Abstract
Extracorporeal high-intensity focused ultrasound (HIFU) is a minimally invasive therapy considered with increased interest for the ablation of small tumors in deeply located organs while sparing surrounding critical tissues. A multitude of preclinical and clinical studies have showed the feasibility of the method; however, concurrently they showed several obstacles, among which the management of respiratory motion of abdominal organs is at the forefront. The aim of this review is to describe the different methods that have been proposed for managing respiratory motion and to identify their advantages and weaknesses. First, we specify the characteristics of respiratory motion for the liver, kidneys, and pancreas and the problems it causes during HIFU planning, treatment, and monitoring. Second, we make an inventory of the preclinical and clinical approaches used to overcome the problem of organ motion. Third, we analyze their respective benefits and drawbacks to identify the remaining physical, technological, and clinical challenges. We thereby consider the outlook of motion compensation techniques and those that would be the most suitable for clinical use, particularly under magnetic resonance thermometry monitoring.
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References
Lele PP (1962) A simple method for production of trackless focal lesions with focused ultrasound: physical factors. J Physiol 160:494–512
Lynn JG, Zwemer RL, Chick AJ, Miller AE (1942) A new method for the generation and use of focused ultrasound in experimental biology. J Gen Physiol 26(2):179–193
Nomura T, Mimata H (2012) Focal therapy in the management of prostate cancer: an emerging approach for localized prostate cancer. Adv Urol 39:14–37
Crouzet S, Murat FJ, Pasticier G, Cassier P, Chapelon JY, Gelet A (2010) High intensity focused ultrasound (HIFU) for prostate cancer: current clinical status, outcomes and future perspectives. Int J Hyperthermia 26(8):796–803
Hesley GK, Gorny KR, Woodrum DA (2013) MR-guided focused ultrasound for the treatment of uterine fibroids. Cardiovasc Intervent Radiol 36(1):5–13
Gianfelice D, Gupta C, Kucharczyk W, Bret P, Havill D, Clemons M (2008) Palliative treatment of painful bone metastases with MR imaging-guided focused ultrasound. Radiology 249(1):355–363
Bradley WG Jr (2009) MR-guided focused ultrasound: a potentially disruptive technology. J Am Coll Radiol 6(7):510–513
Hill CR, ter Haar GR (1995) Review article: high intensity focused ultrasound–potential for cancer treatment. Br J Radiol 68(816):1296–1303
Taylor KJ, Connolly CC (1969) Differing hepatic lesions caused by the same dose of ultrasound. J Pathol 98(4):291–293
Vallancien G, Chartier-Kastler E, Harouni M, Chopin D, Bougaran J (1993) Focused extracorporeal pyrotherapy: experimental study and feasibility in man. Semin Urol 11(1):7–9
Kohrmann KU, Michel MS, Gaa J, Marlinghaus E, Alken P (2002) High intensity focused ultrasound as noninvasive therapy for multilocal renal cell carcinoma: case study and review of the literature. J Urol 167(6):2397–2403
Wu F, Wang ZB, Chen WZ, Bai J, Zhu H, Qiao TY (2003) Preliminary experience using high intensity focused ultrasound for the treatment of patients with advanced stage renal malignancy. J Urol 170(6 Pt 1):2237–2240
Wu F, Wang ZB, Zhu H, Chen WZ, Zou JZ, Bai J et al (2005) Feasibility of US-guided high-intensity focused ultrasound treatment in patients with advanced pancreatic cancer: initial experience. Radiology 236(3):1034–1040
Orgera G, Krokidis M, Monfardini L, Bonomo G, Della Vigna P, Fazio N et al (2011) High intensity focused ultrasound ablation of pancreatic neuroendocrine tumours: report of two cases. Cardiovasc Intervent Radiol 34(2):419–423
Huisman M, van den Bosch MA (2011) MR-guided high-intensity focused ultrasound for noninvasive cancer treatment. Cancer Imaging 11:S161–S166
Zhou YF (2011) High intensity focused ultrasound in clinical tumor ablation. World J Clin Oncol 2(1):8–27
Terraz S, Cernicanu A, Lepetit-Coiffe M, Viallon M, Salomir R, Mentha G et al (2010) Radiofrequency ablation of small liver malignancies under magnetic resonance guidance: progress in targeting and preliminary observations with temperature monitoring. Eur Radiol 20(4):886–897
