2,051
Views
7
CrossRef citations to date
0
Altmetric
Research Article

Feasibility study of MR-guided pancreas ablation using high-intensity focused ultrasound in a healthy swine model

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 786-798 | Received 10 Feb 2020, Accepted 07 Jun 2020, Published online: 03 Jul 2020

References

  • Bray F, Ferlay J, Soerjomataram I, et al. Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.
  • Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2019. CA. CAA Cancer J Clin. 2019;69(1):7–34.
  • Zhang Q, Zeng L, Chen Y, et al. Pancreatic cancer epidemiology, detection, and management. Gastroenterol Res Pract. 2016;2016:8962321–8962310.
  • Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371(11):1039–1049.
  • Isaji S, Mizuno S, Windsor JA, et al. International consensus on definition and criteria of borderline resectable pancreatic ductal adenocarcinoma 2017. Pancreatology. 2018;18(1):2–11.
  • Feig C, Gopinathan A, Neesse A, et al. The pancreas cancer microenvironment. Clin Cancer Res. 2012;18(16):4266–4276.
  • Moffat GT, Epstein AS, O'Reilly EM. Pancreatic cancer—a disease in need: optimizing and integrating supportive care. Cancer. 2019;125(22):3927–3929.
  • Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet. 2011;378(9791):607–620.
  • Carlson CL. Effectiveness of the World Health Organization Cancer Pain Relief Guidelines: an integrative review. J Pain Res. 2016;9:515–534.
  • WHO. Cancer pain relief with a guide to opioid availability. 2nd ed. Geneva, Switzerland: World Health Organization; 1996.
  • Wong GY, Schroeder DR, Carns PE, et al. Effect of neurolytic celiac plexus block on pain relief, quality of life, and survival in patients with unresectable pancreatic cancer: a randomized controlled trial. J Am Med Assoc. 2004;291(9):1092–1099.
  • Xiong L. The preliminary clinical results of the treatment for advanced pancreatic carcinoma by high intensity focused ultrasound. Chin J Gen Surg. 2001;16:345–347.
  • Xu Y, Wang G, Gu Y, et al. The acesodyne effect of high intensity focused ultrasound on the treatment of advanced pancreatic carcinoma. Clin Med J China. 2003;10:322–323.
  • Yuan C, Yang L, Cheng Y. Observation of high intensity focused ultrasound treating 40 cases of cancer of pancreas. Chlin J Clin Hep. 2003;19:145–146.
  • Xiong LL, Hwang JH, Huang XB, et al. Early clinical experience using high intensity focused ultrasound for palliation of inoperable pancreatic cancer. J. Pancreas. 2009;10:123–129.
  • Gao HF, Wang K, Meng ZQ, et al. High intensity focused ultrasound treatment for patients with local advanced pancreatic cancer. Hepatogastroenterology. 2013;60(128):1906–1910.
  • Vidal-Jove J, Perich E, Del Castillo MA. Ultrasound guided high intensity focused ultrasound for malignant tumors: the Spanish experience of survival advantage in stage III and IV pancreatic cancer. Ultrason Sonochem. 2015;27:703–706.
  • Dimcevski G, Kotopoulis S, Bjånes T, et al. A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. J Control Release. 2016;243:172–181.
  • Marinova M, Rauch M, Mücke M, et al. High-intensity focused ultrasound (HIFU) for pancreatic carcinoma: evaluation of feasibility, reduction of tumour volume and pain intensity. Eur Radiol. 2016;26(11):4047–4056.
  • Ji Y, Zhang Y, Zhu J, et al. Response of patients with locally advanced pancreatic adenocarcinoma to high-intensity focused ultrasound treatment: a single-center, prospective, case series in China. CMAR. 2018;10:4439–4446.
  • Marinova M, Huxold HC, Henseler J, et al. Clinical effectiveness and potential survival benefit of US-guided high-intensity focused ultrasound therapy in patients with advanced-stage pancreatic cancer. Ultraschall Med. 2019;40(5):625–637.
