{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T19:21:56Z","timestamp":1790623316126,"version":"4.1.0"},"reference-count":81,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,10,24]],"date-time":"2019-10-24T00:00:00Z","timestamp":1571875200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,10,24]],"date-time":"2019-10-24T00:00:00Z","timestamp":1571875200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Transl Med"],"published-print":{"date-parts":[[2019,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n              <jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Magnetic resonance guided focused ultrasound was suggested for the induction of deep localized hyperthermia adjuvant to radiation- or chemotherapy. In this study we are aiming to validate an experimental model for the induction of uniform temperature elevation in osteolytic bone tumours, using the natural acoustic window provided by the cortical breakthrough.<\/jats:p>\n              <\/jats:sec>\n              <jats:sec>\n                <jats:title>Materials and methods<\/jats:title>\n                <jats:p>Experiments were conducted on ex vivo lamb shank by mimicking osteolytic bone tumours. The cortical breakthrough was exploited to induce hyperthermia inside the medullar cavity by delivering acoustic energy from a phased array HIFU transducer. MR thermometry data was acquired intra-operatory using the proton resonance frequency shift (PRFS) method. Active temperature control was achieved via a closed-loop predictive controller set at 6\u00a0\u00b0C above the baseline. Several beam geometries with respect to the cortical breakthrough were investigated. Numerical simulations were used to further explain the observed phenomena. Thermal safety of bone heating was assessed by cross-correlating MR thermometry data with the measurements from a fluoroptic temperature sensor inserted in the cortical bone.<\/jats:p>\n              <\/jats:sec>\n              <jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Numerical simulations and MR thermometry confirmed the feasibility of spatio-temporal uniform hyperthermia (\u00b1\u20090.5\u00a0\u00b0C) inside the medullar cavity using a fixed focal point sonication. This result was obtained by the combination of several factors: an optimal positioning of the focal spot in the plane of the cortical breakthrough, the direct absorption of the HIFU beam at the focal spot, the \u201cacoustic oven effect\u201d yielded by the beam interaction with the bone, and a predictive temperature controller. The fluoroptical sensor data revealed no heating risks for the bone and adjacent tissues and were in good agreement with the PRFS thermometry from measurable voxels adjacent to the periosteum.<\/jats:p>\n              <\/jats:sec>\n              <jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>To our knowledge, this is the first study demonstrating the feasibility of MR-guided focused ultrasound hyperthermia inside the medullar cavity of bones affected by osteolytic tumours. Our results are considered a promising step for combining adjuvant mild hyperthermia to external beam radiation therapy for sustained pain relief in patients with symptomatic bone metastases.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12967-019-2094-x","type":"journal-article","created":{"date-parts":[[2019,12,18]],"date-time":"2019-12-18T08:14:22Z","timestamp":1576656862000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":32,"title":["Mild hyperthermia by MR-guided focused ultrasound in an ex vivo model of osteolytic bone tumour: optimization of the spatio-temporal control of the delivered temperature"],"prefix":"10.1186","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2792-6543","authenticated-orcid":false,"given":"Pauline C.","family":"Guillemin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Gui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Orane","family":"Lorton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Zilli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lindsey A.","family":"Crowe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"St\u00e9phane","family":"Desgranges","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xavier","family":"Montet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sylvain","family":"Terraz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raymond","family":"Miralbell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rares","family":"Salomir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sana","family":"Boudabbous","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,10,24]]},"reference":[{"issue":"3","key":"2094_CR1","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1016\/j.critrevonc.2005.03.011","volume":"56","author":"G Selvaggi","year":"2005","unstructured":"Selvaggi G, Scagliotti GV. Management of bone metastases in cancer: a review. Crit Rev Oncol Hematol. 