Ultrasound-guided high-intensity focused ultrasound ablation for adenomyosis: the clinical experience of a single center
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1 Ultrasound-guided high-intensity focused ultrasound ablation for adenomyosis: the clinical experience of a single center Min Zhou, M.D., Ph.D., a Jin-Yun Chen, M.D., Ph.D., b Liang-Dan Tang, M.D., Ph.D., a Wen-Zhi Chen, M.D., b and Zhi-Biao Wang, M.D., Ph.D. b a Department of Obstetrics and Gynecology, First Affiliated Hospital, and b Institute of Ultrasound Engineering in Medicine, Chongqing Medical University, Chongqing, People s Republic of China Objective: To assess the midterm outcomes after ultrasound-guided high-intensity focused ultrasound (HIFU) ablation in treatment of patients with symptomatic adenomyosis. Design: A prospective clinical trial. Setting: University teaching hospital. Patient(s): Seventy-eight patients with symptomatic adenomyosis. Intervention(s): A single treatment session of ultrasound-guided HIFU ablation for adenomyosis. Main Outcome Measure(s): Dysmenorrhea and menorrhagia scores and the incidence of complications. Result(s): In all 78 patients, 84.6% tolerated the treatment procedure well with pain scores between 0 and 4. Treatment was terminated in only one patient because of increased blood pressure persistently. Sixty-nine patients have finished at least an 18-month follow-up; the mean follow-up time was 24.2 months. Nonperfused regions in lesions were observed in 60 (87.0%) patients on the enhanced magnetic resonance imaging scans. Scores for menorrhea and dysmenorrhea decreased. Clinical effectiveness of the treatment was observed in 62 women (89.9%) with varying degrees of symptomatic relief of dysmenorrhea. Eight patients had relapses. Twenty-two patients (28.6%) had 27 complications. Of these, four had two or more complications. Twenty-three events (85.1%) did not need medical intervention (Society of Interventional Radiology class A). No serious complications including death or major permanent injuries were observed. Conclusion(s): Ultrasound-guided HIFU ablation may be a safe and effective noninvasive alternative in the treatment of symptomatic adenomyosis. (Fertil Steril Ò 2011;95: Ó2011 by American Society for Reproductive Medicine.) Key Words: High-intensity focused ultrasound, uterus, adenomyosis, ultrasound ablation, thermal ablation Received January 16, 2010; revised September 1, 2010; accepted October 13, 2010; published online November 10, M.Z. has nothing to disclose. J-Y.C. has nothing to disclose. L-D.T. has nothing to disclose. W-Z.C. has nothing to disclose. Z-B.W. has nothing to disclose. Supported by grants from the National Natural Science Foundation of China (no and ). Reprint requests: Liang-Dan Tang, M.D., Ph.D., Department of Obstetrics and Gynecology, First Affiliated Hospital, Chongqing Medical University, 1 Yi Xue Yuan Road, Yu Zhong District, Chongqing , People s Republic of China ( ldtang2002@yahoo.com.cn). Adenomyosis is a common gynecologic disorder that affects women during their reproductive lives. A junctional zone thicker than 12 mm is considered the golden criterion for establishing the presence of adenomyosis (1). The usual treatment for women with symptoms is hysterectomy, which is definitive and radical (2). Conservative surgeries such as local excision of adenomyosis lesions are difficult because of the ill-defined boundary between the endometrium and myometrium. Hysteroscopic endometrial resection is a minimally invasive option that can be used in a minority of patients who are seen with minor symptoms of menorrhagia (3). Uterine artery embolization has gained acceptance as an effective alternative to surgical treatment with control of symptoms (4 6). The levonorgestrelreleasing intrauterine system appears to be an effective method in alleviating dysmenorrhea associated with adenomyosis (7). Conservative medical management including danazol, GnRH analogues, nonsteroidal anti-inflammatory drugs, and oral contraceptives can provide temporary symptomatic relief (8). As a result, a new noninvasive method for the treatment of patients with adenomyosis would be of great value. High-intensity focused ultrasound (HIFU) is a powerful tissueablation technique that has been used to treat a variety of tumors of the prostate, breast, and liver, with use of either ultrasound (US) or