past decade [13], and it has several attractive attributes. The excellent soft-tissue resolution afforded by MRI enables accurate planning of the tissue to be targeted. MRI parameters have an intrinsic sensitivity to temperature change and therefore can be adapted to provide accurate, near real-time thermometry, and thermal damage created by focused ultrasound therapy can be assessed immediately using MRI.
The shift in proton resonant frequency with a rise in temperature can be detected using phase imaging [14]. If sequential phase-shift MR images obtained during an ultrasound sonication are compared with an image obtained immediately before that sonication, the changes in those images can be calibrated to create a real-time thermal map of the increasing temperature at and close to the target [15]. The MRI-guided focused ultrasound therapy system used in this study (ExAblate 2000, InSightec) integrates fully with a 1.5-T MRI system (Signa, GE Healthcare) to enable focused ultrasound therapy to be planned directly with MR images and to give real-time MR thermometry feedback of each sonication. This system, or its earlier prototypes [16], has been used to create lesions in several different body tissues [17–19].
MRI-guided focused ultrasound therapy for fibroids has been shown to be a safe and feasible treatment for uterine fibroids [20]. This article describes the details of MRI-guided focused ultrasound therapy for fibroids and presents the early results of this procedure in addition to posttreatment changes in fibroid volumes.
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This multicenter phase III clinical trial study was performed according to principles of good clinical practice as defined by the Declaration of Helsinki. The participating sites were situated in Europe [2], the United States [3], and Israel [2]. All sites had local approval from their ethics committees or institutional review boards. All patients gave fully informed consent.
Suitable subjects were asked to complete the first eight questions of a Uterine Fibroid Symptoms and Quality of Life Questionnaire [21]. Responses are scored from 1 (not distressed) to 5 (distressed a great deal) and provide a screening tool for fibroid symptoms with possible results from 8 to 40. A minimum score of 21 points was required for inclusion in the study. Women who scored more than 21 on the screening questionnaire and who were enrolled in the study went on to complete the full Uterine Fibroid Symptoms and Quality of Life Questionnaire form consisting of 37 questions.
The anatomic suitability for MRI-guided focused ultrasound therapy was assessed using either MRI or sonography. A clear pathway from the anterior abdominal wall to the fibroid without passing through the bladder or the bowel was required by the protocol. Fibroids greater than 10 cm in diameter or women with uteri greater than a 24-week pregnancy equivalent were excluded from this early study.
In total, 109 patients were treated at seven sites. Fifty-two patients were treated within the United States, and 57 patients were treated in Europe and Israel. The mean age was 44.8 years (range, 30–58 years; SD ± 4.9). The proportion of black (African American, African, or African Caribbean) patients was 11%, and the mean body mass index was 25.8 (range, 18.6–3.9; SD ± 5.2).
Of the fibroids treated, 22% were submucosal, 57% were intramural, and 21% were subserosal. Those fibroids that were intramural required disruption to the myometrium in conventional surgery.
Before the treatment, each patient was asked to shave her anterior abdomen from the umbilicus to the level of the upper margin of the symphysis pubis. It has been noted in previous studies [20] that the presence of hairs in the sonication pathway was associated with the formation of small air bubbles that absorb the ultrasound energy and potentially cause heating at the skin surface and even skin burns.
An additional pregnancy test was performed on the day of treatment. All patients were counseled regarding the lack of safety data for pregnancy after MRI-guided focused ultrasound therapy and, in particular, the possible theoretic risk of uterine rupture suggested by the experience of women who became pregnant after undergoing laparoscopic laser myolysis for fibroids [22, 23]. A urinary catheter was inserted before the patients were positioned on the ExAblate 2000 focused ultrasound therapy system. The patients were placed in the prone position on the system with the fibroid placed above the transducer (Fig. 1). To ensure that an acoustic pathway was maintained, the transducer was positioned on the MRI table in a sealed tank of degassed water. The acoustic pathway then passed from the transducer through a thin membrane into a gel pad on which the patient lay.