2005;56(3):365\u201378.","journal-title":"Crit Rev Oncol Hematol"},{"issue":"3","key":"2094_CR2","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1053\/ctrv.2000.0210","volume":"27","author":"RE Coleman","year":"2001","unstructured":"Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 2001;27(3):165\u201376.","journal-title":"Cancer Treat Rev"},{"issue":"4","key":"2094_CR3","doi-asserted-by":"publisher","first-page":"1810","DOI":"10.1088\/0031-9155\/61\/4\/1810","volume":"61","author":"HM ten Eikelder","year":"2016","unstructured":"ten Eikelder HM, Bosnacki D, Elevelt A, et al. Modelling the temperature evolution of bone under high intensity focused ultrasound. Phys Med Biol. 2016;61(4):1810\u201328.","journal-title":"Phys Med Biol"},{"issue":"Suppl 1","key":"2094_CR4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0305-7372(06)80001-0","volume":"32","author":"RE Coleman","year":"2006","unstructured":"Coleman RE. The role of bone markers in metastatic bone disease. Cancer Treat Rev. 2006;32(Suppl 1):1\u20132.","journal-title":"Cancer Treat Rev"},{"issue":"2","key":"2094_CR5","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1200\/JCO.2004.03.097","volume":"22","author":"MP Goetz","year":"2004","unstructured":"Goetz MP, Callstrom MR, Charboneau JW, et al. Percutaneous image-guided radiofrequency ablation of painful metastases involving bone: a multicenter study. J Clin Oncol. 2004;22(2):300\u20136.","journal-title":"J Clin Oncol"},{"issue":"11","key":"2094_CR6","doi-asserted-by":"publisher","first-page":"798","DOI":"10.1093\/jnci\/dji139","volume":"97","author":"WF Hartsell","year":"2005","unstructured":"Hartsell WF, Scott CB, Bruner DW, et al. Randomized trial of short- versus long-course radiotherapy for palliation of painful bone metastases. J Natl Cancer Inst. 2005;97(11):798\u2013804.","journal-title":"J Natl Cancer Inst"},{"issue":"3","key":"2094_CR7","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/S0167-8140(00)00238-3","volume":"56","author":"E Chow","year":"2000","unstructured":"Chow E, Danjoux C, Wong R, et al. Palliation of bone metastases: a survey of patterns of practice among Canadian radiation oncologists. Radiother Oncol. 2000;56(3):305\u201314.","journal-title":"Radiother Oncol"},{"issue":"11","key":"2094_CR8","doi-asserted-by":"publisher","first-page":"1423","DOI":"10.1200\/JCO.2006.09.5281","volume":"25","author":"E Chow","year":"2007","unstructured":"Chow E, Harris K, Fan G, et al. Palliative radiotherapy trials for bone metastases: a systematic review. J Clin Oncol. 2007;25(11):1423\u201336.","journal-title":"J Clin Oncol"},{"issue":"5","key":"2094_CR9","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1016\/S1090-3801(02)00028-9","volume":"6","author":"T Saarto","year":"2002","unstructured":"Saarto T, Janes R, Tenhunen M, Kouri M. Palliative radiotherapy in the treatment of skeletal metastases. Eur J Pain. 2002;6(5):323\u201330.","journal-title":"Eur J Pain"},{"issue":"10","key":"2094_CR10","doi-asserted-by":"publisher","first-page":"747","DOI":"10.1016\/j.clon.2006.09.007","volume":"18","author":"JP Agarawal","year":"2006","unstructured":"Agarawal JP, Swangsilpa T, van der Linden Y, et al. The role of external beam radiotherapy in the management of bone metastases. Clin Oncol (R Coll Radiol). 2006;18(10):747\u201360.","journal-title":"Clin Oncol (R Coll Radiol)"},{"issue":"1","key":"2094_CR11","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.radonc.2004.09.017","volume":"75","author":"DE Roos","year":"2005","unstructured":"Roos DE, Turner SL, O\u2019Brien PC, et al. Randomized trial of 8\u00a0Gy in 1 versus 20\u00a0Gy in 5 fractions of radiotherapy for neuropathic pain due to bone metastases (Trans-Tasman Radiation Oncology Group, TROG 96.05). Radiother Oncol. 2005;75(1):54\u201363.","journal-title":"Radiother Oncol."},{"issue":"1","key":"2094_CR12","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.ijrobp.2011.10.080","volume":"84","author":"M Huisman","year":"2012","unstructured":"Huisman M, van den Bosch MA, Wijlemans JW, et al. Effectiveness of reirradiation for painful bone metastases: a systematic review and meta-analysis. Int J Radiat Oncol Biol Phys. 2012;84(1):8\u201314.","journal-title":"Int J Radiat Oncol Biol Phys"},{"issue":"5","key":"2094_CR13","doi-asserted-by":"publisher","first-page":"1457","DOI":"10.1002\/cncr.26410","volume":"118","author":"E Chow","year":"2012","unstructured":"Chow E, Nguyen J, Zhang L, et al. International field testing of the reliability and validity of the EORTC QLQ-BM22 module to assess health-related quality of life in patients with bone metastases. Cancer. 