Advertisement
Advances in Clinical Radiology

The Development of Histotripsy for the Treatment of Liver Tumors

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Advances in Clinical Radiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Siegel R.L.
        • Miller K.D.
        • Fuchs H.E.
        • et al.
        Cancer statistics, 2021.
        CA Cancer J Clin. 2021; 71: 7-33
        • Schoenberg S.O.
        • Attenberger U.I.
        • Solomon S.B.
        • et al.
        Developing a roadmap for interventional oncology.
        Oncologist. 2018; 23: 1162-1170
        • Chen M.S.
        • Li J.Q.
        • Zheng Y.
        • et al.
        A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma.
        Ann Surg. 2006; 243: 321-328
        • Gillams A.
        • Goldberg N.
        • Ahmed M.
        • et al.
        Thermal ablation of colorectal liver metastases: a position paper by an international panel of ablation experts, the interventional oncology sans frontières meeting 2013.
        Eur Radiol. 2015; 25: 3438-3454
        • Ziemlewicz T.J.
        • Wells S.A.
        • Lubner M.G.
        • et al.
        Hepatic tumor ablation.
        Surg Clin North Am. 2016; 96: 315-339
        • Lahat E.
        • Eshkenazy R.
        • Zendel A.
        • et al.
        Complications after percutaneous ablation of liver tumors: a systematic review.
        Hepatobiliary Surg Nutr. 2014; 3: 317-31723
        • Livraghi T.
        • Solbiati L.
        • Meloni M.F.
        • et al.
        Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study.
        Radiology. 2003; 226: 441-451
        • Brace C.L.
        Radiofrequency and microwave ablation of the liver, lung, kidney, and bone: what are the differences?.
        Curr Probl Diagn Radiol. 2009; 38: 135-143
        • Cao Y.
        • Yin Y.
        • Wang X.
        • et al.
        Sublethal irradiation promotes the metastatic potential of hepatocellular carcinoma cells.
        Cancer Sci. 2021; 112: 265-274
        • Xu Z.
        • Ludomirsky A.
        • Eun L.Y.
        • et al.
        Controlled ultrasound tissue erosion.
        Proc IEEE Ultrason Symp. 2003; 1: 732-735
        • Bader K.B.
        • Vlaisavljevich E.
        • Maxwell A.D.
        For whom the bubble grows: Physical principles of bubble nucleation and dynamics in histotripsy ultrasound therapy.
        Ultrasound Med Biol. 2019; 45: 1056-1080
        • Knott E.A.
        • Swietlik J.F.
        • Longo K.C.
        • et al.
        Robotically-assisted sonic therapy for renal ablation in a live porcine model: initial preclinical results.
        J Vasc Interv Radiol. 2019; 30: 1293-1302
        • Zhang X.
        • Macoskey J.J.
        • Ives K.
        • et al.
        Non-invasive thrombolysis using microtripsy in a porcine deep vein thrombosis model.
        Ultrasound Med Biol. 2017; 43: 1378-1390
        • Hendricks-Wenger A.
        • Sereno J.
        • Gannon J.
        • et al.
        Histotripsy ablation alters the tumor microenvironment and promotes immune system activation in a subcutaneous model of pancreatic cancer.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2021; 68: 2987-3000
        • Arnold L.
        • Hendricks-Wenger A.
        • Coutermarsh-Ott S.
        • et al.
        Histotripsy ablation of bone tumors: feasibility study in excised canine osteosarcoma tumors.
        Ultrasound Med Biol. 2021; 47: 3435-3446
        • Vlaisavljevich E.
        • Kim Y.
        • Allen S.
        • et al.
        Feasibility Study in an in vivo Porcine Model.
        Ultrasound Med Biol. 2013; 39: 1398-1409
        • Smolock A.R.
        • Cristescu M.M.
        • Vlaisavljevich E.
        • et al.
        Robotically assisted sonic therapy as a noninvasive nonthermal ablation modality: proof of concept in a porcine liver model.
        Radiology. 2018; 287: 485-493
        • Hall T.L.
        • Hempel C.R.
        • Wojno K.
        • et al.
        Histotripsy of the prostate: dose effects in a chronic canine model.
        Urol Elsevier Inc. 2009; 74: 932-937
        • Sukovich J.R.
        • Cain C.A.
        • Pandey A.S.
        • et al.
        In vivo histotripsy brain treatment.
        J Neurosurg. 2019; 131: 1331-1338
        • Swietlik J.F.
        • Mauch S.C.
        • Knott E.A.
        • et al.
        Noninvasive thyroid histotripsy treatment: proof of concept study in a porcine model.
        Int J Hyperth Taylor Francis. 2021; 38: 798-804
        • Xu Z.
        • Owens G.
        • Gordon D.
        • et al.
        Noninvasive creation of an atrial septal defect by histotripsy in a canine model.
        Circulation. 2010; 121: 742-749
        • Schuster T.G.
        • Wei J.T.
        • Hendlin K.
        • et al.
