A review of basic to clinical studies of irreversible electroporation therapy

IEEE Transactions on Biomedical Engineering

Volumn 62, Issue 1, 2015, Pages 4-20

  Jiang, Chunlan ^a   Davalos, Rafael V ^b   Bischof, John C ^c  

^a University of Minnesota   (United States)

^b Virginia Tech Wake Forest School of Biomedical Engineering and Sciences   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Animal; Clinical; Enhancement; In vitro; Irreversible electroporation

Indexed keywords

ANIMALS; DISEASES; ELECTRODES; IMAGE ENHANCEMENT;

CLINICAL; CLINICAL APPLICATION; ELECTROPORATION; IN-VITRO; INTRA-OPERATIVE IMAGING; POTENTIAL BENEFITS; THERMAL INJURIES; TREATMENT PLANNING;

BLOOD VESSELS;

CYTOTOXIC AGENT;

ABLATION THERAPY; CANCER THERAPY; CLINICAL STUDY; CLINICAL TRIAL (TOPIC); ELECTRIC FIELD; ELECTRODE; ELECTROPORATION; HUMAN; IN VITRO STUDY; IRREVERSIBLE ELECTROPORATION; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; SYSTEMATIC REVIEW (TOPIC); TIME; TRANSLATIONAL RESEARCH; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE PERMEABILITY; ELECTROCHEMOTHERAPY; ELECTROMAGNETIC FIELD; ELECTROSTIMULATION THERAPY; EVIDENCE BASED MEDICINE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; TREATMENT OUTCOME;

ANIMALS; CELL MEMBRANE PERMEABILITY; ELECTRIC STIMULATION THERAPY; ELECTROCHEMOTHERAPY; ELECTROMAGNETIC FIELDS; EVIDENCE-BASED MEDICINE; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TREATMENT OUTCOME;

EID: 84919936112     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2014.2367543     Document Type: Review

References (151)