2012;118(5):1457\u201365.","journal-title":"Cancer"},{"key":"2094_CR14","doi-asserted-by":"publisher","first-page":"153303381876220","DOI":"10.1177\/1533033818762207","volume":"17","author":"JM Baust","year":"2018","unstructured":"Baust JM, Rabin Y, Polascik TJ, et al. Defeating cancers\u2019 adaptive defensive strategies using thermal therapies: examining cancer\u2019s therapeutic resistance, ablative, and computational modeling strategies as a means for improving therapeutic outcome. Technol Cancer Res Treat. 2018;17:1533033818762207.","journal-title":"Technol Cancer Res Treat."},{"issue":"9","key":"2094_CR15","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1016\/j.ctrv.2015.05.009","volume":"41","author":"NR Datta","year":"2015","unstructured":"Datta NR, Ordonez SG, Gaipl US, et al. Local hyperthermia combined with radiotherapy and-\/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev. 2015;41(9):742\u201353.","journal-title":"Cancer Treat Rev"},{"issue":"5","key":"2094_CR16","doi-asserted-by":"publisher","first-page":"1025","DOI":"10.1016\/j.ultrasmedbio.2018.12.007","volume":"45","author":"L Zhu","year":"2019","unstructured":"Zhu L, Altman MB, Laszlo A, et al. Ultrasound hyperthermia technology for radiosensitization. Ultrasound Med Biol. 2019;45(5):1025\u201343.","journal-title":"Ultrasound Med Biol"},{"issue":"1","key":"2094_CR17","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1148\/radiol.2018181445","volume":"291","author":"MD Gray","year":"2019","unstructured":"Gray MD, Lyon PC, Mannaris C, et al. Focused ultrasound hyperthermia for targeted drug release from thermosensitive liposomes: results from a phase i trial. Radiology. 2019;291(1):232\u20138.","journal-title":"Radiology"},{"issue":"6","key":"2094_CR18","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1097\/00004728-199211000-00024","volume":"16","author":"HE Cline","year":"1992","unstructured":"Cline HE, Schenck JF, Hynynen K, et al. MR-guided focused ultrasound surgery. J Comput Assist Tomogr. 1992;16(6):956\u201365.","journal-title":"J Comput Assist Tomogr"},{"issue":"4","key":"2094_CR19","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1038\/nrc1591","volume":"5","author":"JE Kennedy","year":"2005","unstructured":"Kennedy JE. High-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer. 2005;5(4):321\u20137.","journal-title":"Nat Rev Cancer"},{"issue":"2","key":"2094_CR20","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1118\/1.1634909","volume":"31","author":"D Melodelima","year":"2004","unstructured":"Melodelima D, Salomir R, Mougenot C, et al. Intraluminal ultrasound applicator compatible with magnetic resonance imaging \u201creal-time\u201d temperature mapping for the treatment of oesophageal tumours: an ex vivo study. Med Phys. 2004;31(2):236\u201344.","journal-title":"Med Phys"},{"issue":"6","key":"2094_CR21","doi-asserted-by":"publisher","first-page":"1065","DOI":"10.1002\/mrm.10176","volume":"47","author":"B Quesson","year":"2002","unstructured":"Quesson B, Vimeux F, Salomir R, et al. Automatic control of hyperthermic therapy based on real-time Fourier analysis of MR temperature maps. Magn Reson Med. 2002;47(6):1065\u201372.","journal-title":"Magn Reson Med"},{"issue":"4","key":"2094_CR22","first-page":"737","volume":"11","author":"CT Moonen","year":"2001","unstructured":"Moonen CT, Quesson B, Salomir R, et al. Thermal therapies in interventional MR imaging. Focused ultrasound. Neuroimaging Clin N Am. 2001;11(4):737\u201347.","journal-title":"Neuroimaging Clin N Am."},{"issue":"3","key":"2094_CR23","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1002\/(SICI)1522-2594(200003)43:3<342::AID-MRM4>3.0.CO;2-6","volume":"43","author":"R Salomir","year":"2000","unstructured":"Salomir R, Vimeux FC, de Zwart JA, et al. Hyperthermia by MR-guided focused ultrasound: accurate temperature control based on fast MRI and a physical model of local energy deposition and heat conduction. Magn Reson Med. 2000;43(3):342\u20137.","journal-title":"Magn Reson Med"},{"issue":"1","key":"2094_CR24","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1148\/radiol.11111189","volume":"263","author":"R Staruch","year":"2012","unstructured":"Staruch R, Chopra R, Hynynen K. Hyperthermia in bone generated with MR imaging-controlled focused ultrasound: control strategies and drug delivery. Radiology. 