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Once positioned, the patient is placed into the MRI scanner, and the patient's position and the sonication pathway is checked using MR images (TR/TE, 3,600/102; matrix, 256 x 224; echo-train length, 16; field of view, 36 cm; number of excitations, 2; slice thickness, 4 mm; slice spacing, 1 mm; scanning time, approximately 2 min 2 sec) (Fig. 2). The patient's pelvis is imaged using T2-weighted fast spin-echo images in the coronal, axial, and sagittal planes. These images are then transferred to the workstation of the focused ultrasound therapy system in which the volume to be ablated is defined by the physician. The system plots the individual sonications and shows the pathway that each sonication will require. These pathways are carefully checked to ensure that they do not pass through any structures that ought to be avoided—such as the small bowel—that can fall in front of the uterus. The far beam also is checked, because some energy deposition remains after the beam has passed through the fibroid, and structures such as large neurovascular bundles should be avoided. The transducer can be tilted in all directions by up to ± 20° to find a suitable pathway. Once correct positioning has been achieved, the target volume defined, and the treatment planned, verification sonications are performed. These sonications are subtherapeutic at low power, typically 10–70 W for 10–20 sec at 1.0 MHz. This low-power sonication is monitored by a thermal map [14] created in the coronal plane and repeated with a thermal map in the sagittal or axial plane to ensure that both the lateral and longitudinal targeting are as planned. Any errors are corrected before repeating the verification at a therapeutic power. Once the operators are satisfied that the targeting is accurate, they proceed to the treatment cycle.
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The treatment itself consists of consecutive sonications producing thermal lesions within the previously defined target area to produce a single large area of ablated tissue. Each sonication is monitored using phase subtraction fast gradient-echo proton resonance frequency-shift-dependent techniques [14].
Typical parameters for these scans were TR/RE, 27/13 msec; flip angle, 30°; bandwidth, 5.68 kHz; matrix, 256 x 128; field of view, 28 cm2; and slice thickness, 3/5 mm.
The focused ultrasound therapy system enslaves the MRI system to ensure that these sequences are timed and positioned to coincide with the deposition of ultrasound energy. A baseline image is created immediately before the sonication, and subsequent images are created every few seconds during a single heating and early cooling phase (Fig. 3). The images are compared and presented as a thermal map either as simple subtraction images or colorized with a threshold temperature. A graph of the temperature rise over time also is created to enable actual temperatures to be assessed at any point (Fig. 4). The time and temperature information for each voxel also is used to calculate the thermal dose, and those voxels with the dose above a threshold value of 240 equivalent min at 438°C are indicated on the images [15]. Thus, for each sonication a complete picture of the tissue effect is created. Although a typical power of 140 W for 20 sec and 1.0 MHz and fibroids with an average depth of 7 cm will lead to a rise in temperature to about 60°C in a fibroid, this rise is extremely variable. It is this extreme variation in response, both between and within fibroids, that makes real-time thermal mapping so vital to the balance of safety and efficacy in MRI-guided focused ultrasound therapy ablation of fibroids.
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Most sonication parameters can be changed in response to the thermal maps being created. The power applied can be increased or decreased. Clearly, greater power will lead to the generation of a higher temperature. The aim is to reach a threshold temperature without approaching higher temperatures at which control of the thermal effect may be compromised. The time for which the energy is applied can be changed. Higher power for a shorter time may compensate for the cooling effect of perfusion in a highly vascular fibroid. The cooling time after each sonication can be assessed by extending the thermal map into the cooling period. The default cooling period of 90 sec may be altered if the thermal map suggests that a return to baseline temperature is achieved in a shorter time or indeed if it requires more time.
The spot size can be altered in both diameter and length so that the target volume can be ablated with as few sonications as possible while maintaining accuracy and control.
The sonication frequency also can be altered. Increasing the transducer frequency will result in more energy being absorbed in the near field thus decreasing the chance of heat buildup in structures such as bone and nerves in the far field; similarly, decreasing the transducer frequency will reduce the near-field absorption, limiting the chance of skin-heating, decreasing aberration caused by the beam passing through irregular structures such as the muscles of the anterior abdominal wall, and increasing the depth at which treatment is possible.
In our study, up to four fibroids were treated in any one patient. A minimum margin of 1.5 cm from the edge of the ablated area to the edge of the uterus (serosal or mucosal surfaces) was stipulated.
All patients remained conscious during the treatment and were given IV analgesia and conscious sedation as required. They remained in constant verbal communication with the operators and were asked to report any pain or discomfort. The patients held an emergency stop button at all times, which enabled them to halt further sonication.