magnetic resonance imaging (MRI) guidance (9 12). It is a noninvasive thermoablative technique that uses an external US energy source to induce a thermal ablation of tissue deep under the intact skin based on its ability to concentrate US waves precisely (12). High-intensity focused US has been used for the treatment of uterine fibroids, showing a symptom reduction in women with symptomatic uterine leiomyomas and an excellent safety profile (13 15), with obvious necrosis histopathologically (16). Similarly, HIFU has been used recently to treat patients with symptomatic adenomyosis. High-intensity focused US induced thermal ablation also results in typical characteristics of coagulative necrosis, and the margin between the treated and untreated regions is well defined (17). Although several publications (18 21) indicate that focused US ablation is safe and effective in the treatment of adenomyosis, further studies are needed to determinate its longterm value. In this study, the safety and efficacy of US-guided HIFU ablation were evaluated and proved it to be a useful technique in the treatment of patients with adenomyosis. 900 Fertility and Sterility â Vol. 95, No. 3, March 1, /$36.00 Copyright ª2011 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert
2 MATERIALS AND METHODS Patients Nonmenopausal women with symptomatic adenomyosis were recruited at the First Affiliated Hospital of the Chongqing Medical University between March 2007 and September The protocol was approved by the Ethics Committee and Institutional Review Board of the institution. Inclusion criteria for this study were [1] age >18 years; [2] no desire to bear children; [3] dysmenorrhea and/or menorrhagia; [4] MRI evidence of typical features of adenomyosis with a depth >3 cm; [5] no previous other treatment or therapy for adenomyosis during the previous 3 months, including surgery; and [6] the ability to communicate clearly with the nurse or physician during the procedure. Patients with any of the following criteria were excluded from the study: [1] clinical examination or US scan that showed pelvic endometriosis or endometrial disease; [2] pregnancy; [3] pelvic inflammatory disease, tumor, or other uncontrolled systemic disease; [4] inability to lie in a prone position for 2 hours; [5] extensive abdominal scars in the proposed path of the US beam; and [6] contraindications to MRI. Ultrasound-guided High-intensity Focused Ultrasound Ablation High-intensity focused US ablation was performed with use of the Haifu JC Focused Ultrasound Tumor Therapeutic System (Chongqing Haifu Tech Co., Ltd., Chongqing, People s Republic of China). Each patient received one session of HIFU ablation as an outpatient. The treatment was performed outside of menstruation. Before treatment, patients underwent careful bowel preparation and were asked to shave the hair of the anterior abdominal region from the umbilicus to the upper margin of the pubic symphysis. During the procedure, a urinary catheter was inserted into the bladder and filled with degassed sterile water through an infusion set to control the bladder volume. Intravenous conscious sedation (fentanyl and benzodiazepine) was administered. The patient was placed in the prone position on the system with the anterior abdominal wall placed above the transducer in a sealed tank of degassed water. Real-time guided ultrasonography was used to determine the location of the target area of the junctional zone and to check whether it would be hazardous to other structures such as the gastrointestinal tract. The focus spot was positioned from the deep to superficial areas at least 1 cm from the border of the junctional zone and at least 1.5 cm from the endometrium, which resulted in complete planing of the target area of the junctional zone covered by the focused region. One slice per 5 mm of the target area of the junctional zone of the uterus was planed from right to left as a focus plane in the sagittal plane. The range of acoustic output power was regulated from 350 W to 400 W. The treatment time was within 3 hours. During the procedure, the sonication time and cooling time were adjusted on the basis of the tolerance of the patient and changes in gray scale on US. High-intensity focused US ablation was terminated once the gray scale covered the lesion margin (22). All patients were observed in a recovery room for 2 hours