Irreversible electroporation: state of the art

Peter Gk Wagstaff, Mara Buijs, Willemien van den Bos, Daniel M de Bruin, Patricia J Zondervan, Jean Jmch de la Rosette, M Pilar Laguna Pes, Peter Gk Wagstaff, Mara Buijs, Willemien van den Bos, Daniel M de Bruin, Patricia J Zondervan, Jean Jmch de la Rosette, M Pilar Laguna Pes

Abstract

The field of focal ablative therapy for the treatment of cancer is characterized by abundance of thermal ablative techniques that provide a minimally invasive treatment option in selected tumors. However, the unselective destruction inflicted by thermal ablation modalities can result in damage to vital structures in the vicinity of the tumor. Furthermore, the efficacy of thermal ablation intensity can be impaired due to thermal sink caused by large blood vessels in the proximity of the tumor. Irreversible electroporation (IRE) is a novel ablation modality based on the principle of electroporation or electropermeabilization, in which electric pulses are used to create nanoscale defects in the cell membrane. In theory, IRE has the potential of overcoming the aforementioned limitations of thermal ablation techniques. This review provides a description of the principle of IRE, combined with an overview of in vivo research performed to date in the liver, pancreas, kidney, and prostate.

Keywords: IRE; ablation; cancer; focal therapy; irreversible electroporation; tumor.

Figures

Figure 1
Figure 1
IRE equipment. Notes: (A) The NanoKnife™ IRE console. (B) User-friendly treatment planning software generates a 2D representation of the ablation zone, perpendicular to the direction of the inserted needle electrodes. (C) Monopolar needle electrodes (16 G), covered in a retractable insulation sheath, allowing for adjustment of the active tip length. The blue spacer allows for parallel external fixation of the IRE needles. (D) AccuSync ECG synchronizer, allowing for synchronization of the IRE pulses with the cardiac rhythm. Abbreviations: ECG, electrocardiogram; IRE, irreversible electroporation; 2D, two-dimensional.