Once all the sonications in a target volume had been completed, additional fibroid treatment could be planned, up to a maximum treatment time of 3 hr or a maximum ablated volume of 100 cm3 per fibroid and a total of 150 cm3 per patient with multiple treated fibroids. This maximum treatment volume was a stipulation of the regulatory authorities and may have led to suboptimal treatment in patients with large or multiple fibroids.
Immediately after completion of the treatment, an MRI gadolinium-based contrast agent (Omniscan [gadodiamide], Nycomed Amersham or equivalent) was given and the effectiveness of the treatment was assessed by measuring the nonperfused area that had been created in the target fibroid. We used the following scanning parameters: T1-weighted fast-spoiled (radiofrequency-spoiled) gradient-echo, TR/TE, 200/1.2; flip angle, 75°; matrix, 256 x 128; zero interpolated to 5122; number of excitations, 2; field of view, 36; slice thickness, 4 mm; slice spacing, 1 mm; scan time, approximately 52 sec for 17 slices (Fig. 5A, 5B). The MR images were sent to a central core laboratory where the fibroid volume and the nonenhancing volume were measured using a standard method as described below. The fibroid was identified on each slice, and the area of the fibroid on each image was estimated by drawing around that area on the workstation and using the workstation software to calculate the defined area. The areas of fibroid from each slice then were summated and multiplied by the sum of the slice thickness and the interval between slices to calculate the volume. This was repeated for the volume that did not enhance after contrast. This volume is known to correspond to the thermal lesion [20].
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Before treatment, the patients were assessed for symptoms and for the impact that the fibroids had made on their quality of life using the Uterine Fibroid Symptoms and Quality of Life questionnaire. This is a disease-specific questionnaire that was developed to assess the efficacy of fibroid therapies [21]. This questionnaire was used before treatment and at 3 and 6 months after MRI-guided focused ultrasound therapy. The primary end-point hypothesis for the study was defined as an improvement in the Uterine Fibroid Symptoms and Quality of Life Questionnaire of 10 points for at least 50% of patients.
Thorough clinical examinations of the patients were performed immediately after treatment and 1 week, 1 month, 3 months, and 6 months later. A structured interview was used to ensure that common or expected adverse events were identified and recorded. Serious adverse events as defined by the protocol (see Table 1) were reported to the local ethics committee or institutional review board and to the regulatory authority (the U.S. Food and Drug Administration, the Medical Devices Agency in the United Kingdom, and the National Helsinki Committee in Israel). Adverse events were classified according to whether they were device related, disease related, or incidental.
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Of the fibroids treated, 22% were submucosal, 57% were intramural, and 21% were subserosal. Intramural fibroids definitively require disruption of the myometrium in conventional surgery.
The mean fibroid volume in patients in whom only a single fibroid was treated (n = 60) was 346 cm3, ± 245 cm 3. In patients with multiple fibroids being treated (n = 32), the mean fibroid volume was correspondingly less at 294 cm3, ± 188 cm 3. The region of treatment as defined by the operators before sonication was 39 cm3 (± 27 cm 3) for single fibroids and a similar 38 cm3 (± 24 cm 3) for multiple fibroid treatments. The actual volume that received a thermal dose as measured using MR thermometry was 36 cm3 (± 18 cm 3)—around 10% of the fibroid volume, and 32 cm3 (± 23 cm 3)—about 11% of the fibroid volume, for single and multiple treatments, respectively.
The posttreatment contrast-enhanced images showed that the volume of the fibroid that was nonperfused was greater than the thermal dose volume at 86 cm3 (± 82 cm 3) for patients with single fibroids and 85 cm3 (± 88 cm 3) for those who had multiple fibroids treated; 25% and 29% of the fibroids volume, respectively.
The mean time that the patients were in the MR scanner was 202 min (range, 90–370 min; ± 56). This time is variable because much of the time is taken with positioning the patient correctly to align the sonication pathway optimally with the transducer. It was noted early in the study that the likelihood of the patient complaining about leg or buttock pain increased if the sacrum was in the direct far field of the sonication pathway close to the target area. This was presumed to be related to thermal nerve stimulation in the far field where a nerve passes in close proximity to the sacrum (3–5 mm) and patients were positioned to maximize the distance between the thermal spot and the pelvis in the far field. This usually can be achieved by positioning the patient with the fibroid farther back so the transducer can be angled caudad (Fig. 2).
