{"paper_id":"323d53bf-29f9-4e38-b42b-52be12ecb75a","body_text":"e-ultrasonography.org Ultrasonography 36(2), April 2017\n95\nCurrent status of high-intensity focused \nultrasound for the management of \nuterine adenomyosis\nVincent Y . T. Cheung\nDepartment of Obstetrics and Gynaecology, Queen Mary Hospital, The University of Hong \nKong, Hong Kong https://doi.org/10.14366/usg.16040\npISSN: 2288-5919 • eISSN: 2288-5943\nUltrasonography 2017;36:95-102\nWhile high-intensity focused ultrasound has been used for some time in the management of \nuterine fibroids, its effectiveness and safety in managing adenomyosis is less well established. \nA literature review was performed of all eligible reports using this modality as a treatment for \nadenomyosis. Relevant publications were obtained from the PubMed electronic database from \ninception through March 2016. Eleven articles, including information from 1,150 treatments and \nfollow-up data from 990 patients, were reviewed. High-intensity focused ultrasound appears to \nbe effective and safe in the management of symptomatic adenomyosis, and can be considered \nas an alternative uterine-sparing option for women with this condition. \nKeywords: Adenomyosis; High-intensity focused ultrasound; Ultrasonography\nReceived: October 1, 2016\nRevised: November 27, 2016\nAccepted: November 30, 2016\nCorrespondence to:\nVincent Y . T. Cheung, MBBS, FRCOG, \nFRCSC, Department of Obstetrics and \nGynaecology, Queen Mary Hospital, \nThe University of Hong Kong, 102 \nPokfulam Road, Hong Kong\nTel. +852-22553914\nFax. +852-25173278\nE-mail: vytc@hku.hk\nREVIEW ARTICLE\nThis is an Open Access article distributed under the \nterms of the Creative Commons Attribution Non-\nCommercial License (http://creativecommons.org/\nlicenses/by-nc/3.0/) which permits unrestricted non-\ncommercial use, distribution, and reproduction in \nany medium, provided the original work is properly \ncited.\nCopyright © 2017 Korean Society of \nUltrasound in Medicine (KSUM)\nHow to cite this article: \nCheung VYT. Current status of high-intensity \nfocused ultrasound for the management of \nuterine adenomyosis. Ultrasonography. 2017 \nApr;36(2):95-102.\nIntroduction\nUterine adenomyosis is a common gynecologic disorder of women of reproductive age. It is \ncharacterized by the presence of ectopic endometrial glands and stroma within the myometrium, \nresulting in uterine enlargement. It can be asymptomatic, but can give rise to significant symptoms, \nmost commonly menorrhagia and dysmenorrhea [1]. The treatment for adenomyosis can be \nchallenging. Historically, the standard of treatment has been hysterectomy. However, this is not always \nan acceptable option, especially for women who wish to maintain their fertility. Medical treatment \nmainly allows the control of symptoms, whereas uterine-sparing surgical techniques, such as the \nexcision of adenomyotic foci or electrocoagulation of the involved myometrium, are associated with \nvariable success and risk of recurrence [1,2]. Although uterine artery embolization has been used as \na minimally invasive treatment option with some success, its impact on future fertility and pregnancy \nremains uncertain [1,3,4]. \nRecently, increasing attention has been paid to high-intensity focused ultrasound (HIFU) therapy for \nthe management of adenomyosis [5,6]. It induces focal thermocoagulation of the adenomyotic lesions \nand has been shown to be a safe and effective treatment for adenomyosis [5,6]. Magnetic resonance \n(MR) imaging and, more recently, ultrasound (US) have been used to target and monitor the ablation \nprocess [5,7,8]. HIFU may also be able to provide an additional minimally invasive treatment option \nfor premenopausal women with uterine adenomyosis. The purpose of this article was to review the \nbackground, clinical use, and treatment outcomes of HIFU in the treatment of adenomyosis. \n\n\nVincent Y . T. Cheung\n96\n Ultrasonography 36(2), April 2017 e-ultrasonography.org\nImaging-Guided HIFU\nIn 1942, Lynn et al. [9] introduced the use of an extracorporeal \nsource of focused US energy to induce coagulative necrosis in \ntargeted tissue without damaging surrounding and overlying vital \nstructures. The principle of this HIFU therapy is to cause tissue \nablation through heating, cavitation, and direct damage to tumor \nblood vessels, by focusing US energy at a targeted spot, with \nminimal damage to the surrounding tissues.