  • Wu F, Wang ZB, Cao YD, et al. Heat fixation of cancer cells ablated with high-intensity-focused ultrasound in patients with breast cancer. Am J Surg. 2006;192(2):179–184.
  • Ter Haar G, Coussios C. High intensity focused ultrasound: physical principles and devices. Int J Hyperthermia. 2007;23(2):89–104.
  • Dababou S, Marrocchio C, Rosenberg J, et al. A meta-analysis of palliative treatment of pancreatic cancer with high intensity focused ultrasound. J Ther Ultrasound. 2017;5:9.
  • Zhao H, Yang G, Wang D, et al. Concurrent gemcitabine and high-intensity focused ultrasound therapy in patients with locally advanced pancreatic cancer. Anticancer Drugs. 2010;21(4):447–452.
  • Orsi F, Zhang L, Arnone P, et al. High-intensity focused ultrasound ablation: effective and safe therapy for solid tumors in difficult locations. AJR Am J Roentgenol. 2010;195(3):W245–252.
  • Wang K, Chen Z, Meng Z, et al. Analgesic effect of high intensity focused ultrasound therapy for unresectable pancreatic cancer. Int J Hyperthermia. 2011;27(2):101–107.
  • Sung HY, Jung SE, Cho SH, et al. Long-term outcome of high-intensity focused ultrasound in advanced pancreatic cancer. Pancreas. 2011;40(7):1080–1086.
  • Sofuni A, Moriyasu F, Sano T, et al. Safety trial of high-intensity focused ultrasound therapy for pancreatic cancer. World J Gastroenterol. 2014;20(28):9570–9577.
  • Li P-Z, Zhu S-H, He W, et al. High-intensity focused ultrasound treatment for patients with unresectable pancreatic cancer. Hbpd Int. 2012;11(6):655–660.
  • Orgera G, Krokidis M, Monfardini L, et al. High intensity focused ultrasound ablation of pancreatic neuroendocrine tumours: report of two cases. Cardiovasc Intervent Radiol. 2011;34(2):419–423.
  • Lv W, Yan T, Wang G, et al. High-intensity focused ultrasound therapy in combination with gemcitabine for unresectable pancreatic carcinoma. Ther. Clin. Risk Manag. 2016;12:687–691.
  • Sapareto SA, Hopwood LE, Dewey WC. Combined effects of X irradiation and hyperthermia on CHO cells for various temperatures and orders of application. Radiat Res. 1978;73(2):221–233.
  • Sapareto S. a, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol. 1984;10(6):787–800.
  • Damianou C, Hynynen K. The effect of various physical parameters on the size and shape of necrosed tissue volume during ultrasound surgery. J Acoust Soc Am. 1994;95(3):1641–1649.
  • Chung AH, Jolesz FA, Hynynen K. Thermal dosimetry of a focused ultrasound beam in vivo by magnetic resonance imaging. Med Phys. 1999;26(9):2017–2026.
  • McDannold N, Hynynen K, Wolf D, et al. MRI evaluation of thermal ablation of tumors with focused ultrasound. J Magn Reson Imaging. 1998;8:91–100.
  • Van Rhoon GC, Samaras T, Yarmolenko PS, et al. CEM43C thermal dose thresholds: a potential guide for magnetic resonance radiofrequency exposure levels? Eur Radiol. 2013;23(8):2215–2227.
  • Yarmolenko PS, Moon EJ, Landon C, et al. Thresholds for thermal damage to normal tissues: an update. Int J Hyperthermia. 2011;27(4):320–343.
  • Dewhirst MW, Viglianti BL, Lora-Michiels M, et al. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int J Hyperthermia. 2003;19(3):267–294.
  • Enholm JK, Köhler M, Quesson B, et al. Improved volumetric MR-HIFU ablation by Robust binary feedback control. IEEE Trans Biomed Eng. 2010;57(1):103–113.
  • Köhler M, Mougenot C, Quesson B, et al. Volumetric HIFU ablation under 3D guidance of rapid MRI thermometry. Med Phys. 2009;36(8):3521–3535.