The pain and discomfort as reported by patients before, during, and immediately after treatment were assessed on a 4-point scale, with 0 = none, 1 = mild, 2 = moderate, and 3 = severe. The pain and discomfort scores are outlined in Table 1. Although 16% of patients complained that the pain was severe during the procedure, only 1% and 7% stated that they were in severe or moderate pain, respectively, when questioned immediately after the treatment.
Nine serious adverse events were reported; of these, only one was thought definitely to be device related. Five of the patients had continued heavy menses in the weeks after the treatment, requiring blood transfusions. These were thought to be related to the underlying cause (i.e., fibroids) rather than to the treatment. Two of these patients withdrew from the study to undergo definitive treatment in the form of hysterectomy. One patient reported pain and bleeding after the treatment. These symptoms were consistent with the patient's symptoms before the treatment and were thought to reflect a treatment failure rather than a device-related adverse event. This patient underwent uterine artery embolization. An additional patient was asked to remain in the hospital overnight because of nausea after the treatment. This was a treatment-related event and represents the only early posttreatment admission but probably was related to the opioid analgesia used rather than the MRI-guided focused ultrasound therapy itself. This patient recovered overnight and was discharged the next day.
Two patients reported serious adverse events that were not thought to be related to the treatment in any way. One had a preexisting brain tumor that progressed during the period of follow-up. The brain tumor was not thought to be related to the treatment and, indeed, the patient had excellent symptom relief. The other patient required admission with a urinary tract infection some 14 weeks after the treatment. She made a full recovery with antibiotic therapy, and it was thought that the temporal relationship between the treatment and the event made causation exceedingly unlikely.
One patient complained of leg and buttock pain immediately after the treatment. Examination of the MR images showed that the sciatic nerve was in the far field of the sonication pathway. Detailed MR neurography and electromyography studies, however, failed to show any intrinsic nerve damage. The patient subsequently made a complete recovery by the follow-up visit using only conservative measures. The patient also had excellent symptomatic relief from fibroid-related symptoms and had made a complete recovery by the final follow-up visit. This case led to a change in operator practice, and 4 cm is now considered the minimum distance between the spot and any major nerve bundles that are in close proximity to a bone surface. The other reported adverse events were minor and transitory.
At 6-month follow-up, the mean fibroid volume was reduced by 13.5%, ± 32. Although the change in fibroid volume is modest, the average relative treatment volume was approximately 0% and the average nonperfused volume at the end of the treatment was approximately 25%, which should have an impact on the modest shrinkage. In addition, a mean non-perfused volume of 51.2 cm3 (± 62.2 cm 3) exists on contrast-enhanced MR images at 6-month follow-up. This may represent future shrinkage and certainly represents nonviable fibroid tissue.
Clinical follow-up shows that 79.3% of patients achieved a greater than 10-point reduction in the Uterine Fibroid Symptoms and Quality of Life Questionnaire score (n = 82, p < 0.0001), thereby proving the primary endpoint hypothesis to be correct. The mean reduction in the symptom severity score on Uterine Fibroid Symptoms and Quality of Life Questionnaire was in fact 27.3 points (p < 0.0.0001; range, 18.75–-81.25 points), and although most of this improvement occurs in the first 3 months after treatment (24.1 points), improvement continues between 3 and 6 months. The Uterine Fibroid Symptoms and Quality of Life Questionnaire can be broken down into symptoms caused by mass effect—where improvement is 32.8 points (63.9/100–31.2/100)—or bleeding symptoms—in which improvement is reported to be 32.8 points (60.1/100–25.3/100).
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Thermoablative treatments for uterine fibroids initially were developed using laser energy delivered via the laparoscopic approach [26]. This resulted in significant reduction in fibroid size and resolution of symptoms but was associated with significant side effects [27, 28]. Many of these side effects seem to have been negated by using an MRI-guided technique for laser ablation with MR thermometry giving real-time feedback to control the thermal lesion created [29]. Despite the low incidence of adverse events, MRI-guided laser ablation of fibroids appears to remain an effective therapy for the treatment of symptomatic uterine fibroids [30].
To our knowledge, we have presented the first short-term follow-up study using MRI-guided focused ultrasound therapy for uterine fibroids. This article outlines the radiologic parameters involved in this new treatment technique, and we have discussed the radiologic appearances of the uterus immediately after and 6 months after this treatment. Our study shows that, despite only a small change in leiomyomata volume, MRI-guided focused ultrasound therapy results in a marked symptomatic improvement in most patients at 6-month follow-up. This improvement is equally marked for pressure symptoms and menstrual bleeding symptoms.