2012;263(1):117\u201327.","journal-title":"Radiology"},{"issue":"4","key":"2094_CR25","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1111\/1754-9485.12085","volume":"57","author":"S Ellis","year":"2013","unstructured":"Ellis S, Rieke V, Kohi M, Westphalen AC. Clinical applications for magnetic resonance guided high intensity focused ultrasound (MRgHIFU): present and future. J Med Imaging Radiat Oncol. 2013;57(4):391\u20139.","journal-title":"J Med Imaging Radiat Oncol."},{"issue":"1","key":"2094_CR26","doi-asserted-by":"publisher","first-page":"6","DOI":"10.3109\/02656736.2013.844366","volume":"30","author":"ST Heijkoop","year":"2014","unstructured":"Heijkoop ST, van Doorn HC, Stalpers LJ, et al. Results of concurrent chemotherapy and hyperthermia in patients with recurrent cervical cancer after previous chemoradiation. Int J Hyperthermia. 2014;30(1):6\u201310.","journal-title":"Int J Hyperthermia."},{"issue":"13","key":"2094_CR27","doi-asserted-by":"publisher","first-page":"3079","DOI":"10.1200\/JCO.2005.05.520","volume":"23","author":"EL Jones","year":"2005","unstructured":"Jones EL, Oleson JR, Prosnitz LR, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol. 2005;23(13):3079\u201385.","journal-title":"J Clin Oncol"},{"issue":"2","key":"2094_CR28","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1016\/S0360-3016(97)00731-1","volume":"40","author":"PK Sneed","year":"1998","unstructured":"Sneed PK, Stauffer PR, McDermott MW, et al. Survival benefit of hyperthermia in a prospective randomized trial of brachytherapy boost\u2009\u00b1\u2009hyperthermia for glioblastoma multiforme. Int J Radiat Oncol Biol Phys. 1998;40(2):287\u201395.","journal-title":"Int J Radiat Oncol Biol Phys"},{"key":"2094_CR29","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1146\/annurev.med.60.041707.170303","volume":"60","author":"FA Jolesz","year":"2009","unstructured":"Jolesz FA. MRI-guided focused ultrasound surgery. Annu Rev Med. 2009;60:417\u201330.","journal-title":"Annu Rev Med"},{"issue":"6","key":"2094_CR30","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1097\/RLI.0b013e318285bbab","volume":"48","author":"A Napoli","year":"2013","unstructured":"Napoli A, Anzidei M, Marincola BC, et al. Primary pain palliation and local tumor control in bone metastases treated with magnetic resonance-guided focused ultrasound. Invest Radiol. 2013;48(6):351\u20138.","journal-title":"Invest Radiol"},{"issue":"5","key":"2094_CR31","doi-asserted-by":"publisher","first-page":"1418","DOI":"10.1002\/jmri.25676","volume":"46","author":"MD Bucknor","year":"2017","unstructured":"Bucknor MD, Ozhinsky E, Shah R, et al. Effect of sonication duration and power on ablation depth during MR-guided focused ultrasound of bone. J Magn Reson Imaging. 2017;46(5):1418\u201322.","journal-title":"J Magn Reson Imaging"},{"issue":"5","key":"2094_CR32","doi-asserted-by":"publisher","first-page":"1174","DOI":"10.1002\/jmri.24451","volume":"40","author":"MD Bucknor","year":"2014","unstructured":"Bucknor MD, Rieke V, Do L, et al. MRI-guided high-intensity focused ultrasound ablation of bone: evaluation of acute findings with MR and CT imaging in a swine model. J Magn Reson Imaging. 2014;40(5):1174\u201380.","journal-title":"J Magn Reson Imaging"},{"issue":"3","key":"2094_CR33","doi-asserted-by":"publisher","first-page":"967","DOI":"10.1148\/radiol.10090374","volume":"255","author":"W Chen","year":"2010","unstructured":"Chen W, Zhu H, Zhang L, et al. Primary bone malignancy: effective treatment with high-intensity focused ultrasound ablation. Radiology. 2010;255(3):967\u201378.","journal-title":"Radiology"},{"issue":"1","key":"2094_CR34","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/j.bone.2013.06.032","volume":"57","author":"A Herman","year":"2013","unstructured":"Herman A, Avivi E, Brosh T, et al. Biomechanical properties of bone treated by magnetic resonance-guided focused ultrasound\u2014an in vivo porcine model study. Bone. 2013;57(1):92\u20137.","journal-title":"Bone"},{"issue":"10","key":"2094_CR35","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1016\/S0301-5629(01)00454-9","volume":"27","author":"NB Smith","year":"2001","unstructured":"Smith NB, Temkin JM, Shapiro F, Hynynen K. Thermal effects of focused ultrasound energy on bone tissue. Ultrasound Med Biol. 2001;27(10):1427\u201333.","journal-title":"Ultrasound Med Biol"},{"key":"2094_CR36","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s40349-015-0033-8","volume":"3","author":"SY Yeo","year":"2015","unstructured":"Yeo SY, Arias Moreno AJ, van Rietbergen B, et al. Effects of magnetic resonance-guided high-intensity focused ultrasound ablation on bone mechanical properties and modeling. J Ther Ultrasound. 