  • Ebbini ES, Ter Haar G. Ultrasound-guided therapeutic focused ultrasound: current status and future directions. Int J Hyperthermia. 2015;31(2):77–89.
  • Hynynen K. MRIgHIFU: a tool for image-guided therapeutics. J Magn Reson Imaging. 2011;34(3):482–493.
  • Shahmirzadi D, Hou GY, Chen J, et al. Ex vivo characterization of canine liver tissue viscoelasticity after high-intensity focused ultrasound ablation. Ultrasound Med Biol. 2014;40(2):341–350.
  • Zhang S, Zhou F, Wan M, et al. Feasibility of using Nakagami distribution in evaluating the formation of ultrasound-induced thermal lesions. J Acoust Soc Am. 2012;131(6):4836–4844.
  • Shankar PM. Ultrasonic tissue characterization using a generalized Nakagami model. IEEE Trans Ultrason Ferroelectr Freq Control. 2001;48(6):1716–1720.
  • Lewis MA, Staruch RM, Chopra R. Thermometry and ablation monitoring with ultrasound. Int J Hyperthermia. 2015;31(2):163–181.
  • Bamber J, Hill C. Ultrasonic attenuation and propagation speed in mammalian tissues as a function of temperature. Ultrasound Med Biol. 1979;5(2):149–157.
  • Teixeira CA, Alvarenga AV, Cortela G, et al. Feasibility of non-invasive temperature estimation by the assessment of the average gray-level content of B-mode images. Ultrasonics. 2014;54(6):1692–1702.
  • Maraghechi B, Kolios MC, Tavakkoli J. Feasibility of detecting change in backscattered energy of acoustic harmonics in locally heated tissues. Int J Hyperth. 2019;36:964–974.
  • Ishihara Y, Calderon A, Watanabe H, et al. A precise and fast temperature mapping using water proton chemical shift. Magn Reson Med. 1995;34(6):814–823.
  • Hall LD, Talagala SL. Mapping of pH and temperature distribution using chemical-shift-resolved tomography. J Magn Reson. 1985;65(3):501–505.
  • Vimeux F, De Zwart JA, Palussiére J, et al. Real-time control of focused ultrasound heating based on rapid MR thermometry. Invest Radiol. 1999;34(3):190–193.
  • Daum DR, Hynynen K. Thermal dose optimization via temporal switching in ultrasound surgery. IEEE Trans Ultrason Ferroelectr Freq Control. 1998;45(1):208–215.
  • Siedek F, Yeo SY, Heijman E, et al. Magnetic resonance-guided high-intensity focused ultrasound (MR-HIFU): technical background and overview of current clinical applications (part 1). Rofo. 2019;191(6):522–530.
  • Siedek F, Yeo SY, Heijman E, et al. Magnetic resonance-guided high-intensity focused ultrasound (MR-HIFU): overview of emerging applications (part 2). Rofo. 2019;191(6):531–539.
  • Focused Ultrasound Foundation. State of the Technology [Internet]. [cited 2019 Aug 15]. Available from: https://www.fusfoundation.org/the-technology/state-of-the-technology.
  • Anzidei M, Marincola BC, Bezzi M, et al. Magnetic resonance-guided high-intensity focused ultrasound treatment of locally advanced pancreatic adenocarcinoma: preliminary experience for pain palliation and local tumor control. Invest Radiol. 2014;49(12):759–765.
  • Ligresti D, Kuo YT, Baraldo S, et al. EUS anatomy of the pancreatobiliary system in a swine model: the WISE experience. Endosc Ultrasound. 2019;8(4):249–254.
  • Swindle MM, Makin A, Herron AJ, et al. Swine as models in biomedical research and toxicology testing. Vet Pathol. 2012;49(2):344–356.
  • Ferrer J, Scott WE, Weegman BP, et al. Pig Pancreas Anatomy: Implications for Pancreas Procurement, preservation, and islet isolation. Transplantation. 2008;86(11):1503–1510.