        Histotripsy treatment of benign prostatic enlargement using the Vortx Rx system: initial human safety and efficacy outcomes.
        Urol Elsevier Inc. 2018; 114: 184-187
        • Vidal-Jove J.
        • Serres-Creixams X.
        • Ziemlewicz T.J.
        • et al.
        Liver histotripsy mediated abscopal effect—case report.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2021; 68: 3001-3005
        • Ter Haar G.R.
        High intensity focused ultrasound for the treatment of tumors.
        Echocardiography. 2001; 18: 317-322
        • Maxwell A.D.
        • Cain C.A.
        • Hall T.L.
        • et al.
        Probability of cavitation for single ultrasound pulses applied to tissues and tissue-mimicking materials.
        Ultrasound Med Biol. 2013; 39: 449-465
        • Vlaisavljevich E.
        • Lin K.-W.
        • Maxwell A.
        • et al.
        Effects of ultrasound frequency and tissue stiffness on the histotripsy intrinsic threshold for cavitation.
        Ultrasound Med Biol. 2015; 41: 1651-1667
        • Mancia L.
        • Vlaisavljevich E.
        • Xu Z.
        • et al.
        Predicting Tissue Susceptibility to Mechanical Cavitation Damage in Therapeutic Ultrasound.
        Ultrasound Med Biol. 2017; 43: 1421-1440
        • Maxwell A.D.
        • Wang T.-Y.
        • Cain C.A.
        • et al.
        Cavitation clouds created by shock scattering from bubbles during histotripsy.
        J Acoust Soc Am. 2011; 130: 1888-1898
        • Vlaisavljevich E.
        • Maxwell A.
        • Warnez M.
        • et al.
        Histotripsy-induced cavitation cloud initiation thresholds in tissues of different mechanical properties.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2014; 61: 341-352
        • Khokhlova T.D.
        • Wang Y.N.
        • Simon J.C.
        • et al.
        Ultrasound-guided tissue fractionation by high intensity focused ultrasound in an in vivo porcine liver model.
        Proc Natl Acad Sci U S A. 2014; 111: 8161-8166
        • Vlaisavljevich E.
        • Xu Z.
        • Maxwell A.
        • et al.
        Effects of Temperature on the Histotripsy Intrinsic Threshold for Cavitation.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2016; 63: 1064-1077
        • Pahk K.J.
        Control of the dynamics of a boiling vapour bubble using pressure-modulated high intensity focused ultrasound without the shock scattering effect: a first proof-of-concept study.
        Ultrason Sonochem Elsevier B.V. 2021; 77: 105699
        • Vlaisavljevich E.
        • Maxwell A.
        • Mancia L.
        • et al.
        Visualizing the histotripsy process: bubble cloud-cancer cell interactions in a tissue-mimicking environment.
        Ultrasound Med Biol. 2016; 42: 2466-2477
        • Mancia L.
        • Vlaisavljevich E.
        • Yousefi N.
        • et al.
        Modeling tissue-selective cavitation damage.
        Phys Med Biol. 2019; 64: 225001
        • Wang T.Y.
        • Xu Z.
        • Hall T.L.
        • et al.
        An efficient treatment strategy for histotripsy by removing cavitation memory.
        Ultrasound Med Biol. 2012; 38: 753-766
        • Vlaisavljevich E.
        • Gerhardson T.
        • Hall T.
        • et al.
        Effects of F-Number on the Histotripsy Intrinsic Threshold and Cavitation Bubble Cloud Behavior.
        Phys Med Biol. 2017; 62: 1269-1290
        • Edsall C.
        • Ham E.
        • Holmes H.
        • et al.
        Effects of frequency on bubble-cloud behavior and ablation efficiency in intrinsic threshold histotripsy.
        Phys Med Biol IOP Publishing. 2021; 66https://doi.org/10.1088/1361-6560/ac33ed
        • Hendricks-Wenger A.
        • Weber P.
        • Simon A.
        • et al.
        Histotripsy for the treatment of cholangiocarcinoma liver tumors: in vivo feasibility and Ex Vivo dosimetry study.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2021; 68: 2953-2964
        • Hu Z.
        • Xiao Y.Y.
        • Liu Y.
        • et al.
        Release of endogenous danger signals from HIFU-treated tumor cells and their stimulatory effects on APCs.
        Biochem Biophys Res Commun. 2005; 335: 124-131
        • Eranki A.
        • Srinivasan P.
        • Ries M.
        • et al.
        High-intensity focused ultrasound (hIFU) triggers immune sensitization of refractory murine neuroblastoma to checkpoint inhibitor therapy.
        Clin Cancer Res. 2020; 26: 1152-1161
        • Longo K.C.
        • Knott E.A.
        • Watson R.F.
        • et al.
        Robotically assisted sonic therapy (RAST) for noninvasive hepatic ablation in a porcine model: mitigation of body wall damage with a modified pulse sequence.
        Cardiovasc Intervent Radiol. 2019; 42: 1016-1023
        • Vlaisavljevich E.
        • Owens G.