References

    1. Lencioni R, Cioni D, Della Pina C, Crocetti L. Hepatocellular carcinoma: new options for image-guided ablation. J Hepatobiliary Pancreat Sci. 2010;17:399–403.
    1. Sharma A, Abtin F, Shepard JA. Image-guided ablative therapies for lung cancer. Radiol Clin North Am. 2012;50:975–999.
    1. Volpe A, Cadeddu JA, Cestari A, et al. Contemporary management of small renal masses. Eur Urol. 2011;60:501–515.
    1. Olweny EO, Cadeddu JA. Novel methods for renal tissue ablation. Curr Opin Urol. 2012;22:379–384.
    1. Valerio M, Ahmed HU, Emberton M, et al. The role of focal therapy in the management of localised prostate cancer: a systematic review. Eur Urol. 2014;66:732–751.
    1. van den Bos W, Muller BG, Ehdaie B, Scardino P, de la Rosette JJ. What is still needed to make focal therapy an accepted segment of standard therapy? Curr Opin Urol. 2014;24:247–255.
    1. Rubinsky B, Onik G, Mikus P. Irreversible electroporation: a new ablation modality – clinical implications. Technol Cancer Res Treat. 2007;6:37–48.
    1. Wagstaff PG, de Bruin DM, Zondervan PJ, et al. The efficacy and safety of irreversible electroporation for the ablation of renal masses: a prospective, human, in-vivo study protocol. BMC Cancer. 2015;15:165.
    1. Miklavcic D, Mali B, Kos B, Heller R, Sersa G. Electrochemotherapy: from the drawing board into medical practice. Biomed Eng Online. 2014;13:29.
    1. Yarmush ML, Golberg A, Sersa G, Kotnik T, Miklavcic D. Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng. 2014;16:295–320.
    1. Howick J, Phillips B, Ball C, et al. Oxford Centre for Evidence-based Medicine – Levels of Evidence. Centre for Evidence-Based Medicine, University of Oxford; 2009. [Accessed October 1, 2015]. Available from:
    1. Lee EW, Wong D, Prikhodko SV, et al. Electron microscopic demonstration and evaluation of irreversible electroporation-induced nanopores on hepatocyte membranes. J Vasc Interv Radiol. 2012;23:107–113.
    1. Chang DC, Reese TS. Changes in membrane-structure induced by electroporation as revealed by rapid-freezing electron-microscopy. Biophys J. 1990;58:1–12.
    1. Neumann E, Schaeferridder M, Wang Y, Hofschneider PH. Gene-transfer into mouse lyoma cells by electroporation in high electric-fields. EMBO J. 1982;1:841–845.
    1. Mir LM, Orlowski S, Belehradek J, Paoletti C. Electrochemotherapy potentiation of antitumor effect of bleomycin by local electric pulses. Eur J Cancer. 1991;27:68–72.
    1. Al-Sakere B, Andre F, Bernat C, et al. Tumor ablation with irreversible electroporation. PLoS One. 2007;2:e1135.
    1. Olweny EO, Kapur P, Tan YK, Park SK, Adibi M, Cadeddu JA. Irreversible electroporation: evaluation of nonthermal and thermal ablative capabilities in the porcine kidney. Urology. 2013;81:679–684.
    1. Pech M, Janitzky A, Wendler JJ, et al. Irreversible electroporation of renal cell carcinoma: a first-in-man phase I clinical study. Cardiovasc Intervent Radiol. 2011;34:132–138.
    1. Bertacchini C, Margotti PM, Bergamini E, Lodi A, Ronchetti M, Cadossi R. Design of an irreversible electroporation system for clinical use. Technol Cancer Res Treat. 2007;6:313–320.
    1. Kinosita K, Ashikawa I, Saita N, et al. Electroporation of cell-membrane visualized under a pulsed-laser fluorescence microscope. Biophys J. 1988;53:1015–1019.
    1. Hibino M, Shigemori M, Itoh H, Nagayama K, Kinosita K. Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys J. 1991;59:209–220.
    1. Jiang CL, Davalos RV, Bischof JC. A Review of basic to clinical studies of irreversible electroporation therapy. IEEE Trans Biomed Eng. 2015;62:4–20.
    1. Granot Y, Ivorra A, Maor E, Rubinsky B. In vivo imaging of irreversible electroporation by means of electrical impedance tomography. Phys Med Biol. 2009;54:4927–4943.
    1. van Gemert MJ, Wagstaff PG, de Bruin DM, et al. Irreversible electroporation: just another form of thermal therapy? Prostate. 2015;75(3):332–335.
    1. Wagstaff PG, de Bruin DM, van den Bos W, et al. Irreversible electroporation of the porcine kidney: temperature development and distribution. Urol Oncol. 2015;33(4):168.e1–168.e7.
    1. van den Bos W, Scheffer HJ, Vogel JA, et al. Thermal energy during irreversible electroporation and the influence of different ablation parameters. J Vasc Interv Radiol. 2015 Dec 17; Epub.
    1. Davalos RV, Bhonsle S, Neal RE. Implications and considerations of thermal effects when applying irreversible electroporation tissue ablation therapy. Prostate. 2015;75:1114–1118.
    1. Golberg A, Yarmush ML. Nonthermal irreversible electroporation: fundamentals, applications, and challenges. IEEE Trans Biomed Eng. 2013;60:707–714.
    1. van den Bos W, de Bruin DM, Jurhil RR, et al. The correlation between the electrode configuration and histopathology of Irreversible Electroporation ablations in prostate cancer patients. World J Urol. 2015 Aug 22; Epub.
    1. Tracy CR, Kabbani W, Cadeddu JA. Irreversible electroporation (IRE): a novel method for renal tissue ablation. BJU Int. 2011;107:1982–1987.
    1. Wimmer T, Srimathveeravalli G, Gutta N, et al. Planning irreversible electroporation in the porcine kidney: are numerical simulations reliable for predicting empiric ablation outcomes? Cardiovasc Intervent Radiol. 2015;38:182–190.
    1. Nielsen K, Scheffer HJ, Vieveen JM, et al. Anaesthetic management during open and percutaneous irreversible electroporation. Br J Anaesth. 2014;113:985–992.
    1. Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology. 2011;53:1020–1022.