\nHIFU can be performed under the guidance of MR or US imaging \nin order to target and monitor the ablation process. MR imaging \noffers excellent anatomic resolution and temperature sensitivity \nduring real-time treatment monitoring. The ExAblate device \n(Insightec, Tirat Carmel, Israel) is currently the only United States \nFood and Drug Administration (FDA)-approved MR-guided HIFU \nsystem. Another system, the Sonalleve (Philips Healthcare, Andover, \nMA, USA), has received \nConformité Européene  (CE) marking for \nfibroid treatment.\nUS-guided HIFU uses grayscale or echogenicity changes to \ndetermine the adequacy of ablation instead of temperature-\nmapping changes, as in MR-guided HIFU. The JC HIFU system \n(Chongqing Haifu Technology, Chongqing, China) (Fig. 1) has \nbeen installed at Queen Mary Hospital since 2006, mainly for the \ntreatment of hepatocellular carcinoma [10]; since 2011, the ablation \nof symptomatic uterine fibroids has also been performed [7,8]. \nAs described in a previous review of fibroid management [7], this \nHIFU system consists of a real-time 3.5-MHz diagnostic US scanner \nintegrated into the center of a 12-cm in diameter, 15-cm in focal \nlength, 0.8-MHz therapeutic US transducer (Fig. 2). In addition to \nthe US system, it contains a 6-direction therapeutic planning system, \na degassed water circulation system, and a master control \ncomputer unit. The system can attain an acoustic output power of \nup to 400 W, and the linear motion deviation of the therapeutic \ndevice is ±1 mm. During treatment, patients are placed in the prone \nposition under intravenous conscious sedation. This enables minimal \npatient movement while the lower abdominal skin is in contact with \nthe degassed water. The entirety of the lesion is divided into slices \nof 5 mm. The acoustic output power is set between 350 and 400 W, \nand with successive sweeps from the deep to the shallow region, \nthe entire volume of the lesion is ablated [7]. Fig. 3 illustrates the \nMR images of a woman with extensive adenomyosis before and 3 \nmonths after HIFU treatment. Other similar systems, including the \nHIFU-2001 (SJTU Suntec Industry, Shanghai, China), HIFUNIT9000 \n(Shanghai A&S Science and Technology, Shanghai, China), and FEP-\nBY Series (China Medical Technologies, Beijing, China) are also \ncurrently used clinically for the treatment of fibroids. However, none \nof these systems described have received FDA approval.\nThe selection criteria for HIFU therapy for adenomyosis vary \ndepending on the experience of an individual center. The criteria used \nin most studies can be summarized as follows: (1) premenopausal \nwomen of over 18 years of age with no plans for future child-\nbearing [11\n-16]; (2) significant symptoms related to adenomyosis \n[11-17]; (3) features of adenomyosis on MR imaging [11,13 -16]; \n(4) adenomyotic lesions greater than 3 cm but less than 10 cm in \ndiameter [11,14]; (5) no evidence of known or suspected extensive \npelvic adhesions, such as a history of acute pelvic inflammatory \ndisease, severe pelvic endometriosis, or lower abdominal surgery \n[12\n-18]; and (6) body weight of less than 100 kg [16] or abdominal \nwall thickness of less than 5 cm [17]. \nTreatment centers vary in their protocols for patient assessment \nFig. 1.  Ultrasound-guided high-intensity focused ultrasound \nsystem.