1. J. C. Weaver, "Electroporation of cells and tissues, " IEEE Trans. Plasma Sci., vol. 28, no. 1, pp. 24-33, Feb. 2000.
2. A. Ivorra and B. Rubinsky, Irreversible Electroporation. Berlin, Germany: Springer, 2010, pp. 1-21.
3. R. Stampfli, "Reversible electrical breakdown of the excitable membrane of a Ranvier node, " Acad. Bras. Cienc., vol. 30, pp. 57-63, 1958.
4. A. J. H. Sale and W. A. Hamilton, "Effects of high electric fields on microorganisms: I. Killing of bacteria and yeasts, " Biochim. Biophys. Acta BBA Gen. Subj., vol. 148, no. 3, pp. 781-788, Dec. 1967.
5. M. J. Jaroszeski et al., "In vivo gene delivery by electroporation, " Adv. Drug Del. Rev., vol. 35, no. 1, pp. 131-137, Jan. 1999.
6. L. M. Mir, "Therapeutic perspectives of in vivo cell electropermeabiliza-tion, " Bioelectrochemistry, vol. 53, no. 1, pp. 1-10, Jan. 2001.
7. J. Gehl, "Electroporation: Theory and methods, perspectives for drug delivery, gene therapy and research, " Acta Physiol. Scand., vol. 177, no. 4, pp. 437-447, Apr. 2003.
8. M. Okino and H. Mohri, "Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors, " Jpn. J. Cancer Res., vol. 78, no. 12, pp. 1319-1321, 1987.
9. D. Miklavcic et al., "Electrochemotherapy: From the drawing board into medical practice, " Biomed. Eng. OnLine, vol. 13, no. 1, p. 29, Mar. 2014.
10. R. Cadossi et al., "Locally enhanced chemotherapy by electroporation: Clinical experiences and perspective of use of electrochemotherapy, " Future Oncol., vol. 10, no. 5, pp. 877-890, Apr. 2014.
11. G. A. Hofmann et al., "Electroporation therapy: A new approach for the treatment of head and neck cancer, " IEEE Trans. Biomed. Eng., vol. 46, no. 6, pp. 752-759, Jun. 1999.
12. A. Gothelf et al., "Electrochemotherapy: Results of cancer treatment using enhanced delivery of bleomycin by electroporation, " Cancer Treat. Rev., vol. 29, no. 5, pp. 371-387, Oct. 2003.
13. G. Sersa et al., "Vascular disrupting action of electroporation and elec-trochemotherapy with bleomycin in murine sarcoma, " Brit. J. Cancer, vol. 98, no. 2, pp. 388-398, Jan. 2008.
14. L. M. Mira et al., "Standard operating procedures of the elec-trochemotherapy: Instructions for the use of bleomycin or cisplatin administered either systemically or locally and electric pulses delivered by the Cliniporator TM by means of invasive or non-invasive electrodes, " CR Acad. Sci. Paris, vol. 313, pp. 613-618, 2006.
15. R. V. Davalos et al., "Tissue ablation with irreversible electroporation, " Ann. Biomed. Eng., vol. 33, no. 2, pp. 223-231, Feb. 2005.
16. J. Rubinsky et al., "Optimal parameters for the destruction of prostate cancer using irreversible electroporation, " J. Urol., vol. 180, no. 6, pp. 2668-2674, Dec. 2008.
17. N. Bao et al., "Microfluidic electroporation of tumor and blood cells: Observation of nucleus expansion and implications on selective analysis and purging of circulating tumor cells, " Integr. Biol. Quantum Biosci. Nano Macro, vol. 2, no. 2-3, pp. 113-120, Mar. 2010.
18. L. Miller et al., "Cancer cells ablation with irreversible electro-poration, " Technol. Cancer Res. Treat., vol. 4, no. 6, pp. 699-705, Dec. 2005.
19. H. Shafiee et al., "Apreliminary studyto delineate irreversible electropo-ration from thermal damage using the Arrhenius equation, " J. Biomech. Eng., vol. 131, no. 7, pp. 074-509, Jul. 2009.
20. J. F. Edd et al., "In vivo results of a new focal tissue ablation technique: Irreversible electroporation, " IEEE Trans. Biomed. Eng., vol. 53, no. 7, pp. 1409-1415, Jul. 2006.
21. B. Al-Sakere et al., "Tumor ablation with irreversible electroporation, " PLoS ONE, vol. 2, no. 11, p. e1135, Nov. 2007.
22. P. A. Garcia et al., "Intracranial nonthermal irreversible electroporation: In vivo analysis, " J. Membr. Biol., vol. 236, no. 1, pp. 127-136, Jul. 2010.