There seemed to be greater improvement reported in the Uterine Fibroid Symptoms and Quality of Life Questionnaire by patients who had a greater proportion of the fibroid treated. The average improvement in the scores was 25.8 at 6 months in those patients in which the nonperfused volume on contrast-enhanced MR images obtained immediately after treatment represented less than 30% of the fibroid volume compared with an improvement of 31.7 in patients who had more than 30% of the fibroid treated. The volume of the fibroid treated was limited by safety margins imposed by the regulatory authorities. These restrictions now have been lifted, and the challenge remains to increase the proportion of the fibroid that is thermally ablated while avoiding thermal damage outside the fibroid (i.e., damage to the myometrium, endometrium, or serosal surface). We believe that the real-time thermal map, which is integral to the performance of focused ultrasound therapy using the technique described, will allow this challenge to be met.
Analysis of the contrast-enhanced images at 6 months reveals that in many cases the volume of the fibroid that remains nonenhancing is significant and therefore is not perfused. The mean nonperfused volume on the 6-month contrast-enhanced scans was 51.2 cm3 (± 62.2 cm 3). This nonperfused area may represent an area of burn that has yet to resolve. If this is the case, it is reasonable to expect further shrinkage beyond the 6-month follow-up reported here. This is the case with MRI-guided laser ablation of fibroids—an analogous technique also resulting in thermal damage [30]. Confirmation of this hypothesis will result when longer follow-up is available. If the nonperfused volume is not an unresolved burn, it is likely to be collagen deposits formed as a result of the burn. If this is the case, it may be that the improvement in fibroid symptoms is not, in fact, volume dependent but caused by the destruction of the leiomyoma cells and the breakdown of local secretory pathways. The mechanisms by which fibroid symptoms are mediated are not yet fully explained.
The lesion produced is shown as the non-enhancing volume in the immediate posttreatment contrast-enhanced MR images and is larger that the volume expected from thermal damage alone. The mechanism by which this occurs has not been elucidated. It may be that the temperature required for lethal damage in fibroid tissue is lower than the 55°C threshold that we believed was required, but this seems unlikely because the expansion in the lesion occurs laterally as well as in the direction of the sonication pathway. This expansion may be a result of the passage of mediators of apoptosis from the lethally damaged cells to their neighbors [20], as previously shown in gene transfection experiments on leiomyomas [31]. Other mechanisms may be responsible. These may include the thermal occlusion of internal fibroid blood vessels leading to areas of infarction, as has been shown in animal models [32]. The striking absence of pain after the procedure, in stark contrast to uterine artery embolization, suggests that pain is not a major component in the tissue destruction caused by MRI-guided focused ultrasound therapy. Local edema produced as a result of the thermal damage may cause a pressure rise within the fibroid. Although fibroids are not strictly encapsulated, they tend to have well-demarcated edges effectively producing the same effect as a capsule so that edema within the fibroid would cause a rise in pressure that may be sufficient to explain the local extension of the lethal volume. Another possibility is that the delay between sonications (approximately 60–90 sec) was not sufficient to avoid thermal buildup in the ultrasound beam path over the course of multiple sonications [33]. Because the MR thermometry only measured temperature changes and a new baseline image was acquired before each sonication, this slow buildup of heat would not be detected during the treatment. However, this effect could not be the full explanation because cases existed in which regions were nonenhancing that were distant from the targeted zone and clearly unheated. Further studies will be needed fully to explain this phenomenon, which may of course have a multifactorial explanation. It is clear that the expansion of the lesion is confined in all cases to the treated fibroid with no examples of damage to the myometrium or endometrium beyond.
We believe that MRI-guided focused ultrasound therapy provides a potentially important new noninvasive and effective treatment for uterine fibroids, particularly in women who wish to avoid invasive or painful therapies. In particular, the total lack of invasiveness of MRI-guided focused ultrasound therapy compared with all other fibroid procedures and the fact that the procedure is performed as an out-patient procedure make it particularly attractive for patients.
We also believe that MRI-guided focused ultrasound therapy for fibroids may prove to be an important model for the spread of this noninvasive, precise, controlled, tissue-destructive technology to other disorders in a variety of organs.
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