Allen M, Rivens I, Visioli A, Ter Haar G (2002) Focused ultrasound surgery (FUS): A noninvasive technique for the thermal ablation of liver metastases. In: Ultrasound. PnIST, pp 17–25
Sapareto SA, Dewey WC (1984) Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 10(6):787–800
Auboiroux V, Petrusca L, Viallon M, Goget T, Becker C, Salomir R (2012) Ultrasonography-based 2D motion-compensated HIFU sonication integrated with reference-free MR temperature monitoring: a feasibility study ex vivo. Phys Med Biol 57(10):N159–N171
Ritchie RW, Leslie T, Phillips R, Wu F, Illing R, ter Haar G et al (2010) Extracorporeal high intensity focused ultrasound for renal tumours: a 3-year follow-up. BJU Int 106(7):1004–1009
Jung SE, Cho SH, Jang JH, Han JY (2011) High-intensity focused ultrasound ablation in hepatic and pancreatic cancer: complications. Abdom Imaging 36(2):185–195
Jolesz FA, McDannold N (2008) Current status and future potential of MRI-guided focused ultrasound surgery. J Magn Reson Imaging 27(2):319–391
Voogt MJ, Trillaud H, Kim YS, Mali WP, Barkhausen J, Bartels LW et al (2012) Volumetric feedback ablation of uterine fibroids using magnetic resonance-guided high intensity focused ultrasound therapy. Eur Radiol 22(2):411–417
Rieke V, Vigen KK, Sommer G, Daniel BL, Pauly JM, Butts K (2004) Referenceless PRF shift thermometry. Magn Reson Med 51(6):1223–1231
Salomir R, Viallon M, Kickhefel A, Roland J, Morel DR, Petrusca L et al (2012) Reference-free PRFS MR-thermometry using near-harmonic 2-D reconstruction of the background phase. IEEE Trans Med Imaging 31(2):287–301
Wade OL (1954) Movements of the thoracic cage and diaphragm in respiration. J Physiol 124(2):193–212
Suramo I, Paivansalo M, Myllyla V (1984) Cranio-caudal movements of the liver, pancreas and kidneys in respiration. Acta Radiol Diagn (Stockh) 25(2):129–131
Bryan PJ, Custar S, Haaga JR, Balsara V (1984) Respiratory movement of the pancreas: an ultrasonic study. J Ultrasound Med 3(7):317–320
Davies SC, Hill AL, Holmes RB, Halliwell M, Jackson PC (1994) Ultrasound quantitation of respiratory organ motion in the upper abdomen. Br J Radiol 67(803):1096–1102
Brandner ED, Wu A, Chen H, Heron D, Kalnicki S, Komanduri K et al (2006) Abdominal organ motion measured using 4D CT. Int J Radiat Oncol Biol Phys 65(2):554–560
Hallman JL, Mori S, Sharp GC, Lu HM, Hong TS, Chen GT (2012) A four-dimensional computed tomography analysis of multiorgan abdominal motion. Int J Radiat Oncol Biol Phys 83(1):435–441
Korin HW, Ehman RL, Riederer SJ, Felmlee JP, Grimm RC (1992) Respiratory kinematics of the upper abdominal organs: a quantitative study. Magn Reson Med 23(1):172–178
von Siebenthal M, Szekely G, Gamper U, Boesiger P, Lomax A, Cattin P (2007) 4D MR imaging of respiratory organ motion and its variability. Phys Med Biol 52(6):1547–1564
de Senneville BD, Ries M, Maclair G, Moonen C (2011) MR-guided thermotherapy of abdominal organs using a robust PCA-based motion descriptor. IEEE Trans Med Imaging 30(11):1987–1995
Bhasin DK, Rana SS, Jahagirdar S, Nagi B (2006) Does the pancreas move with respiration? J Gastroenterol Hepatol 21(9):1424–1427
Xi M, Liu MZ, Li QQ, Cai L, Zhang L, Hu YH (2009) Analysis of abdominal organ motion using four-dimensional CT. Ai Zheng 28(9):989–993
Pai Panandiker AS, Sharma S, Naik MH, Wu S, Hua C, Beltran C et al (2012) Novel assessment of renal motion in children as measured via four-dimensional computed tomography. Int J Radiat Oncol Biol Phys 82(5):1771–1776
Kim YS, Park SH, Ahn SD, Lee JE, Choi EK, Lee SW et al (2007) Differences in abdominal organ movement between supine and prone positions measured using four-dimensional computed tomography. Radiother Oncol 85(3):424–428
Gwynne S, Wills L, Joseph G, John G, Staffurth J, Hurt C et al (2009) Respiratory movement of upper abdominal organs and its effect on radiotherapy planning in pancreatic cancer. Clin Oncol (R Coll Radiol) 21(9):713–719