23. B. Rubinsky et al., "Irreversible electroporation: A new ablation modality-clinical implications, " Technol. Cancer Res. Treat., vol. 6, no. 1, pp. 37-48, Feb. 2007.
24. G. Onik et al., "Irreversible electroporation: Implications for prostate ablation, " Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 295-300, Aug. 2007.
25. T. L. Ellis et al., "Nonthermal irreversible electroporation for intracranial surgical applications, " J. Neurosurg., vol. 114, no. 3, pp. 681-688, Mar. 2011.
26. A. Deodhar et al., "Renal tissue ablation with irreversible electro-poration: Preliminary results in a porcine model, " Urology, vol. 77, no. 3, pp. 754-760, Mar. 2011.
27. C. R. Tracy et al., "Irreversible electroporation (IRE): A novel method for renal tissue ablation, " BJU Int., vol. 107, no. 12, pp. 1982-1987, Jun. 2011.
28. Y. Guo et al., "Irreversible electroporation therapy in the liver: Longitudinal efficacy studies in a rat model of hepatocellular carcinoma, " Cancer Res., vol. 70, no. 4, pp. 1555-1563, Feb. 2010.
29. J. C. Weaver and Y. A. Chizmadzhev, "Theory of electroporation: A review, " Bioelectrochem. Bioenerg., vol. 41, no. 2, pp. 135-160, 1996.
30. R. C. Lee et al., "Transient and stable ionic permeabilization of isolated skeletal muscle cells after electrical shock, " J. Burn Care Res., vol. 14, no. 5, pp. 528-540, 1993.
31. A. Golberg and M. L. Yarmush, "Nonthermal irreversible electropora-tion: Fundamentals, applications, and challenges, " IEEE Trans. Biomed. Eng., vol. 60, no. 3, pp. 707-714, Mar. 2013.
32. J. C. Weaver et al., "A brief overview of electroporation pulse strength-duration space: A region where additional intracellular effects are expected, " Bioelectrochemistry, vol. 87, pp. 236-243, Oct. 2012.
33. C. Chen et al., "Membrane electroporation theories: A review, " Med. Biol. Eng. Comput., vol. 44, nos. 1/2, pp. 5-14, Mar. 2006.
34. N. Jourabchi et al., "Irreversible electroporation (NanoKnife) in cancer treatment, " Gastrointest. Interv., vol. 3, no. 1, pp. 8-18, Jun. 2014.
35. M. L. Yarmush et al., "Electroporation-based technologies for medicine: Principles, applications, and challenges, " Annu. Rev. Biomed. Eng., vol. 16, pp. 295-320, Jul. 2014.
36. R. C. Lee et al., "Biophysical injury mechanisms in electrical shock trauma, " Annu. Rev. Biomed. Eng., vol. 2, no. 1, pp. 477-509, 2000.
37. A. Ben-Or and B. Rubinsky, Irreversible Electroporation. Berlin, Germany: Springer, 2010, pp. 63-83.
38. T. Kotnik et al., "Cell membrane electroporation-Part 1: The phenomenon, " IEEE Electr. Insul. Mag., vol. 28, no. 5, pp. 14-23, Oct. 2012.
39. M. Pavlin et al., "Chapter seven electroporation of planar lipid bilayers and membranes, " in Advances in Planar Lipid Bilayers and Liposomes, vol. 6, A. Leitmannova Liu, Ed. San Francisco, CA, USA: Academic, 2008, pp. 165-226.
40. E. Neumann and K. Rosenheck, "Permeability changes induced by electric impulses in vesicular membranes, " J. Membr. Biol., vol. 10, no. 1, pp. 279-290, 1972.
41. I. G. Abiror et al., "246-electric breakdown of bilayer lipid membranes I. The main experimental facts and their qualitative discussion, " Bioelec-trochem. Bioenerg., vol. 6, no. 1, pp. 37-52, Mar. 1979.
42. V. F. Pastushenko et al., "247-electric breakdown of bilayer lipid membranes II. Calculation of the membrane lifetime in the steady-state diffusion approximation, " Bioelectrochem. Bioenerg., vol. 6, no. 1, pp. 53-62, Mar. 1979.
43. Y. Chizmadzhev et al., "248-electric breakdown of bilayer lipid membranes III. Analysis of possible mechanisms of defect origination, " Bioelectrochem. Bioenerg., vol. 6, no. 1, pp. 63-70, Mar. 1979.
44. V. F. Pastushenko et al., "249-electric breakdown of bilayer lipid membranes IV. Consideration of the kinetic stage in the case of the single-defect membrane, " Bioelectrochem. Bioenerg., vol. 6, no. 1, pp. 71-79, Mar. 1979.