2015;3:13.","journal-title":"J Ther Ultrasound."},{"issue":"7","key":"2094_CR37","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1097\/01.ajp.0000210902.67849.e6","volume":"22","author":"KG Halvorson","year":"2006","unstructured":"Halvorson KG, Sevcik MA, Ghilardi JR, et al. Similarities and differences in tumor growth, skeletal remodeling and pain in an osteolytic and osteoblastic model of bone cancer. Clin J Pain. 2006;22(7):587\u2013600.","journal-title":"Clin J Pain"},{"issue":"4","key":"2094_CR38","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/nrc2618","volume":"9","author":"JA Joyce","year":"2009","unstructured":"Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239\u201352.","journal-title":"Nat Rev Cancer"},{"issue":"Suppl 1","key":"2094_CR39","doi-asserted-by":"publisher","first-page":"S54","DOI":"10.1016\/j.pain.2013.07.044","volume":"154","author":"P Mantyh","year":"2013","unstructured":"Mantyh P. Bone cancer pain: causes, consequences, and therapeutic opportunities. Pain. 2013;154(Suppl 1):S54\u201362.","journal-title":"Pain"},{"issue":"2","key":"2094_CR40","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1007\/s00774-006-0734-8","volume":"25","author":"M Nagae","year":"2007","unstructured":"Nagae M, Hiraga T, Yoneda T. Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J Bone Miner Metab. 2007;25(2):99\u2013104.","journal-title":"J Bone Miner Metab"},{"issue":"4","key":"2094_CR41","doi-asserted-by":"publisher","first-page":"421","DOI":"10.3109\/02656736.2015.1009501","volume":"31","author":"L Petrusca","year":"2015","unstructured":"Petrusca L, Salomir R, Manasseh G, et al. Spatio-temporal quantitative thermography of pre-focal interactions between high intensity focused ultrasound and the rib cage. Int J Hyperthermia. 2015;31(4):421\u201332.","journal-title":"Int J Hyperthermia."},{"issue":"1","key":"2094_CR42","first-page":"15","volume":"3","author":"MA Sabino","year":"2005","unstructured":"Sabino MA, Mantyh PW. Pathophysiology of bone cancer pain. J Support Oncol. 2005;3(1):15\u201324.","journal-title":"J Support Oncol."},{"issue":"2","key":"2094_CR43","first-page":"137","volume":"100","author":"WT Chen","year":"2001","unstructured":"Chen WT, Shih TT, Shih LS, et al. Paget\u2019s disease of the bone: a case report. J Formos Med Assoc. 2001;100(2):137\u201341.","journal-title":"J Formos Med Assoc"},{"key":"2094_CR44","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/2050-5736-2-16","volume":"2","author":"M Huisman","year":"2014","unstructured":"Huisman M, Lam MK, Bartels LW, et al. Feasibility of volumetric MRI-guided high intensity focused ultrasound (MR-HIFU) for painful bone metastases. J Ther Ultrasound. 2014;2:16.","journal-title":"J Ther Ultrasound."},{"key":"2094_CR45","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1093\/jnci\/dju082","volume":"106","author":"MD Hurwitz","year":"2014","unstructured":"Hurwitz MD, Ghanouni P, Kanaev SV, et al. Magnetic resonance-guided focused ultrasound for patients with painful bone metastases: phase III trial results. J Natl Cancer Inst. 2014;106:5.","journal-title":"J Natl Cancer Inst."},{"issue":"1","key":"2094_CR46","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1245\/s10434-008-0011-2","volume":"16","author":"B Liberman","year":"2009","unstructured":"Liberman B, Gianfelice D, Inbar Y, et al. Pain palliation in patients with bone metastases using MR-guided focused ultrasound surgery: a multicenter study. Ann Surg Oncol. 2009;16(1):140\u20136.","journal-title":"Ann Surg Oncol"},{"issue":"12","key":"2094_CR47","doi-asserted-by":"publisher","first-page":"1102","DOI":"10.4161\/cbt.8.12.8556","volume":"8","author":"C Li","year":"2009","unstructured":"Li C, Wu P, Zhang L, et al. Osteosarcoma: limb salvaging treatment by ultrasonographically guided high-intensity focused ultrasound. Cancer Biol Ther. 2009;8(12):1102\u20138.","journal-title":"Cancer Biol Ther"},{"issue":"1","key":"2094_CR48","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.suronc.2014.10.001","volume":"24","author":"W Yu","year":"2015","unstructured":"Yu W, Tang L, Lin F, et al. High-intensity focused ultrasound: noninvasive treatment for local unresectable recurrence of osteosarcoma. Surg Oncol. 