von Siebenthal M, Szekely G, Lomax AJ, Cattin PC (2007) Systematic errors in respiratory gating due to intrafraction deformations of the liver. Med Phys 34(9):3620–3629
Wu F, Wang ZB, Chen WZ, Zou JZ, Bai J, Zhu H et al (2005) Advanced hepatocellular carcinoma: treatment with high-intensity focused ultrasound ablation combined with transcatheter arterial embolization. Radiology 235(2):659–667
Keall PJ, Mageras GS, Balter JM, Emery RS, Forster KM, Jiang SB et al (2006) The management of respiratory motion in radiation oncology report of AAPM Task Group 76. Med Phys 33(10):3874–3900
Okada A, Murakami T, Mikami K, Onishi H, Tanigawa N, Marukawa T et al (2006) A case of hepatocellular carcinoma treated by MR-guided focused ultrasound ablation with respiratory gating. Magn Reson Med Sci 5(3):167–171
Kubo HD, Len PM, Minohara S, Mostafavi H (2000) Breathing-synchronized radiotherapy program at the University of California Davis Cancer Center. Med Phys 27(2):346–353
de Zwart JA, Vimeux FC, Palussiere J, Salomir R, Quesson B, Delalande C et al (2001) On-line correction and visualization of motion during MRI-controlled hyperthermia. Magn Reson Med 45(1):128–137
Park M, Jung S, Cho S, Piao X, Hahn S, Han J et al (2009) Preliminary experience using high intensity focused ultrasound for treating liver metastasis from colon and stomach cancer. Int J Hyperthermia 25(3):180–188
Auboiroux V, Viallon M, Roland J, Hyacinthe JN, Petrusca L, Morel DR et al (2012) ARFI-prepared MRgHIFU in liver: simultaneous mapping of ARFI-displacement and temperature elevation, using a fast GRE-EPI sequence. Magn Reson Med 68(3):932–946
Illing RO, Kennedy JE, Wu F, ter Haar GR, Protheroe AS, Friend PJ et al (2005) The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a Western population. Br J Cancer 93(8):890–895
Biro P, Eyrich G, Rohling RG (1998) The efficiency of CO2 elimination during high-frequency jet ventilation for laryngeal microsurgery. Anesth Analg 87(1):180–184
Abderhalden S, Biro P, Hechelhammer L, Pfiffner R, Pfammatter T (2011) CT-guided navigation of percutaneous hepatic and renal radiofrequency ablation under high-frequency jet ventilation: feasibility study. J Vasc Interv Radiol 22(9):1275–1278
Evans E, Biro P, Bedforth N (2007) Jet ventilation. Contin Educ Anaesth Crit Care Pain 7(1):2–5
Yin F, Kim JG, Haughton C, Brown SL, Ajlouni M, Stronati M et al (2001) Extracranial radiosurgery: immobilizing liver motion in dogs using high-frequency jet ventilation and total intravenous anesthesia. Int J Radiat Oncol Biol Phys 49(1):211–216
Fritz P, Kraus HJ, Dolken W, Muhlnickel W, Muller-Nolte F, Hering W (2006) Technical note: gold marker implants and high-frequency jet ventilation for stereotactic, single-dose irradiation of liver tumors. Technol Cancer Res Treat 5(1):9–14
Warner MA, Warner ME, Buck CF, Segura JW (1988) Clinical efficacy of high frequency jet ventilation during extracorporeal shock wave lithotripsy of renal and ureteral calculi: a comparison with conventional mechanical ventilation. J Urol 139(3):486–487
Mucksavage P, Mayer WA, Mandel JE, Van Arsdalen KN (2010) High-frequency jet ventilation is beneficial during shock wave lithotripsy utilizing a newer unit with a narrower focal zone. Can Urol Assoc J 4(5):333–335
Biro P, Spahn DR, Pfammatter T (2009) High-frequency jet ventilation for minimizing breathing-related liver motion during percutaneous radiofrequency ablation of multiple hepatic tumours. Br J Anaesth 102(5):650–653
Holbrook AB, Ghanouni P, Santos JM, Dumoulin C, Medan Y, Pauly KB (2013, March 4) Respiration based steering for high intensity focused ultrasound liver ablation. Magn Reson Med [Epub ahead of print]
Marquet F, Pernot M, Aubry JF, Tanter M, Montaldo G, Fink M (2006) In-vivo non-invasive motion tracking and correction in high intensity focused ultrasound therapy. Conf Proc IEEE Eng Med Biol Soc 1:688–691
Pernot M, Tanter M, Fink M (2004) 3-D real-time motion correction in high-intensity focused ultrasound therapy. Ultrasound Med Biol 30(9):1239–1249
Marquet F, Aubry JF, Pernot M, Fink M, Tanter M (2011) Optimal transcostal high-intensity focused ultrasound with combined real-time 3D movement tracking and correction. Phys Med Biol 56(22):7061–7080