45. V. Arakelyan et al., "250-electric breakdown of bilayer lipid membranes V. Consideration of the kinetic stage in the case of the membrane containing an arbitrary number of defects, " Bioelectrochem. Bioenerg., vol. 6, no. 1, pp. 81-87, Mar. 1979.
46. V. F. Pastushenko et al., "251-electric breakdown of bilayer lipid membranes VI. A stochastic theory taking into account the processes of defect formation and death: Membrane lifetime distribution function, " Bioelec-trochem. Bioenerg., vol. 6, no. 1, pp. 89-95, Mar. 1979.
47. R. Susil et al., "Electric field-induced transmembrane potential depends on cell density and organization, " Electromagn. Biol. Med., vol. 17, no. 3, pp. 391-399, 1998.
48. W. Krassowska and P. D. Filev, "Modeling electroporation in a single cell, " Biophys. J., vol. 92, no. 2, pp. 404-417, Jan. 2007.
49. G. Pucihar et al., "A time-dependent numerical model of transmem-brane voltage inducement and electroporation of irregularly shaped cells, " IEEE Trans. Biomed. Eng., vol. 56, no. 5, pp. 1491-1501, May 2009.
50. K. A. DeBruin and W. Krassowska, "Modeling electroporation in a single cell. I. Effects of field strength and rest potential, " Biophys. J., vol. 77, no. 3, pp. 1213-1224, 1999.
51. K. Kinosita Jr et al., "Electroporation of cell membrane visualized under a pulsed-laser fluorescence microscope, " Biophys. J., vol. 53, no. 6, pp. 1015-1019, Jun. 1988.
52. M. Hibino et al., "Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential, " Biophys. J., vol. 59, no. 1, pp. 209-220, Jan. 1991.
53. M. Hibino et al., "Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential, " Biophys. J., vol. 64, no. 6, pp. 1789-1800, Jun. 1993.
54. J. M. Crowley, "Electrical breakdown of bimolecular lipid membranes as an electromechanical instability, " Biophys. J., vol. 13, no. 7, pp. 711-724, Jul. 1973.
55. J. D. Litster, "Stability of lipid bilayers and red blood cell membranes, " Phys. Lett. A, vol. 53, no. 3, pp. 193-194, Jun. 1975.
56. C. Taupin et al., "Osmotic pressure-induced pores in phospholipid vesicles, " Biochemistry, vol. 14, no. 21, pp. 4771-4775, Oct. 1975.
57. J. C. Weaver and R. A. Mintzer, "Decreased bilayer stability due to transmembrane potentials, " Phys. Lett. A, vol. 86, no. 1, pp. 57-59, Oct. 1981.
58. C. Jiang et al., "Membrane-targeting approaches for enhanced cancer cell destruction with irreversible electroporation, " Ann. Biomed. Eng., vol. 42, no. 1, pp. 193-204, Jan. 2014.
59. K. T. Powell and J. C. Weaver, "Transient aqueous pores in bilayer membranes: A statistical theory, " Bioelectrochem. Bioenerg., vol. 15, no. 2, pp. 211-227, Apr. 1986.
60. M. Toner and E. G. Cravalho, "Kinetics and likelihood of membrane rupture during electroporation, " Phys. Lett. A, vol. 143, no. 8, pp. 409-412, Jan. 1990.
61. D. C. Chang and T. S. Reese, "Changes in membrane structure induced by electroporation as revealed by rapid-freezing electron microscopy, " Biophys. J., vol. 58, no. 1, pp. 1-12, Jul. 1990.
62. R. Benz et al., "Reversible electrical breakdown of lipid bilayer membranes: A charge-pulse relaxation study, " J. Membr. Biol., vol. 48, no. 2, pp. 181-204, Jun. 1979.
63. O. Tovar and L. Tung, "Electroporation and recovery of cardiac cell membrane with rectangular voltage pulses, " Amer. J. Physiol.-Heart Circ. Physiol., vol. 263, no. 4, pp. H1128-H1136, Oct. 1992.
64. A. Ivorra and B. Rubinsky, "In vivo electrical impedance measurements during and after electroporation of rat liver, " Bioelectrochemistry, vol. 70, no. 2, pp. 287-295, May 2007.
65. Y. Granot et al., "In vivo imaging of irreversible electroporation by means of electrical impedance tomography, " Phys. Med. Biol., vol. 54, no. 16, pp. 4927-4943, Aug. 2009.
66. R. Shirakashi et al., "Measurement of the permeability and resealing time constant of the electroporated mammalian cell membranes, " Int. J. Heat Mass Transf., vol. 47, no. 21, pp. 4517-4524, Oct. 2004.