    1. Cho YK, Kim JK, Kim MY, Rhim H, Han JK. Systematic review of randomized trials for hepatocellular carcinoma treated with percutaneous ablation therapies. Hepatology. 2009;49:453–459.
    1. Teratani T, Yoshida H, Shiina S, et al. Radiofrequency ablation for hepatocellular carcinoma in so-called high-risk locations. Hepatology. 2006;43:1101–1108.
    1. Thomson KR, Cheung W, Ellis SJ, et al. Investigation of the safety of irreversible electroporation in humans. J Vasc Interv Radiol. 2011;22:611–621.
    1. Sugimoto K, Moriyasu F, Kobayashi Y, et al. Irreversible electroporation for nonthermal tumor ablation in patients with hepatocellular carcinoma: initial clinical experience in Japan. Jpn J Radiol. 2015;33:424–432.
    1. Kingham TP, Karkar AM, D’Angelica MI, et al. Ablation of perivascular hepatic malignant tumors with irreversible electroporation. J Am Coll Surg. 2012;215:379–387.
    1. Niessen C, Igl J, Pregler B, et al. Factors associated with short-term local recurrence of liver cancer after percutaneous ablation using irreversible electroporation: a prospective single-center study. J Vasc Interv Radiol. 2015;26:694–702.
    1. Cannon R, Ellis S, Hayes D, Narayanan G, Martin RC. Safety and early efficacy of irreversible electroporation for hepatic tumors in proximity to vital structures. J Surg Oncol. 2013;107:544–549.
    1. Cheung W, Kavnoudias H, Roberts S, Szkandera B, Kemp W, Thomson KR. Irreversible electroporation for unresectable hepatocellular carcinoma: initial experience and review of safety and outcomes. Technol Cancer Res Treat. 2013;12:233–241.
    1. Cheng RG, Bhattacharya R, Yeh MM, Padia SA. Irreversible electroporation can effectively ablate hepatocellular carcinoma to complete pathologic necrosis. J Vasc Interv Radiol. 2015;26:1184–1188.
    1. Yeo CJ. Pancreatic cancer – in brief. Curr Probl Cancer. 2002;26:170.
    1. Pandya GJ, Shelat VG. Radiofrequency ablation of pancreatic ductal adenocarcinoma: the past, the present and the future. World J Gastrointest Oncol. 2015;7:6–11.
    1. Narayanan G, Hosein PJ, Arora G, et al. Percutaneous irreversible electroporation for downstaging and control of unresectable pancreatic adenocarcinoma. J Vasc Interv Radiol. 2012;23:1613–1621.
    1. Paiella S, Butturini G, Frigerio I, et al. Safety and feasibility of Irreversible Electroporation (IRE) in patients with locally advanced pancreatic cancer: results of a prospective study. Dig Surg. 2015;32:90–97.
    1. Martin RC, McFarland K, Ellis S, Velanovich V. Irreversible electroporation therapy in the management of locally advanced pancreatic adenocarcinoma. J Am Coll Surg. 2012;215:361–369.
    1. Martin RC, McFarland K, Ellis S, Velanovich V. Irreversible electroporation in locally advanced pancreatic cancer: potential improved overall survival. Ann Surg Oncol. 2013;20(suppl 3):S443–S449.
    1. Martin RC, Kwon D, Chalikonda S, et al. Treatment of 200 locally advanced (Stage III) pancreatic adenocarcinoma patients with irreversible electroporation: safety and efficacy. Ann Surg. 2015;262:486–494.
    1. Katsanos K, Mailli L, Krokidis M, McGrath A, Sabharwal T, Adam A. Systematic review and meta-analysis of thermal ablation versus surgical nephrectomy for small renal tumours. Cardiovasc Intervent Radiol. 2014;37:427–437.
    1. Wagstaff P, Ingels A, Zondervan P, de la Rosette JJ, Laguna MP. Thermal ablation in renal cell carcinoma management: a comprehensive review. Curr Opin Urol. 2014;24:474–482.
    1. Trimmer CK, Khosla A, Morgan M, Stephenson SL, Ozayar A, Cadeddu JA. Minimally invasive percutaneous treatment of small renal tumors with irreversible electroporation: a single-center experience. J Vasc Interv Radiol. 2015;26(10):1465–1471.
    1. Wendler JJ, Ricke J, Pech M, et al. First delayed resection findings after irreversible electroporation (IRE) of human localised renal cell carcinoma (RCC) in the IRENE pilot Phase 2a trial. Cardiovasc Intervent Radiol. 2015;39(2):239–250.
    1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60:277–300.
    1. Resnick MJ, Koyama T, Fan KH, et al. Long-term functional outcomes after treatment for localized prostate cancer. N Engl J Med. 2013;368:436–445.
    1. Ficarra V, Novara G, Ahlering TE, et al. Systematic review and meta-analysis of studies reporting potency rates after robot-assisted radical prostatectomy. Eur Urol. 2012;62:418–430.
    1. Ficarra V, Novara G, Rosen RC, et al. Systematic review and meta-analysis of studies reporting urinary continence recovery after robot-assisted radical prostatectomy. Eur Urol. 2012;62:405–417.
    1. Onik G, Rubinsky B. Irreversible electroporation: first patient experience focal therapy of prostate cancer. In: Rubinsky B, editor. Irreversible Electroporation. Berlin Heidelberg: Springer-Verlag; 2010. pp. 235–247.
    1. Valerio M, Stricker PD, Ahmed HU, et al. Initial assessment of safety and clinical feasibility of irreversible electroporation in the focal treatment of prostate cancer. Prostate Cancer Prostatic Dis. 2014;17:343–347.
    1. McCulloch P, Altman DG, Campbell WB, et al. No surgical innovation without evaluation: the IDEAL recommendations. Lancet. 2009;374:1105–1112.
    1. Silk MT, Wimmer T, Lee KS, et al. Percutaneous ablation of peribiliary tumors with irreversible electroporation. J Vasc Interv Radiol. 2014;25:112–118.
    1. Scheffer HJ, Nielsen K, van Tilborg AA, et al. Ablation of colorectal liver metastases by irreversible electroporation: results of the COLD-FIRE-I ablate-and-resect study. Eur Radiol. 2014;24:2467–2475.

Source: PubMed

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