        • Lundt J.
        • et al.
        Non-invasive liver ablation using histotripsy: preclinical safety study in an in vivo porcine model.
        Ultrasound Med Biol. 2017; 43: 1237-1251
        • Vlaisavljevich E.
        • Kim Y.
        • Owens G.
        • et al.
        Effects of tissue mechanical properties on susceptibility to histotripsy-induced tissue damage.
        Phys Med Biol. 2014; 59: 253-270
        • Vlaisavljevich E.
        • Lin K.
        • Warnez M.
        • et al.
        Effects of tissue stiffness, ultrasound frequency, and pressure on histotripsy-induced cavitation bubble behavior.
        Phys Med Biol. 2015; 60: 2271-2292
        • Vlaisavljevich E.
        • Greve J.
        • Cheng X.
        • et al.
        Non-invasive ultrasound liver ablation using histotripsy: chronic study in an in vivo rodent model.
        Ultrasound Med Biol. 2016; 42: 1890-1902
        • Lin K.
        • Kim Y.
        • Maxwell A.D.
        • et al.
        Histotripsy beyond the “Intrinsic” Cavitation Threshold using Very Short Ultrasound Pulses: “Microtripsy.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2014; 61: 251-265
        • Lundt J.
        • Allen S.P.
        • Shi J.
        • et al.
        Noninvasive, rapid ablation of tissue volume using histotripsy.
        Ultrasound Med Biol. 2017; 43: 2834-2847
        • Mallay M.G.
        • Woodacre J.K.
        • Landry T.G.
        • et al.
        A dual-frequency lens-focused endoscopic histotripsy transducer.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2021; 68: 2906-2916
        • 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: 394-424
        • El-Serag H.
        Hepatocellular carcinoma.
        N Engl J Med. 2011; 365: 1118-1127
        • Brace C.L.
        Microwave tissue ablation: biophysics, technology, and applications.
        Crit Rev Biomed Eng. 2010; 38: 65-78
        • Longo K.C.
        • Zlevor A.M.
        • Laeseke P.F.
        • et al.
        Histotripsy Ablations in a Porcine Liver Model: Feasibility of Respiratory Motion Compensation by Alteration of the Ablation Zone Prescription Shape.
        Cardiovasc Intervent Radiol. 2020; 43: 1695-1701
        • Knott E.A.
        • Longo K.C.
        • Vlaisavljevich E.
        • et al.
        Transcostal histotripsy ablation in an in vivo acute hepatic porcine model.
        Cardiovasc Intervent Radiol. 2021; 44: 1643-1650
        • SC M.
        • AM Z.
        • EA K.
        • et al.
        Hepatic and renal histotripsy in an anticoagulated porcine model.
        Soc Interv Oncol. 2022;
        • Wheat J.C.
        • Hall T.L.
        • Hempel C.R.
        • et al.
        Prostate histotripsy in an anticoagulated model.
        Urology. 2010; 75: 207-211
        • Knott E.
        • Zlevor A.
        • Hinshaw J.
        • et al.
        A comparison study between an ultrasound-guided non-invasive ablation modality (histotripsy) vs. microwave ablation in a porcine model.
        Soc Abdom Radiol. 2022;
        • Hendricks-Wenger A.
        • Aycock K.N.
        • Nagai-Singer M.A.
        • et al.
        Establishing an immunocompromised porcine model of human cancer for novel therapy development with pancreatic adenocarcinoma and irreversible electroporation.
        Sci Rep. 2021; 11 (Nature Publishing Group UK): 1-14
        • Hendricks-Wenger A.
        • Arnold L.
        • Gannon J.
        • et al.
        Histotripsy ablation in preclinical animal models of cancer and spontaneous tumors in veterinary patients: a review.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2022; 69: 5-26
        • Worlikar T.
        • Mendiratta-Lala M.
        • Vlaisavljevich E.
        • et al.
        Effects of histotripsy on local tumor progression in an in vivo orthotopic rodent liver tumor model.
        BME Front. 2020; 2020: 1-14
        • Qu S.
        • Worlikar T.
        • Felsted A.E.
        • et al.
        Non-thermal histotripsy tumor ablation promotes abscopal immune responses that enhance cancer immunotherapy.
        J Immunother Cancer. 2020; 8: 1-12
        • Styn N.R.
        • Hall T.L.
        • Fowlkes J.B.
        • et al.
        Histotripsy of renal implanted VX-2 tumor in a rabbit model: Investigation of metastases.
        Urol Elsevier Inc. 2012; 80: 724-729
        • Swietlik J.F.
        • Wagner M.G.
        • Periyasamy S.
        • et al.
        Optimization of image acquisition for histotripsy target prediction using cone beam CT and fluoroscopy.
        Cardiovasc Interv Radiol Soc Eur. 2021;
        • Periyasamy S.
        • Wagner M.
        • Swietlik J.F.
        • et al.
        Guidance and Assessment of Histotripsy Ablations using C-Arm Imaging Systems.
        Soc Interv Oncol. 2021;