67. W. Chen et al., "Supramembrane potential-induced electroconforma-tional changes in sodium channel proteins: A potential mechanism involved in electric injury, " Burns J. Int. Soc. Burn Inj., vol. 32, no. 1, pp. 52-59, Feb. 2006.
68. S. K. Frandsen et al., "Direct therapeutic applications of calcium electroporation to effectively induce tumor necrosis, " Cancer Res., vol. 72, no. 6, pp. 1336-1341, Mar. 2012.
69. H. Schoellnast et al., "The delayed effects of irreversible electroporation ablation on nerves, " Eur. Radiol., vol. 23, no. 2, pp. 375-380, Feb. 2013.
70. R. Heller et al., "Phase I/II trial for the treatment of cutaneous and subcutaneous tumors using electrochemotherapy, " Cancer, vol. 77, no. 5, pp. 964-971, 1998.
71. B. Alberts et al., Essential Cell Biology. New York, NY, USA: Garland Science, 2013.
72. G. L. Andreason and G. A. Evans, "Optimization of electroporation for transfection of mammalian cell lines, " Anal. Biochem., vol. 180, no. 2, pp. 269-275, Aug. 1989.
73. S. Y. Ho and G. S. Mittal, "Electroporation of cell membranes: A review, " Crit. Rev. Biotechnol., vol. 16, no. 4, pp. 349-362, 1996.
74. G. C. Troiano et al., "The reduction in electroporation voltages by the addition of a surfactant to planar lipid bilayers, " Biophys. J., vol. 75, no. 2, pp. 880-888, Aug. 1998.
75. P. Kramar et al., "A system for the determination of planar lipid bilayer breakdown voltage and its applications, " IEEE Trans. Nanobiosci., vol. 8, no. 2, pp. 132-138, Jun. 2009.
76. D. K. L. Cheng et al., "Nonuniform responses of transmembrane potential during electric field stimulation of single cardiac cells, " Amer. J. Physiol.-Heart Circ. Physiol., vol. 277, no. 1, pp. H351-H362, 1999.
77. A. V. Somlyo and A. P. Somlyo, "Electromechanical and pharmacome-chanical coupling in vascular smooth muscle, " J. Pharmacol. Exp. Ther., vol. 159, no. 1, pp. 129-145, Jan. 1968.
78. J. M. McMahon and D. J. Wells, "Electroporation for gene transfer to skeletal muscles: Current status, " BioDrugs, vol. 18, no. 3, pp. 155-165, 2004.
79. A. Lau et al., "A single cell electroporation chip, " Lab. Chip, vol. 5, no. 1, pp. 38-43, 2005.
80. J. Olofsson et al., "Single-cell electroporation, " Curr. Opin. Biotechnol., vol. 14, no. 1, pp. 29-34, 2003.
81. J. L. Rae and R. A. Levis, "Single-cell electroporation, " Pflüg. Arch. Eur. J. Physiol., vol. 443, no. 4, pp. 664-670, 2002.
82. M. Wang et al., "Single-cell electroporation, " Anal. Bioanal. Chem., vol. 397, no. 8, pp. 3235-3248, 2010.
83. R. Ziv et al., "Micro-electroporation of mesenchymal stem cells with alternating electrical current pulses, " Biomed. Microdevices, vol. 11, no. 1, pp. 95-101, Feb. 2009.
84. A. Kaner et al., "Model of pore formation in a single cell in a flow-through channel with micro-electrodes, " Biomed. Microdevices, vol. 16, pp. 181-189, Apr. 2014.
85. T. Y. Tsong, "Electroporation of cell membranes, " Biophys. J., vol. 60, no. 2, pp. 297-306, 1991.
86. K. Kinosita et al., "Events of membrane electroporation visualized on a time scale from microsecond to seconds, " in Guide to Electroporation Electrofusion. New York, NY, USA: Elsevier, 1992, pp. 29-46.
87. D. Gross et al., "Optical imaging of cell membrane potential changes induced by applied electric fields, " Biophys. J., vol. 50, no. 2, pp. 339-348, 1986.
88. Y. Rosemberg and R. Korenstein, "Electroporation of the photosynthetic membrane: A study by intrinsic and external optical probes, " Biophys. J., vol. 58, no. 4, pp. 823-832, 1990.
89. E. H. Serpersu et al., "Reversible and irreversible modification of ery-throcyte membrane permeability by electric field, " Biochim. Biophys. Acta BBA-Biomembr., vol. 812, no. 3, pp. 779-785, 1985.
90. R. V. Davalos et al., "A feasibility study for electrical impedance tomography as a means to monitor tissue electroporation for molecular medicine, " IEEE Trans. Biomed. Eng., vol. 49, no. 4, pp. 400-403, Apr. 2002.