2015;24(1):9\u201315.","journal-title":"Surg Oncol"},{"key":"2094_CR49","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1186\/s13014-016-0592-z","volume":"11","author":"J Crezee","year":"2016","unstructured":"Crezee J, van Leeuwen CM, Oei AL, et al. Biological modelling of the radiation dose escalation effect of regional hyperthermia in cervical cancer. Radiat Oncol. 2016;11:14.","journal-title":"Radiat Oncol."},{"issue":"2","key":"2094_CR50","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1080\/02656730010001333","volume":"17","author":"Y Harima","year":"2001","unstructured":"Harima Y, Nagata K, Harima K, et al. A randomized clinical trial of radiation therapy versus thermoradiotherapy in stage IIIB cervical carcinoma. Int J Hyperthermia. 2001;17(2):97\u2013105.","journal-title":"Int J Hyperthermia."},{"issue":"4","key":"2094_CR51","doi-asserted-by":"publisher","first-page":"492","DOI":"10.4103\/0973-1482.77101","volume":"6","author":"NG Huilgol","year":"2010","unstructured":"Huilgol NG, Gupta S, Sridhar CR. Hyperthermia with radiation in the treatment of locally advanced head and neck cancer: a report of randomized trial. J Cancer Res Ther. 2010;6(4):492\u20136.","journal-title":"J Cancer Res Ther."},{"issue":"3","key":"2094_CR52","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1007\/s10147-006-0647-5","volume":"12","author":"M Mitsumori","year":"2007","unstructured":"Mitsumori M, Zeng ZF, Oliynychenko P, et al. Regional hyperthermia combined with radiotherapy for locally advanced non-small cell lung cancers: a multi-institutional prospective randomized trial of the International Atomic Energy Agency. Int J Clin Oncol. 2007;12(3):192\u20138.","journal-title":"Int J Clin Oncol."},{"issue":"5","key":"2094_CR53","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1080\/02656730903091986","volume":"25","author":"J Overgaard","year":"2009","unstructured":"Overgaard J, Gonzalez D, Hulshof MC, et al. Hyperthermia as an adjuvant to radiation therapy of recurrent or metastatic malignant melanoma. A multicentre randomized trial by the European Society for Hyperthermic Oncology. Int J Hyperthermia. 2009;25(5):323\u201334.","journal-title":"Int J Hyperthermia."},{"key":"2094_CR54","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/s40349-018-0115-5","volume":"6","author":"E Ozhinsky","year":"2018","unstructured":"Ozhinsky E, Salgaonkar VA, Diederich CJ, Rieke V. MR thermometry-guided ultrasound hyperthermia of user-defined regions using the ExAblate prostate ablation array. J Ther Ultrasound. 2018;6:7.","journal-title":"J Ther Ultrasound."},{"key":"2094_CR55","doi-asserted-by":"publisher","first-page":"3","DOI":"10.3390\/cancers11030348","volume":"11","author":"V Carina","year":"2019","unstructured":"Carina V, Costa V, Sartori M, et al. Adjuvant biophysical therapies in osteosarcoma. Cancers (Basel). 2019;11:3.","journal-title":"Cancers (Basel)."},{"issue":"7","key":"2094_CR56","doi-asserted-by":"publisher","first-page":"1473","DOI":"10.1002\/jcp.24302","volume":"228","author":"SC Genet","year":"2013","unstructured":"Genet SC, Fujii Y, Maeda J, et al. Hyperthermia inhibits homologous recombination repair and sensitizes cells to ionizing radiation in a time- and temperature-dependent manner. J Cell Physiol. 2013;228(7):1473\u201381.","journal-title":"J Cell Physiol"},{"issue":"11","key":"2094_CR57","doi-asserted-by":"publisher","first-page":"3872","DOI":"10.1158\/0008-5472.CAN-10-4482","volume":"71","author":"A Sen","year":"2011","unstructured":"Sen A, Capitano ML, Spernyak JA, et al. Mild elevation of body temperature reduces tumor interstitial fluid pressure and hypoxia and enhances efficacy of radiotherapy in murine tumor models. Cancer Res. 2011;71(11):3872\u201380.","journal-title":"Cancer Res"},{"key":"2094_CR58","doi-asserted-by":"publisher","first-page":"e1633","DOI":"10.1038\/cddis.2015.12","volume":"6","author":"A Morle","year":"2015","unstructured":"Morle A, Garrido C, Micheau O. Hyperthermia restores apoptosis induced by death receptors through aggregation-induced c-FLIP cytosolic depletion. Cell Death Dis. 2015;6:e1633.","journal-title":"Cell Death Dis."},{"issue":"10","key":"2094_CR59","doi-asserted-by":"publisher","first-page":"1765","DOI":"10.1016\/j.yexcr.2006.02.008","volume":"312","author":"M Moulin","year":"2006","unstructured":"Moulin M, Arrigo AP. Long lasting heat shock stimulation of TRAIL-induced apoptosis in transformed T lymphocytes. Exp Cell Res. 2006;312(10):1765\u201384.","journal-title":"Exp Cell Res"},{"issue":"1","key":"2094_CR60","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1148\/radiology.148.1.6344136","volume":"148","author":"CT Coughlin","year":"1983","unstructured":"Coughlin CT, Douple EB, Strohbehn JW, et al. Interstitial hyperthermia in combination with brachytherapy. Radiology. 