before discharge after the procedure. Oral prophylactic antibiotics were administered for the first 3 days after treatment, and patients returned to a normal diet gradually. Patients were required to practice contraception after the procedure. Outcome Measures All patients were surveyed regarding their pain levels during treatment using the Numerical Rating Scale immediately after the procedure. They also were asked if they would consent to receiving the same procedure again. A posttreatment enhanced MRI scan was performed within the first 3 months after the procedure in accordance with pretreatment imaging parameters that were used to assess the extent of the nonperfused region, which was determined subsequently by measuring the widening of the nonperfused region and the widening of the junctional zone on the T2-weighted images. Symptoms of menorrhea and dysmenorrhea were recorded with use of a 5-point categorical scale (1 ¼ not at all; 2 ¼ alittlebit;3¼ somewhat; 4 ¼ a great deal; 5 ¼ a very great deal) (23). Three months after treatment, the efficacy of US ablation was determined according to the degree of dysmenorrhea alleviation as follows: [1] complete relief: dysmenorrhea completely disappeared after treatment; [2] partial relief: after treatment, the pain score was reduced by 2 points or more and dysmenorrhea was not resolved completely; [3] minor relief: after treatment, the pain score lowered by 1 point and dysmenorrhea was still present; [4] ineffective: no change in the pain score after treatment; [5] exacerbated: after treatment, the pain score was higher; and [6] complete relief: partial and minor relief were determined as clinically effective. Clinical relapse was defined as the recurrence of clinical symptoms or an increase in the score described herein. Complications were described and graded with the use of the classification system of the Society of Interventional Radiology (SIR) (24), and they were assigned to categories according to the criteria of the American College of Obstetricians and Gynecologists (25). RESULTS Study Population Seventy-eight patients aged between 26 and 48 years, with an average age of years, were enrolled in the study. All patients had varying degrees of dysmenorrhea; 46 (59%) were seen with menorrhagia. The average uterine wall thickness was mm, and the average width of the junctional zone was mm. All patients received HIFU ablation therapy. Treatment had to be terminated in one patient (1.25%) because of her elevated blood pressure during the procedure. One patient (1.25%) withdrew from the study after 2 months on the advice of her physician and underwent a hysterectomy at her own request. Because a 3-month time period was used to evaluate effectiveness, that patient was not included in the effectiveness analyses, although her dysmenorrhea continued for 2 months after HIFU treatment despite adhering to the protocol to alleviate her symptoms. One patient (1.25%) became pregnant 5 months after the HIFU ablation procedure despite taking contraception as per the advice of her own physician. She delivered a boy by emergency cesarean section at 32 weeks because of hemorrhage caused by a complete placenta previa. A hysterectomy subsequently was performed. This patient also was not included in the effectiveness analyses. As of March 2010, 6 out of 75 patients (8%) were lost between the 1- and 2-month follow-up period. Data were obtained from the remaining 69 patients during the rest of the follow-up period with an average follow-up duration of months (18 36 months). Patients with complete follow-up data were included in the effectiveness analyses, and all patients were included in the safety analyses. Tolerance of Treatment and Satisfaction Of 78 patients, 23 (29.4%) had pain scores of 1 to 2 points, 43 (55.1%) scored 3 to 4 points, 12 (15.4%) scored 5 to 6 points, and 0 scored 0, 7 to 8, or 9 to 10 points. Patients with a score that was %4 points accounted for 84.6% of the patients in this study. Seventy-five patients (96.1%) were satisfied with the treatment process and expressed their willingness to undergo a repeated procedure. Efficacy For the 69 patients with complete follow-up data, efficacy was determined on the basis of the degree of alleviation of dysmenorrhea at 3 months after treatment. Among the patients, seven (10.1%) showed no improvement and required continued oral pain medication. Sixty-two (89.9%) had varying degrees of alleviation of their symptoms of dysmenorrhea with overall effectiveness rates as Fertility and Sterility â 901