\nFig. 2. Real-time diagnostic ultrasound scanner integrated into \nthe center of the therapeutic ultrasound transducer. \n\nHigh-intensity focused ultrasound and adenomyosis\ne-ultrasonography.org Ultrasonography 36(2), April 2017\n97\nand preparation. Pretreatment imaging to confirm the diagnosis and \nto establish the extent of adenomyosis is performed. Additionally, \npretreatment planning is carried out with the patient lying prone \non the treatment table, which mimics the treatment process and \nfamiliarizes the patient with the treatment. During the planning \nprocess, the path of sonication, depth of the target, proximity of the \ntarget to the sacrum, and the likelihood of the presence of a bowel \nloop along the path of sonication are evaluated [7].\nLiterature Review\nA review of the literature published in English was obtained from \nthe PubMed electronic database from inception through March \n2016, using the search words ‘‘adenomyosis’’ and “high-intensity \nfocused ultrasound,” “HIFU,” or “focused ultrasound ablation,” \nsupplemented by hand-searching the references of the relevant \narticles. The acceptability of the articles to be included in the \nreview was decided by reading the articles’ abstracts and full text \nif necessary, and only those articles that evaluated the use of HIFU \nin the treatment of adenomyosis without associated fibroids and \nincluded complete interpretable information with relevant outcome \ndata were reviewed. Ultimately, 11 articles were reviewed. The \ninformation that was retrieved from the eligible articles included \nthe number of patients, treatment details, criteria for symptom \nassessment, volume of uteri and adenomyotic lesions, and related \ncomplications.  \nEleven articles were identified, including information from 1,150 \ntreatments and follow-up data from 990 patients [11\n-21]. Table 1 \nsummarizes the background information of each article. Of these 11 \narticles, five were MR-guided and six were US-guided HIFU studies, \nreporting a total of 84 and 1,066 treatments with follow-up data, \nrespectively. Two articles were excluded because their reported \ntreatment(s) were likely duplicates of those reported in other articles \n[22,23]. Among the reviewed articles, seven were prospective cohort \nstudies [11,12,14\n-16,18,21], three were retrospective reviews \n[13,17,20], and one was a case report [19]. All articles reported the \ndegree of symptom improvement, but only four reported the degree \nof uterine volume or adenomyotic lesion reduction [11,12,14,17]. \nTreatment Outcomes\nTable 2 presents details of the 10 studies that evaluated the \nimprovement of menorrhagia; seven studies used the symptom \nseverity score of a quality of life questionnaire specific to fibroids \nknown as the Uterine Fibroid Symptom and Quality of Life \nquestionnaire [24]; while three studies used the menstrual volume \nor menorrhagia scale, which was scored according to patients’ \ndescriptions on a 5-point scale [15,21] or as described by Sharp \net al. in 1995 [25]. The reported degree of menorrhagia reduction \nranged from 12.4% to 33.3%, 25.3% to 80.8%, 16.4% to 52.4%, \n24.9% to 66.4%, 44.0%, and 44.8% at 1-, 3-, 6-, 12-, 18-, and \n24-month follow-ups, respectively (Table 2). \nThe reduction of dysmenorrhea, as determined based on the \nmenstrual pain score using a visual analog scale, was evaluated in \nFig. 3. Magnetic resonance (MR) images from a 47-year-old woman with adenomyosis.\nA. Pretreatment MR image shows extensive adenomyosis involving mostly the fundal and anterior uterine wall (arrows). B. MR image (with \ncontrast) 3 months after treatment shows a well-defined hypoperfused area (arrows) as the result of focused ultrasound ablation.  \nA\nB\n\n\nVincent Y . T. Cheung\n98\n Ultrasonography 36(2), April 2017 e-ultrasonography.org\nseven studies (Table 3); all showed a reduction of dysmenorrhea \nat 3 months (range, 25.0% to 83.3%), 6 months (range, 44.7% to \n100%), 12 months (range, 64.0% to 72.1%), 18 months (54.2%), \nand 24 months (56.0%).