91. R. V. Davalos et al., "Electrical impedance tomography for imaging tissue electroporation, " IEEE Trans. Biomed. Eng., vol. 51, no. 5, pp. 761-767, May 2004.
92. R. E. Neal et al., "Experimental characterization and numerical modeling of tissue electrical conductivity during pulsed electric fields for irreversible electroporation treatment planning, " IEEE Trans. Biomed. Eng., vol. 59, no. 4, pp. 1076-1085, Apr. 2012.
93. K. Kinosita Jr and T. Y. Tsong, "Voltage-induced conductance in human erythrocyte membranes, " Biochim. Biophys. Acta BBA-Biomembr., vol. 554, no. 2, pp. 479-497, 1979.
94. E. W. Lee et al., "Electron microscopic demonstration and evaluation of irreversible electroporation-induced nanopores on hepatocyte membranes, " J. Vasc. Interv. Radiol., vol. 23, no. 1, pp. 107-113, Jan. 2012.
95. A. Silve et al., "Comparison of the effects of the repetition rate between microsecond and nanosecond pulses: Electropermeabilization-induced electro-desensitization?" Biochim. Biophys. Acta BBA Gen. Subj., vol. 1840, no. 7, pp. 2139-2151, Jul. 2014.
96. C. Jiang et al., "Comparison of irreversible electroporation, cryo, and thermal ablations on cardiovascular cells, " presented at the Design Med. Devices Conf., Minneapolis, MN, USA, 2014.
97. Y. Guo et al., "Irreversible electroporation in the liver: Contrast-enhanced inversion-recovery MR imaging approaches to differentiate reversibly electroporated penumbra from irreversibly electroporated ablation zones, " Radiology, vol. 258, no. 2, pp. 461-468, Feb. 2011.
98. D. Miklavcic et al., "A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy, " Biochim. Biophys. Acta BBA Gen. Subj., vol. 1523, no. 1, pp. 73-83, Sep. 2000.
99. M. B. Sano et al., "Towards the creation of decellularized organ constructs using irreversible electroporation and active mechanical perfu-sion, " Biomed. Eng. Online, vol. 9, no. 1, p. 83, 2010.
100. M. A. Phillips et al., "Irreversible electroporation on the small intestine, " Brit. J. Cancer, vol. 106, no. 3, pp. 490-495, Jan. 2012.
101. C. B. Arena et al., "High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction, " Biomed. Eng. Online, vol. 10, p. 102, 2011.
102. P. A. Garcia et al., "A parametric study delineating irreversible electro-poration from thermal damage based on a minimally invasive intracranial procedure, " Biomed. Eng. Online, vol. 10, p. 34, 2011.
103. A. Deodhar et al., "Irreversible electroporation near the heart: Ventricular arrhythmias can be prevented with ECG synchronization, " Amer. J. Roentgenol., vol. 196, no. 3, pp. W330-W335, Mar. 2011.
104. J. J. Wendler et al., "Angiography in the isolated perfused kidney: Radiological evaluation of vascular protection in tissue ablation by nonthermal irreversible electroporation, " Cardiovasc. Intervent. Radiol., vol. 35, pp. 383-390, 2012.
105. B. Al-Sakere et al., "A study of the immunological response to tumor ablation with irreversible electroporation, " Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 301-306, Aug. 2007.
106. A. Ivorra et al., "In vivo electrical conductivity measurements during and after tumor electroporation: Conductivity changes reflect the treatment outcome, " Phys. Med. Biol., vol. 54, no. 19, pp. 5949-5963, Oct. 2009.
107. R. E. Neal 2nd et al., "Treatment of breast cancer through the application of irreversible electroporation using a novel minimally invasive single needle electrode, " Breast Cancer Res. Treat., vol. 123, no. 1, pp. 295-301, Aug. 2010.
108. Z. Qin et al., "Irreversible electroporation: An in vivo study with dorsal skin fold chamber, " Ann. Biomed. Eng., vol. 41, pp. 619-629, Mar. 2013.