3 FIGURE 1 Sagittal T1-weighted gadolinium-enhanced magnetic resonance images of the patients pelvis. (A) Before treatment. (B) Three months after treatment, showing a nonperfused region over 50% of lesion. (C) Before treatment. (D) Three months after treatment, showing a nonperfused region below 50% of lesion. (E) Before treatment. (F) Three months after treatment, no significant nonperfused region showing. follows: complete relief in 27 (39.1%); significant relief in 26 (37.7%); partial relief in nine (13.0%); and exacerbated pain in 0. In the 62 patients with clinically effective results, 8 (13%) had relapses (2 in the complete relief group, 1 in the partial relief group, and 5 in the minor relief group). Of these patients, 6 (9.7%) had a relapse at the 6-month point after treatment and 2 (3.2%) at 12 months after treatment, with a cumulative relapse rate of 12.9%. In 1 patient (1.6%) among those who had relapses, the dysmenorrhea score rose to 5 points, which reached the level of the pretreatment assessment. As a result, she received levonorgestrel-releasing 902 Zhou et al. Ultrasound ablation for adenomyosis Vol. 95, No. 3, March 1, 2011
4 TABLE 1 Nonperfused region and clinical efficacy (n [ 69). Nonperfused region No. (%) Clinical efficacies Effective (complete relief/partial relief/ minor relief) Ineffective 0 9 (13.0) 6 (4/0/2) 3 <50% 13 (18.9) 10 (3/4/3) 3 R50% 47 (68.1) 46 (20/22/4) 1 Note: c 2 ¼ , P¼.004. TABLE 2 Relapse and clinical outcome, relapse and nonperfused region (n [ 62). No. Yes Relapse No Symptomatic relief a Complete relief Partial relief Minor relief Nonperfused region b <50% R50% a c 2 ¼ , P<.001. b c 2 ¼ 3.401, P¼.183. intrauterine device therapy. The remaining 7 patients (11.3%) had dysmenorrhea scores that did not reach or exceed the pretreatment level, and these were subsequently given treatment with oral pain medication alone. Scores of and for patients with menorrhagia and dysmenorrhea, respectively, at 3 months after treatment were compared with those of and before treatment; the difference was statistically significant (P<.001 for both). Scores of and at the 18-month follow-up assessment were compared with the baseline; the difference was statistically significant (P<.001 for both). For the extent of coagulative necrosis assessed by enhanced MRI, 60 patients (87.0%) who had a nonperfused region had their treatment area assessed. Among the patients, there were a nonperfused region over 50% of lesion in 47 patients (68.1%) and a nonperfused region below 50% of lesion in 13 patients (18.9%), and there were 9 (13.0%) without a nonperfused region. Examples of the MRI are shown in Figure 1. There was statistical significance between the extent of nonperfused region and the clinical outcomes (P¼.004; see Table 1). Among the 8 patients (13%) who had a relapse out of the 62 patients in the study, the relationship was analyzed between relapses of different clinical significances and the extent of nonperfused region. There was a significant association between the occurrence of a relapse and different symptomatic relief (P<.001; see Table 2); however, there was no significant association between the occurrence of a relapse and the extent of nonperfused region (P¼.183; see Table 2). Safety Seven of the 77 patients (10%) who received the procedure were lost to follow-up at between 1 and 2 months after treatment, during which no complications had occurred in these patients. This showed that 22 patients (28.6%) had complications, of whom 4 (5.2%) had more than two types of complications. Twenty-three (85.1%) of the 27 complications required no medical symptomatic treatment (SIR class A). Management of SIR class B complications was as follows: there was one case (4.3%) of skin blisters and one case (4.3%) of erythema, which were both treated with local dressings; one case (4.3%) of abdominal pain was treated with an oral analgesic agent twice; in one case (4.3%) of numbness over the perineum the patient was given vitamins for neurotrophy for 1 month; all recovered. Patients reported no severe adverse events, extended hospitalization, or readmission. Details of complications are shown in Table 3. With use of American College of