\nFive studies reported the degree of uterine volume reduction \nafter HIFU therapy, with values ranging from 12.7% to 54.0% over \nfollow-up periods of 1 to 12 months (Table 4). However, only two \narticles reported the degree of reduction in adenomyotic lesions \nover 12 months (Table 4). The nonperfused volume, which is the \npercentage of the uterine volume ablated and shown as a non-\nenhancing area on contrast-enhanced T1-weighed MR imaging after \nthe treatment, has been suggested to be associated with the degree \nof subsequent symptom improvement. This indicator was reported \nin seven studies, with mean values ranging from 24.4% to 62.5% \n[11\n-16,19]. However, a study that reported a range of 5% to 99% \nwas excluded [21]. \nTreatment Data\nTable 5 shows the treatment data, including treatment and \nTable 2. Improvement of menorrhagia after high-intensity focused ultrasound for adenomyosis\nStudy Reduction in menorrhagia (%)\na)\n1 3 6 12 18 24\nMagnetic resonance-guided\n　Ferrari et al. [18], 2016 - - - 66.4 - -\n　Fan et al. [11], 2012 12.4 25.3 16.4 24.9 - -\n　Polina et al. [19], 2012 - 31.6 47.4 - - -\n　Kim et al. [20], 2011 - 25.9 40.7 - - -\n　Fukunishi et al. [12], 2008 33.3 53.5 44.8 - - -\nUltrasound-guided\n　Lee et al. [17], 2015 - 55.6 52.4 58 - -\n　Shui et al. [21], 2015 -   44.8\nb)\n- 48.3\nb)\n- 44.8\nb)\n　Long et al. [14], 2015 - 32.9 50.4 64.7 - -\n　Zhou et al. [15], 2011 -   48.0\nb)\n- - 44.0\nb)\n-\n　Wang et al. [16], 2009 - 57.0-80.8\nb, c)\n- - -\na)\nMonths after treatment, based on the symptom severity score of the Uterine Fibroid Symptom and Quality of Life questionnaire, unless otherwise specified. \nb)\nBased on \nmenstrual volume/menorrhagia score. \nc)\nVaried depending on power output (290-420 W).\nTable 1. Summary of studies of high-intensity focused ultrasound for adenomyosis\nStudy City, country High-intensity focused \nultrasound system No. of treatments No. of patients who \ncompleted follow-up\nDuration of \nfollow-up (mo)\nMagnetic resonance-guided \n　Ferrari et al. [18], 2016 L' Aquila, Italy ExAblate\na)\n18 18 12\n　Fan et al. [11], 2012 Chongqing, China JM15100\nb)\n10 10 12\n　Polina et al. [19], 2012 Andhra Pradesh, India ExAblate\na)\n1 1 6\n　Kim et al. [20], 2011 Gyeonggi-do, South Korea ExAblate\na)\n35 35 6\n　Fukunishi et al. [12], 2008 Kobe, Japan ExAblate\na)\n20 20 6\nUltrasound-guided \n　Liu et al. [13], 2016 Beijing, China JC\nb)\n230 208 3\n　Lee et al. [17], 2015 Incheon, South Korea JC\nb)\n346 346 12\n　Shui et al. [21], 2015 Chongqing and Sichuan, China JC200\nb)\n350 224 24\n　Long et al. [14], 2015 Chongqing, China JC200\nb)\n51 47 12\n　Zhou et al. [15], 2011 Chongqing, China JC\nb)\n77 69 18\n　Wang et al. [16], 2009 Beijing, China JC\nb)\n12 12 3\na)\nInsightec, Tirat Carmel, Israel. \nb)\nChongqing Haifu Technology, Chongqing, China. \n\nHigh-intensity focused ultrasound and adenomyosis\ne-ultrasonography.org Ultrasonography 36(2), April 2017\n99\nTable 3. Improvement of dysmenorrhea after high-intensity focused ultrasound for adenomyosis\nStudy Reduction in dysmenorrhea (%)\na)\n3 6 12 18 24\nMagnetic resonance-guided\n　Polina et al. [19], 2012 60 100 - - -\n　Kim et al. [20], 2011 30.6 44.7 - - -\nUltrasound-guided\n　Liu et al. [13], 2016 61.8 - - - -\n　Shui et al. [21], 2015 62 - 64 - 56\n　Long et al. [14], 2015 28.8 53.5 72.1 - -\n　Zhou et al. [15], 2011 56.3 - - 54.2 -\n　Wang et al. [16], 2009 25.0-83.3\nb)\n- - - -\na)\nMonths after treatment, based on menstrual pain score. \nb)\nVaried depending on power output (290-420 W).\nTable 4. Volume reduction of the uterus or adenomyotic lesion after high-intensity focused ultrasound\nStudy Reduction in uterine volume or adenomyotic lesion volume (%)\na)\n1 3 6 12\nMagnetic resonance-guided\n　Fan et al. [11], 2012 21.9 (11.9)\na)\n22.5 (28.3)\na)\n29.3 (40.2)\na)\n23.8 (29.1)\na)\n　Fukunishi et al. [12], 2008 - - 12.7 -\nUltrasound-guided\n　Lee et al. [17], 2015 \n- 44 47 54\n　Long et al. [14], 2015 - - - 22 (30.2)\na)\na)\nMonths after treatment.