109. P. A. Garcia et al., "Non-thermal irreversible electroporation (N-TIRE) and adjuvant fractionated radiotherapeutic multimodal therapy for in-tracranial malignant glioma in a canine patient, " Technol. Cancer Res. Treat., vol. 10, no. 1, pp. 73-83, Feb. 2011.
110. P. A. Garcia et al., "Electrical conductivity changes during irreversible electroporation treatment of brain cancer, " in Proc. IEEE Eng. Med. Biol. Soc. Annu. Int. Conf., 2011, pp. 739-742.
111. R. E. Neal 2nd et al., "Successful treatment of a large soft tissue sarcoma with irreversible electroporation, " J. Clin. Oncol., vol. 29, no. 13, pp. e372-e377, May 2011.
112. E. Maor et al., "The effect of irreversible electroporation on blood vessels, " Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 307-312, Aug. 2007.
113. E. Maor et al., "Non thermal irreversible electroporation: Novel technology for vascular smooth muscle cells ablation, " PLoS ONE, vol. 4, no. 3, p. e4757, Mar. 2009.
114. M. Phillips et al., "Nonthermal irreversible electroporation for tissue decellularization, " J. Biomech. Eng., vol. 132, no. 9, p. 091003, Sep. 2010.
115. M. Phillips et al., "Principles of tissue engineering with nonthermal irreversible electroporation, " J. Heat Transf., vol. 133, no. 1, p. 011004, 2011.
116. J. Lavee et al., "A novel nonthermal energy source for surgical epicar-dial atrial ablation: Irreversible electroporation, " in Proc. Heart Surgery Forum, 2007, vol. 10, pp. 162-167.
117. J. F. Edd and R. V. Davalos, "Mathematical modeling of irreversible electroporation for treatment planning, " Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 275-286, 2007.
118. R. Cannon et al., "Safety and early efficacy of irreversible electroporation for hepatic tumors in proximity to vital structures, " J. Surg. Oncol., vol. 107, no. 5, pp. 544-549, Apr. 2013.
119. P. A. Garcia et al., "A numerical investigation of the electric and thermal cell kill distributions in electroporation-based therapies in tissue, " PloS One, vol. 9, no. 8, p. e103083, 2014.
120. R. Goel et al., "TNF-α-based accentuation in cryoinjury-Dose, delivery, and response, " Mol. Cancer Ther., vol. 6, no. 7, pp. 2039-2047, Jul. 2007.
121. R. E. Neal II, "Spectrum of imaging and characteristics for liver tumors treated with irreversible electroporation, " J. Biomed. Sci. Eng., vol. 05, no. 12, pp. 813-818, 2012.
122. E. W. Lee et al., "Imaging guided percutaneous irreversible electropora-tion: ultrasound and immunohistological correlation, " Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 287-294, Aug. 2007.
123. L. Appelbaum et al., "US findings after irreversible electroporation ablation: Radiologic-pathologic correlation, " Radiology, vol. 262, no. 1, pp. 117-125, Jan. 2012.
124. J.E. Coad and J.C. Bischof, "Histologic differences between cryothermic and hyperthermic therapies, " Proc. SPIE, vol. 4954, p. 27, 2003.
125. C. C. Rupp et al., "Cryosurgical changes in the porcine kidney: Histologic analysis with thermal history correlation, " Cryobiology, vol. 45, no. 2, pp. 167-182, 2002.
126. N.Z. Wu et al., "Measurement of material extravasation in microvascular networks using fluorescence video-microscopy, " Microvasc. Res., vol. 46, no. 2, pp. 231-253, Sep. 1993.
127. K. Thomson, "Human experience with irreversible electroporation, " in Irreversible Electroporation, B. Rubinsky, Ed. Berlin, Germany: Springer, 2010, pp. 249-254.
128. M. Pech et al., "Irreversible electroporation of renal cell carcinoma: A first-in-man phase I clinical study, " Cardiovasc. Intervent. Radiol., vol. 34, no. 1, pp. 132-138, 2011.
129. K. R. Thomson et al., "Investigation of the safety of irreversible electroporation in humans, " J. Vasc. Interv. Radiol., vol. 22, no. 5, pp. 611-621, May 2011.
130. T. P. Kingham et al., "Ablation of perivascular hepatic malignant tumors with irreversible electroporation, " J. Am. Coll. Surg., vol. 215, no. 3, pp. 379-387, Sep. 2012.