Obstetricians and Gynecologists criteria, febrile morbidity was the only complication, and the incidence of this was low at 2.6%. DISCUSSION The results of this study show that US-guided HIFU ablation appears to be a safe intervention for the treatment of adenomyosis. In addition, this method is well tolerated by patients. In this study, none of the patients had severe complications. Only two patients (2.6%) had redness or blisters of the skin; however, both had no skin ulcerations. Similar complications were reported by Stewart et al. (14). Only one case of third-degree skin burns has ever been reported (26). The most common adverse reaction is a skin injury occurring in the acoustic pathway of the US ablation. In addition, because the heat transfer of energy may affect nerve fibers and lead to indirect injury, Hindley et al. (27) reported one patient who had sensory abnormalities in the lower extremities after treatment that resolved only after 12 months. In the study, two cases of lower limb weakness, two cases of perianal pain, and one case of perineal numbness were observed, all of which were considered to be due to neurotoxicity related to heat transfer of energy. All patients recovered within days. Dysmenorrhea is the major symptom of adenomyosis. Therefore, in this benign disease, the extent of relief of dysmenorrhea after treatment can be used as an important indicator of the effectiveness of a treatment method. Yoon et al. (19) treated one case of adenomyosis with severe dysmenorrhea using MRI-guided focused US surgery; relief of dysmenorrhea was maintained during the 1-year follow-up period. Fukunishi et al. (20) treated 20 patients and followed them for up to 6 months, during which the clinical symptoms of adenomyosis also were relieved. The results of this study show that US-guided HIFU ablation effectively can alleviate clinical symptoms of adenomyosis. During an average of 24 months of follow-up (range: months), it was observed that the relief from symptoms was maintained. Moreover, our results show that the extent of nonperfused regions that exceeded 50% of lesions resulted in improved clinical efficacy, and, as a general rule, the larger the extent of coagulative necrosis, the better the clinical efficacy of the treatment. This is consistent with the preliminary study results that were reported by Wang et al. (21). Fertility and Sterility â 903
5 TABLE 3 Summary of complications according to the classification system of the Society of Interventional Radiology (n [ 77). SIR class Description No. (%) Complications No. (%) A No therapy, no consequences 23 (29.9) Vaginal discharge 10 (13.0) Lower abdominal pain 4 (5.2) Odynuria 4 (5.2) Perianal pain 2 (2.6) Hematuria 2 (2.6) Lower limb weakness 2 (2.6) Vomiting 1 (1.3) B Nominal therapy, observation, no consequences C Required therapy, minor hospitalization (<48 h) D Major therapy, unplanned 0 increase in level of care, prolonged hospitalization (R48 h) E Permanent adverse sequelae 0 F Death 0 Total no. Patients with complications a 22 (28.6) Patients without complications 4 (5.2) Redness or blisters on the skin 2 (2.6) Perineal numbness 1 (1.3) Lower abdominal pain 1 (1.3) 0 55 (71.4) Note: SIR ¼ Society of Interventional Radiology. a Twenty-two patients had a total of 27 complications. Four patients had two or more than two complications. All complications occurred within 30 days of the procedure. Currently, US-guided HIFU ablation remains a safe and effective noninvasive treatment for women with adenomyosis and represents an important development in this field. Further studies, such as a large multicenter clinical trial or a randomized controlled trial, will be significant in assessing its therapeutic value, as well as determining the best indications and scope of application of HIFU ablation for adenomyosis. REFERENCES 1. Tamai K, Togashi K, Ito T, Morisawa N, Fujiwara T, Koyama T. MR imaging findings of adenomyosis: correlation with histopathologic features and diagnostic pitfalls. Radiographics 2005;25: Matalliotakis IM, Kourtis AI, Panidis DK. Adenomyosis. Obstet Gynecol Clin North Am 2003;30: McCausland V, McCausland A. The response of adenomyosis to endometrial ablation/resection. Hum Reprod Update 1998;4: Goodwin SC, Spies JB, Worthington-Kirsch R, Peterson E, Pron G, Li S, et al. Uterine artery embolization for treatment of leiomyomata: long-term