\nTable 5. Treatment data\nStudy Treatment time\na)\nSonication time\nb)\nTotal exposure energy (J) Volume of uterus (cm\n3\n) Volume of adenomyotic \nlesion (cm\n3\n)\nMagnetic resonance-guided\n　Fan et al. [11], 2012 114±48 \n(42-192)\n990.5±480.6 \n(245.0-1,727.0)\n299,019.5±154,636.0 272.0±99.2 \n(148.8-440.0)\n94.9±54.6 \n(30.4-208.4)\n　Polina et al. [19], 2012 110 NA 108,996 NA 91\n　Kim et al. [20], 2011 150±40 NA NA 430±230 NA\n　Fukunishi et al. [12], 2008 <180 NA 157,745.4\nc) \n(69,066.8-491,840.3)\n445±296 \n(95% CI, 307-584)\nNA\nUltrasound-guided\n　Liu et al. [13], 2016 64\nc) \n(IQR, 47-91) \n1,135\nc) \n \n(IQR, 769-1,561)\nNA 274.4±174.8 \n(47-1,390)\n70.7±33.0 \n(16-177)\n　Lee et al. [17], 2015 82.3\nc) \n1,049.4\nc) \n363,556.6\nc) \n264.1\nc) \nNA\n　Shui et al. [21], 2015 103.8±59.4 \n(11.0-247.0)\n1,197.3±744.2 \n(114-4,000)\n454,016.2±282,200.6 \n(43,228.8-1,516,800)\n253.1±109.3 \n(100.4-708.2)\n66.2±48.6 \n(4.2-373.3)\n　Zhou et al. [15], 2011 <180 NA\nd)\nNA\nd)\nNA\nd)\nNA\n　Wang et al. [16], 2009 NA (468-3,413) (138,000-1,432,000) NA\nd)\nNA\nValues are presented as mean±standard deviation (range), unless otherwise specified.\nNA, not available; CI, confidence interval; IQR, interquartile range.\na)\nTreatment time (in minutes) was defined as the time from the first sonication to the last sonication, except in the study by Fan et al. [11], in which it was defined as the time \nfrom the first magnetic resonance localization scan to the last sonication. \nb)\nSonication time (in seconds) was defined as the time of ablation when energy was delivered to the \ntarget. \nc)\nMedian value. \nd)\nMean treatment time between 1,132 and 1,820 seconds, mean total exposure energy between 384,637 and 765,571 J, and mean uterine volume \nbetween 213 and 253 cm\n3\n; varied depending on power output (290-420 W). \n\nVincent Y . T. Cheung\n100\n Ultrasonography 36(2), April 2017 e-ultrasonography.org\nsonication time, and the total exposure energy. The volume of \nthe uteri and the adenomyotic lesions were also included when \navailable for reference, as these values may have directly influenced \nthe duration of treatment. Treatment time was generally defined as \nthe time from the first sonication to last sonication, unless otherwise \nspecified in the article, and sonication time referred to the time of \nablation when energy was being delivered to the target.\nComplications\nComplications arising from HIFU in the treatment of adenomyosis \nwere rare. Five of the 11 studies reported no adverse events or \nserious complications [11,16,18\n-20]. The complications reported in \nthe other five studies are summarized in Table 6. The most common \ncomplication was vaginal discharge or bleeding (range, 2.6% to \n58.8%). Tissue burns, as the result of excessive power generated \nor accumulated in an incorrect target or in organs adjacent to \nthe target, were uncommon. Skin burns, mostly of a mild degree, \noccurred in seven patients, and there were no reports of bowel \nor urinary bladder injury. The study carried out by Lee et al. [17] \nwas excluded, as their safety data combined both fibroid and \nadenomyosis treatment.\nDiscussion\nThe management of uterine adenomyosis can be challenging, \nparticularly in patients who wish to maintain their fertility [1]. \nWhile making treatment decisions, the age of the patients, severity \nof symptoms, desire for future fertility, and associated pelvic \npathologies such as fibroids and endometriosis are important \nconsiderations. Various uterine-sparing interventions have been \ndescribed in managing adenomyosis, including uterine artery \nembolization, myometrial or adenomyoma excision or reduction, or \nmyometrial electrocoagulation [1,2]. However, insufficient properly \ndesigned trials have been conducted for adequate evidence to \nsupport one treatment over the other. \nHIFU has been shown to be effective and safe in the treatment \nof uterine fibroids [6\n-8]. However, in treating adenomyosis, the \neffectiveness of HIFU is less well established and therefore, in our \ncenter, this treatment modality is still considered investigational. \nAdenomyosis can be a cause of significant morbidity, and further \nwork is needed to explore more effective and safe therapies. The \nfindings from this review seem encouraging, as HIFU appears to be \neffective in relieving, at least in part, the symptoms of adenomyosis, \nincluding menorrhagia and dysmenorrhea over a period of 1\n-2 \nyears after treatment. This modality can be considered as an \nalternative option for women with adenomyosis who wish to \npreserve their uteri. However, as a fertility-sparing option, further \nevidence is certainly required to reassure clinicians and patients of \nthe safety of this intervention if further pregnancy is desired. \nThis review includes studies of both MR-guided and US-guided \nHIFU. Although the principle of therapy is similar in both techniques, \nit is unclear whether one type of image guidance has advantages \nover the other. There is no doubt that the guiding images obtained \nduring MR-guided therapy are much better than those obtained \nduring US-guided therapy, especially during intraoperative mapping \nof the adenomyotic lesion, but whether this leads to better and safer \ntreatment outcomes remains uncertain. \nThis review has limitations. The lack of primary data in most \nstudies made it impossible to carry out comparative evaluations \nof certain important parameters, such as the degree of symptom \nrelief, treatment time, and sonication time. Data combining both \nTable 6. Summary of complications\nComplication Fukunishi et al. [12] Liu et al. [13] Shui et al. [21] Long et al. [14] Zhou et al. [15]\nNo. of patients 20 230 350 51 77\nLeg pain, prolonged\na)\n1 (5) - - - -\nSacrococcygeal or buttock pain, prolonged\na)\n2 (10) - - 4 (7.8) 2 (2.6)\nAbdominal pain, prolonged\na)\n- - - 1 (1.9) 1 (1.3)\nLower limb or perineal numbness - 2 (0.8) 1 (0.3) 9 (17.6) 3 (3.9)\nSkin burn - 2\nb)\n (0.8) 3\nb)\n (0.9) - 2\nb)\n (2.6)\nLow grade fever - - 1 (0.3) - -\nVaginal discharge or bleeding - 6 (2.6) 27 (7.7) 30 (58.8) 10 (13.0)\nHematuria - - - - 2 (2.6)\nContact dermatitis to acoustic gel pad 1 (5) - - - -\nData are presented as number (%).\na)\nLasted more than 7 days. \nb)\nFour of the seven patients had first-degree burns, and three of the seven patients had second-degree burns.\n\nHigh-intensity focused ultrasound and adenomyosis\ne-ultrasonography.org Ultrasonography 36(2), April 2017\n101\nfibroid and adenomyosis treatment rendered a study unsuitable for \nevaluation [17]. The cost of each modality was not evaluated. The \ndefinitions of certain complications were not provided, so it was \ndifficult to make comparisons between studies. Additionally, it is \nunfortunate that we were not able to include a recent large review \nconsisting of 9,988 cases, of which 2,549 were adenomyosis, in this \nstudy, as no symptom outcome data were reported [6]. Nevertheless, \ndespite these shortcomings, the availability of HIFU is indicative \nof the potential of advancements in adenomyosis treatment, and \nawareness of this treatment modality will allow physicians to \nprovide optimal care to their patients. \nConclusion\nHIFU appears to be effective and safe in the management of \nsymptomatic adenomyosis, and can be considered as an alternative \nuterine-sparing option for women with this condition. \nORCID: Vincent Y . T. Cheung: http://orcid.org/0000-0002-3293-0697\nConflict of Interest\nNo potential conflict of interest relevant to this article was reported.\nReferences\n 1. Struble J, Reid S, Bedaiwy MA. 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