131. P. Philips et al., "Irreversible electroporation ablation (IRE) of unre-sectable soft tissue tumors: Learning curve evaluation in the first 150 patients treated, " PLoS ONE, vol. 8, no. 11, p. e76260, Nov. 2013.
132. S. Robert et al., "Irreversible electroporation for unresectable hepatocel-lular carcinoma: Initial experience and review of safety and outcomes, " Technol. Cancer Res. Treat., vol. 12, no. 3, pp. 233-241, 2013.
133. R. C. G. Martin II et al., "Irreversible electroporation therapy in the management of locally advanced pancreatic adenocarcinoma, " J. Am. Coll. Surg., vol. 215, no. 3, pp. 361-369, Sep. 2012.
134. R. E. Neal et al., "In vivo characterization and numerical simulation of prostate properties for non-thermal irreversible electroporation ablation, " The Prostate, vol. 74, no. 5, pp. 458-468, May 2014.
135. R. C. G. Martin II et al., "Irreversible electroporation in locally advanced pancreatic cancer: Potential improved overall survival, " Ann. Surg. Oncol., vol. 20, no. 3, pp. 443-449, Dec. 2013.
136. H. J. Scheffer et al., "Irreversible electroporation for nonthermal tumor ablation in the clinical setting: A systematic review of safety and efficacy, " J. Vasc. Interv. Radiol., vol. 25, no. 7, pp. 997-1011, Jul. 2014.
137. B. Mali et al., "The effect of electroporation pulses on functioning of the heart, " Med. Biol. Eng. Comput., vol. 46, no. 8, pp. 745-757, Aug. 2008.
138. L. Solbiati et al., "Percutaneous radio-frequency ablation of hepatic metastases from colorectal cancer: Long-term results in 117 patients, " Radiology, vol. 221, no. 1, pp. 159-166, Oct. 2001.
139. E. K. Abdalla et al., "Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases, " Ann. Surg., vol. 239, no. 6, pp. 818-827, Jun. 2004.
140. A. S. Pearson et al., "Intraoperative radiofrequency ablation or cryoablation for hepatic malignancies, " Am. J. Surg., vol. 178, no. 6, pp. 592-598, Dec. 1999.
141. R. Goel et al., "Adjuvant approaches to enhance cryosurgery, " J. Biomech. Eng., vol. 131, no. 7, p. 074003, 2009.
142. C. Daniels and B. Rubinsky, "Electrical field and temperature model of nonthermal irreversible electroporation in heterogeneous tissues, " J. Biomech. Eng., vol. 131, no. 7, p. 071006, Jul. 2009.
143. C. B. Arena et al., "Theoretical considerations of tissue electroporation with high-frequency bipolar pulses, " IEEE Trans. Biomed. Eng., vol. 58, no. 5, pp. 1474-1482, May 2011.
144. M. Kanduser et al., "Effectofsurfactant polyoxyethylene glycol (C12E8) on electroporation of cell line DC3F, " Colloids Surf. Physicochem. Eng. Asp., vol. 214, no. 1, pp. 205-217, 2003.
145. C. Jiang et al., "An in vitro study on adjuvant enhanced irreversible elec-troporation, " presented at the Summer Bioengineering Conf., Farjardo, PR, USA, 2012.
146. S. N. Murthy et al., "Surfactant-enhanced transdermal delivery by elec-troporation, " J. Controlled Release, vol. 98, no. 2, pp. 307-315, Aug. 2004.
147. S. N. Murthy et al., "Cyclodextrin enhanced transdermal delivery of piroxicam and carboxyfluorescein by electroporation, " J. Controlled Release, vol. 99, no. 3, pp. 393-402, Oct. 2004.
148. G. C. Troiano et al., "The effects of gramicidin on electroporation of lipid bilayers, " Biophys. J., vol. 76, no. 6, pp. 3150-3157, Jun. 1999.
149. I. van Uitert et al., "The influence of different membrane components on the electrical stability of bilayer lipid membranes, " Biochim. Biophys. Acta BBA Biomembr., vol. 1798, no. 1, pp. 21-31, Jan. 2010.
150. J. C. Weaver et al., "Heparin alters transdermal transport associated with electroporation, " Biochem. Biophys. Res. Commun., vol. 234, no. 3, pp. 637-640, May 1997.
151. T. E. Zewert et al., "Creation of transdermal pathways for macro-molecule transport by skin electroporation and a low toxicity, pathway-enlarging molecule, " Bioelectrochem. Bioenerg., vol. 49, no. 1, pp. 11-20, Oct. 1999.