1983;148(1):285\u20138.","journal-title":"Radiology"},{"issue":"6","key":"2094_CR61","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1016\/S1470-2045(10)70071-1","volume":"11","author":"RD Issels","year":"2010","unstructured":"Issels RD, Lindner LH, Verweij J, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: a randomised phase 3 multicentre study. Lancet Oncol. 2010;11(6):561\u201370.","journal-title":"Lancet Oncol."},{"issue":"1","key":"2094_CR62","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1016\/j.ijrobp.2017.09.030","volume":"100","author":"MS Chi","year":"2018","unstructured":"Chi MS, Yang KL, Chang YC, et al. Comparing the effectiveness of combined external beam radiation and hyperthermia versus external beam radiation alone in treating patients with painful bony metastases: a phase 3 prospective, randomized, controlled trial. Int J Radiat Oncol Biol Phys. 2018;100(1):78\u201387.","journal-title":"Int J Radiat Oncol Biol Phys"},{"issue":"3","key":"2094_CR63","doi-asserted-by":"publisher","first-page":"162","DOI":"10.4103\/0973-1482.19596","volume":"1","author":"S Hede","year":"2005","unstructured":"Hede S, Trivedi N, Mekala A, Huilgol N. Thermometry studies of radio-frequency induced hyperthermia on hydrogel based neck phantoms. J Cancer Res Ther. 2005;1(3):162\u20137.","journal-title":"J Cancer Res Ther."},{"key":"2094_CR64","doi-asserted-by":"publisher","first-page":"518787","DOI":"10.1155\/2014\/518787","volume":"2014","author":"I Saletes","year":"2014","unstructured":"Saletes I, Gilles B, Auboiroux V, et al. In vitro demonstration of focused ultrasound thrombolysis using bifrequency excitation. Biomed Res Int. 2014;2014:518787.","journal-title":"Biomed Res Int"},{"issue":"2","key":"2094_CR65","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/0301-5629(91)90123-E","volume":"17","author":"K Hynynen","year":"1991","unstructured":"Hynynen K. The threshold for thermally significant cavitation in dog\u2019s thigh muscle in vivo. Ultrasound Med Biol. 1991;17(2):157\u201369.","journal-title":"Ultrasound Med Biol"},{"key":"2094_CR66","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1186\/s40349-016-0073-8","volume":"4","author":"E Ozhinsky","year":"2016","unstructured":"Ozhinsky E, Han M, Bucknor M, et al. T2-based temperature monitoring in bone marrow for MR-guided focused ultrasound. J Ther Ultrasound. 2016;4:26.","journal-title":"J Ther Ultrasound."},{"issue":"5","key":"2094_CR67","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1002\/jmri.25064","volume":"43","author":"M Parmala","year":"2016","unstructured":"Parmala M, Eriksson M, Rytioja M, et al. Temperature measurement in human fat with T2 imaging. J Magn Reson Imaging. 2016;43(5):1171\u20138.","journal-title":"J Magn Reson Imaging"},{"key":"2094_CR68","doi-asserted-by":"publisher","first-page":"927","DOI":"10.1039\/C8TB01491D","volume":"7","author":"S Desgranges","year":"2019","unstructured":"Desgranges S, Lorton O, Gui-Levy L, et al. Micron-sized PFOB liquid core droplets stabilized with tailored-made perfluorinated surfactants as a new class of endovascular sono-sensitizers for focused ultrasound thermotherapy. J Mater Chem. 2019;7:927\u201339.","journal-title":"J Mater Chem"},{"issue":"2","key":"2094_CR69","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/S0301-5629(00)00304-5","volume":"27","author":"KV Ramnarine","year":"2001","unstructured":"Ramnarine KV, Anderson T, Hoskins PR. Construction and geometric stability of physiological flow rate wall-less stenosis phantoms. Ultrasound Med Biol. 2001;27(2):245\u201350.","journal-title":"Ultrasound Med Biol"},{"issue":"6","key":"2094_CR70","doi-asserted-by":"publisher","first-page":"1324","DOI":"10.1109\/TMI.2014.2310704","volume":"33","author":"L Petrusca","year":"2014","unstructured":"Petrusca L, Auboiroux V, Goget T, et al. A nonparametric temperature controller with nonlinear negative reaction for multi-point rapid MR-guided HIFU ablation. IEEE Trans Med Imaging. 2014;33(6):1324\u201337.","journal-title":"IEEE Trans Med Imaging"},{"issue":"10","key":"2094_CR71","doi-asserted-by":"publisher","first-page":"4726","DOI":"10.1118\/1.3215534","volume":"36","author":"R Salomir","year":"2009","unstructured":"Salomir R, Rata M, Cadis D, et al. Endocavitary thermal therapy by MRI-guided phased-array contact ultrasound: experimental and numerical studies on the multi-input single-output PID temperature controller\u2019s convergence and stability. Med Phys. 2009;36(10):4726\u201341.","journal-title":"Med Phys"},{"issue":"1","key":"2094_CR72","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1118\/1.3668316","volume":"39","author":"G Pinton","year":"2012","unstructured":"Pinton G, Aubry JF, Bossy E, et al. Attenuation, scattering, and absorption of ultrasound in the skull bone. Med Phys. 2012;39(1):299\u2013307.","journal-title":"Med Phys"},{"key":"2094_CR73","first-page":"716","volume":"70","author":"Y Ken","year":"2014","unstructured":"Ken Y. Visualization of acoustic evanescent waves by photoelastic method. Phys Procedia. 