  • Mahadevan V. Anatomy of the pancreas and spleen. Surgery. 2016;34(6):261–265.
  • Swindle MM, Smith AC. Comparative anatomy and physiology of the pig. Scand J Lab Anim Sci. 1998;25:11–21.
  • Khokhlova TD, Hwang JH. HIFU for palliative treatment of pancreatic cancer. J Gastrointest Oncol. 2011;2:83–95.
  • Liu CX, Gao XS, Xiong LL, et al. A preclinical in vivo investigation of high-intensity focused ultrasound combined with radiotherapy. Ultrasound Med Biol. 2011;37(1):69–77.
  • Hwang JH, Wang YN, Warren C, et al. Preclinical in vivo evaluation of an extracorporeal HIFU device for ablation of pancreatic tumors. Ultrasound Med Biol. 2009;35(6):967–975.
  • Xie B, Li YY, Jia L, et al. Experimental ablation of the pancreas with High Intensity Focused Ultrasound (HIFU) in a porcine model. Int J Med Sci. 2011;8(1):9–15.
  • Dupré A, Melodelima D, Pflieger H, et al. Thermal ablation of the pancreas with intraoperative high-intensity focused ultrasound: safety and efficacy in a porcine model. Pancreas. 2017;46(2):219–224.
  • Chang W, Lee JY, Lee JH, et al. A portable high-intensity focused ultrasound system for the pancreas with 3d electronic steering: a preclinical study in a swine model. Ultrasonography. 2018;37(4):298–306.
  • Li T, Khokhlova T, Maloney E, et al. Endoscopic high-intensity focused US: technical aspects and studies in an in vivo porcine model. Gastrointest Endosc. 2015;81(5):1243–1250.
  • Kothapalli S, Altman MB, Partanen A, et al. Acoustic field characterization of a clinical magnetic resonance-guided high-intensity focused ultrasound system inside the magnet bore. Med Phys. 2017;44(9):4890–4899.
  • Ferrer CJ, Bartels LW, van Stralen M, et al. Fluid filling of the digestive tract for improved proton resonance frequency shift-based MR thermometry in the pancreas. J Magn Reson Imaging. 2018;47(3):692–701.
  • Strunk HM, Henseler J, Rauch M, et al. Clinical use of high-intensity focused ultrasound (HIFU) for tumor and pain reduction in advanced pancreatic cancer. Rofo. 2016;188(7):662–670.
  • Shimizu M, Hayashi T, Saitoh Y, et al. Postmortem autolysis in the pancreas: multivariate statistical study. The influence of clinicopathological conditions. Pancreas. 1990;5(1):91–94.
  • Eltoum I, Fredenburgh J, Myers RB, et al. Introduction to the theory and practice of fixation of tissues. J Histotechnol. 2001;24(3):173–190.
  • Szabo TL. Time domain wave equations for Lossy media obeying a frequency power law. J Acoust Soc Am. 1994;96(1):491–500.
  • Bottomley PA. In-vivo soft tissue NMR imaging of the rat thorax and abdomen. Experientia. 1981;37(7):768–770.
  • Wallner BK, Schumacher KA, Weidenmaier W, et al. Dilated biliary tract: evaluation with MR cholangiography with a T2-weighted contrast-enhanced fast sequence. Radiology. 1991;181(3):805–808.
  • Wedeen V, Meuli R, Edelman R, et al. Projective imaging of pulsatile flow with magnetic resonance. Science. 1985;230(4728):946–948.
  • Mougenot C, Moonen C. Magnetic resonance-guided high intensity focused ultrasound in the presence of biopsy markers. J Ther Ultrasound. 2017;5:4–13.
  • Gurney-Champion OJ, Lens E, Van Der Horst A, et al. Visibility and artifacts of gold fiducial markers used for image guided radiation therapy of pancreatic cancer on MRI. Med Phys. 2015;42(5):2638–2647.
  • Stowell RE. Effect on tissue volume of various methods of fixation, dehydration, and embedding. Biotech. Histochem. 1941;16(2):67–83.