outcomes from the FIBROID Registry. Obstet Gynecol 2008;111: Kim MD, Kim S, Kim NK, Lee MH, Ahn EH, Kim HJ, et al. Long-term results of uterine artery embolization for symptomatic adenomyosis. AJR Am J Roentgenol 2007;188: Bratby MJ, Walker WJ. Uterine artery embolisation for symptomatic adenomyosis mid-term results. Eur J Radiol 2009;70: Sheng J, Zhang WY, Zhang JP, Lu D. The LNG-IUS study on adenomyosis: a 3-year follow-up study on the efficacy and side effects of the use of levonorgestrel intrauterine system for the treatment of dysmenorrhea associated with adenomyosis. Contraception 2009;79: Levgur M. Therapeutic options for adenomyosis: a review. Arch Gynecol Obstet 2007;276: Hou AH, Sullivan KF, Crawford ED. Targeted focal therapy for prostate cancer: a review. Curr Opin Urol 2009;19: Gianfelice D, Khiat A, Boulanger Y, Amara M, Belblidia A. Feasibility of magnetic resonance imaging guided focused ultrasound surgery as an adjunct to tamoxifen therapy in high-risk surgical patients with breast carcinoma. J Vasc Interv Radiol 2003;14: Zhang L, Zhu H, Jin C, Zhou K, Li K, Su H, et al. High-intensity focused ultrasound (HIFU): effective and safe therapy for hepatocellular carcinoma adjacent to major hepatic veins. Eur Radiol 2009;19: Wu F, Wang ZB, Chen WZ, Zou JZ, Bai J, Zhu H, et al. Extracorporeal focused ultrasound surgery for treatment of human solid carcinomas: early Chinese clinical experience. Ultrasound Med Biol 2004;30: Hesley GK, Gorny KR, Henrichsen TL, Woodrum DA, Brown DL. A clinical review of focused ultrasound ablation with magnetic resonance guidance: an option for treating uterine fibroids. Ultrasound Q 2008;24: Stewart EA, Rabinovici J, Tempany CM, Inbar Y, Regan L, Gostout B, et al. Clinical outcomes of focused ultrasound surgery for the treatment of uterine fibroids. Fertil Steril 2006; 85: Stewart EA, Gostout B, Rabinovici J, Kim HS, Regan L, Tempany CM. Sustained relief of leiomyoma symptoms by using focused ultrasound surgery. Obstet Gynecol 2007;110(2 Pt 1): Ren XL, Zhou XD, Zhang J, He GB, Han ZH, Zheng MJ, et al. Extracorporeal ablation of uterine fibroids with high-intensity focused ultrasound: imaging and histopathologic evaluation. J Ultrasound Med 2007;26: Yang Z, Cao YD, Hu LN, Wang ZB. Feasibility of laparoscopic high-intensity focused ultrasound treatment for patients with uterine localized adenomyosis. Fertil Steril 2009;91: Rabinovici J, Inbar Y, Eylon SC, Schiff E, Hananel A, Freundlich D. Pregnancy and live birth after focused ultrasound surgery for symptomatic focal adenomyosis: a case report. Hum Reprod 2006;21: Zhou et al. Ultrasound ablation for adenomyosis Vol. 95, No. 3, March 1, 2011
6 19. Yoon SW, Kim KA, Cha SH, Kim YM, Lee C, Na YJ. Successful use of magnetic resonance guided focused ultrasound surgery to relieve symptoms in a patient with symptomatic focal adenomyosis. Fertil Steril 2008;90:2018.e Fukunishi H, Funaki K, Sawada K, Yamaguchi K, Maeda T, Kaji Y. Early results of magnetic resonance guided focused ultrasound surgery of adenomyosis: analysis of 20 cases. J Minim Invasive Gynecol 2008;15: Wang W, Wang Y, Tang J. Safety and efficacy of high intensity focused ultrasound ablation therapy for adenomyosis. Acad Radiol 2009;16: Rabkin BA, Zderic V, Vaezy S. Hyperecho in ultrasound images of HIFU therapy: involvement of cavitation. Ultrasound Med Biol 2005;31: Spies JB, Coyne K, Guaou N, Boyle D, Skyrnarz- Murphy K, Gonzalves SM. The UFS-QOL, a new disease-specific symptom and health-related quality of life questionnaire for leiomyomata. Obstet Gynecol 2002;99: Goodwin SC, Bonilla SC, Sacks D, Reed RA, Spies JB, Landow WJ, et al. Reporting standards for uterine artery embolization for the treatment of uterine leiomyomata. J Vasc Interv Radiol 2003;14(9 Pt 2):S Sawin SW, Pilevsky ND, Berlin JA, Barnhart KT. Comparability of perioperative morbidity between abdominal myomectomy and hysterectomy for women with uterine leiomyomas. Am J Obstet Gynecol 2000;183: Leon-Villapalos J, Kaniorou-Larai M, Dziewulski P. Full thickness abdominal burn following magnetic resonance guided focused ultrasound therapy. Burns 2005;31: Hindley J, Gedroyc WM, Regan L, Stewart E, Tempany C, Hynyen K, et al. MRI guidance of focused ultrasound therapy of uterine fibroids: early results. AJR Am J Roentgenol 2004;183: Fertility and Sterility â 905
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