2014;70:716\u201320.","journal-title":"Phys Procedia"},{"issue":"1","key":"2094_CR74","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1093\/annonc\/mdl335","volume":"18","author":"R Catane","year":"2007","unstructured":"Catane R, Beck A, Inbar Y, et al. MR-guided focused ultrasound surgery (MRgFUS) for the palliation of pain in patients with bone metastases\u2013preliminary clinical experience. Ann Oncol. 2007;18(1):163\u20137.","journal-title":"Ann Oncol"},{"issue":"4","key":"2094_CR75","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1080\/02656730600609122","volume":"22","author":"Z Liu","year":"2006","unstructured":"Liu Z, Ahmed M, Weinstein Y, et al. Characterization of the RF ablation-induced \u2018oven effect\u2019: the importance of background tissue thermal conductivity on tissue heating. Int J Hyperthermia. 2006;22(4):327\u201342.","journal-title":"Int J Hyperthermia."},{"issue":"2","key":"2094_CR76","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1148\/radiology.197.2.7480692","volume":"197","author":"DI Rosenthal","year":"1995","unstructured":"Rosenthal DI, Springfield DS, Gebhardt MC, et al. Osteoid osteoma: percutaneous radio-frequency ablation. Radiology. 1995;197(2):451\u20134.","journal-title":"Radiology"},{"issue":"1\u20132","key":"2094_CR77","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0304-3959(96)03267-8","volume":"69","author":"S Mercadante","year":"1997","unstructured":"Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain. 1997;69(1\u20132):1\u201318.","journal-title":"Pain"},{"issue":"5","key":"2094_CR78","doi-asserted-by":"publisher","first-page":"2380","DOI":"10.1118\/1.3377777","volume":"37","author":"AJ Krafft","year":"2010","unstructured":"Krafft AJ, Jenne JW, Maier F, et al. A long arm for ultrasound: a combined robotic focused ultrasound setup for magnetic resonance-guided focused ultrasound surgery. Med Phys. 2010;37(5):2380\u201393.","journal-title":"Med Phys"},{"issue":"6","key":"2094_CR79","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1016\/j.ultrasmedbio.2010.02.012","volume":"36","author":"MO Culjat","year":"2010","unstructured":"Culjat MO, Goldenberg D, Tewari P, Singh RS. A review of tissue substitutes for ultrasound imaging. Ultrasound Med Biol. 2010;36(6):861\u201373.","journal-title":"Ultrasound Med Biol"},{"issue":"10","key":"2094_CR80","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.1088\/0031-9155\/39\/10\/011","volume":"39","author":"AJ Clarke","year":"1994","unstructured":"Clarke AJ, Evans JA, Truscott JG, et al. A phantom for quantitative ultrasound of trabecular bone. Phys Med Biol. 1994;39(10):1677\u201387.","journal-title":"Phys Med Biol"},{"key":"2094_CR81","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1186\/1746-1596-1-35","volume":"1","author":"L Luo","year":"2006","unstructured":"Luo L, Molnar J, Ding H, et al. Ultrasound absorption and entropy production in biological tissue: a novel approach to anticancer therapy. Diagn Pathol. 2006;1:35.","journal-title":"Diagn Pathol."}],"container-title":["Journal of Translational Medicine"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12967-019-2094-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12967-019-2094-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12967-019-2094-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,10,22]],"date-time":"2020-10-22T23:12:25Z","timestamp":1603408345000},"score":1,"resource":{"primary":{"URL":"https:\/\/translational-medicine.biomedcentral.com\/articles\/10.1186\/s12967-019-2094-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,24]]},"references-count":81,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["2094"],"URL":"https:\/\/doi.org\/10.1186\/s12967-019-2094-x","relation":{},"ISSN":["1479-5876"],"issn-type":[{"value":"1479-5876","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,24]]},"assertion":[{"value":"22 May 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 October 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 October 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Not applicable.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"350"}}