de Senneville BD, Mougenot C, Moonen CT (2007) Real-time adaptive methods for treatment of mobile organs by MRI-controlled high-intensity focused ultrasound. Magn Reson Med 57(2):319–330
Tokuda J, Morikawa S, Haque HA, Tsukamoto T, Matsumiya K, Liao H et al (2008) Adaptive 4D MR imaging using navigator-based respiratory signal for MRI-guided therapy. Magn Reson Med 59(5):1051–1061
Kokuryo D, Kaihara T, Kumamoto E, Fujii S, Kuroda K (2007) Method for target tracking in focused ultrasound surgery of liver using magnetic resonance filtered venography. Conf Proc IEEE Eng Med Biol Soc 2007:2614–2617
Ries M, de Senneville BD, Roujol S, Berber Y, Quesson B, Moonen C (2010) Real-time 3D target tracking in MRI guided focused ultrasound ablations in moving tissues. Magn Reson Med 64(6):1704–1712
de Oliveira PL, de Senneville BD, Dragonu I, Moonen CT (2010) Rapid motion correction in MR-guided high-intensity focused ultrasound heating using real-time ultrasound echo information. NMR Biomed 23(9):1103–1108
Tang AM, Kacher DF, Lam EY, Wong KK, Jolesz FA, Yang ES (2008) Simultaneous ultrasound and MRI system for breast biopsy: compatibility assessment and demonstration in a dual modality phantom. IEEE Trans Med Imaging 27(2):247–254
Feinberg DA, Giese D, Bongers DA, Ramanna S, Zaitsev M, Markl M et al (2010) Hybrid ultrasound MRI for improved cardiac imaging and real-time respiration control. Magn Reson Med 63(2):290–296
Viallon M, Terraz S, Roland J, Dumont E, Becker CD, Salomir R (2010) Observation and correction of transient cavitation-induced PRFS thermometry artifacts during radiofrequency ablation, using simultaneous ultrasound/MR imaging. Med Phys 37(4):1491–1506
Cossmann PH (2012) Video-coaching as biofeedback tool to improve gated treatments: possibilities and limitations. Z Med Phys 22(3):224–230
Hacker A, Michel MS, Marlinghaus E, Kohrmann KU, Alken P (2006) Extracorporeally induced ablation of renal tissue by high-intensity focused ultrasound. BJU Int 97(4):779–785
Rijkhorst EJ, Rivens I, Haar G, Hawkes D, Barratt D (2011) Effects of respiratory liver motion on heating for gated and model-based motion-compensated high-intensity focused ultrasound ablation. Med Image Comput Comput Assist Interv 14(Pt 1):605–612
Visioli A, Rivens I, ter Haar G, Horwich A, Huddart R, Moskovic E et al (1999) Preliminary results of a phase I dose escalation clinical trial using focused ultrasound in the treatment of localised tumours. Eur J Ultrasound 9(1):11–18
Jenkins K, Baker AB (2003) Consent and anaesthetic risk. Anaesthesia 58(10):962–984
Li JJ, Gu MF, Luo GY, Liu LZ, Zhang R, Xu GL (2009) Complications of high intensity focused ultrasound for patients with hepatocellular carcinoma. Technol Cancer Res Treat 8(3):217–224
Zhang L, Zhu H, Jin C, Zhou K, Li K, Su H et al (2009) High-intensity focused ultrasound (HIFU): effective and safe therapy for hepatocellular carcinoma adjacent to major hepatic veins. Eur Radiol 19(2):435–445
Wu F, Wang ZB, Chen WZ, Zou JZ, Bai J, Zhu H, Li KQ et al (2004) Extracorporeal focused ultrasound surgery for treatment of human solid carcinomas: early Chinese clinical experience. Ultrasound Med Biol 30(2):245–260
Kennedy JE, Wu F, ter Haar GR, Gleeson FV, Phillips RR, Middleton MR et al (2004) High-intensity focused ultrasound for the treatment of liver tumours. Ultrasonics 42(1–9):931–935
Marberger MSG, Cranston D, Kennedy JE (2005) Extracorporeal ablation of renal tumours with high-intensity focused ultrasound. BJU Int 95(Suppl 2):52–55
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A. Muller, L. Petrusca, V. Auboiroux, P. J. Valette, R. Salomir, F. Cotton have no conflict of interest.
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Muller, A., Petrusca, L., Auboiroux, V. et al. Management of Respiratory Motion in Extracorporeal High-Intensity Focused Ultrasound Treatment in Upper Abdominal Organs: Current Status and Perspectives. Cardiovasc Intervent Radiol 36, 1464–1476 (2013). https://doi.org/10.1007/s00270-013-0713-0
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DOI: https://doi.org/10.1007/s00270-013-0713-0