High-Voltage Electrical Pulses in Oncology: Irreversible Electroporation, Electrochemotherapy, Gene Electrotransfer, Electrofusion, and Electroimmunotherapy

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Table of Contents

Abstract

Irreversible electroporation, electrochemotherapy, and other electroporation-based therapies represent a treatment paradigm for difficult-to-treat solid tumors; the potent combination of high-voltage electrical pulses with immune cascade–enhancing drugs may offer a bridge between locoregional and systemic treatments in oncology.

This review summarizes the use of high-voltage electrical pulses (HVEPs) in clinical oncology to treat solid tumors with irreversible electroporation (IRE) and electrochemotherapy (ECT). HVEPs increase the membrane permeability of cells, a phenomenon known as electroporation. Unlike alternative ablative therapies, electroporation does not affect the structural integrity of surrounding tissue, thereby enabling tumors in the vicinity of vital structures to be treated. IRE uses HVEPs to cause cell death by inducing membrane disruption, and it is primarily used as a radical ablative therapy in the treatment of soft-tissue tumors in the liver, kidney, prostate, and pancreas. ECT uses HVEPs to transiently increase membrane permeability, enhancing cellular cytotoxic drug uptake in tumors. IRE and ECT show immunogenic effects that could be augmented when combined with immunomodulatory drugs, a combination therapy the authors term electroimmunotherapy. Additional electroporation-based technologies that may reach clinical importance, such as gene electrotransfer, electrofusion, and electroimmunotherapy, are concisely reviewed. HVEPs represent a substantial advancement in cancer research, and continued improvement and implementation of these presented technologies will require close collaboration between engineers, interventional radiologists, medical oncologists, and immuno-oncologists.

References

1. Nollet JA. Recherches sur les causes particulieres des phénoménes électriques. Paris, France: Chez H.L. Guerin & L.F. Delatour, 1754. Google Scholar

2. Doevenspeck H. Influencing cells and cell walls by electrostatic impulses. Fleishwirtshaft 1961;13:986–987. Google Scholar

3. Sitzmann W, Vorobiev E, Lebovka N. Pulsed Electric Fields for Food Industry: Historical Overview. In: Miklavčič D, ed. Handbook of Electroporation. Cham, Switzerland: Springer, 2017; 2335–2354. Crossref, Google Scholar

4. Sale AJ, Hamilton WA. Effects of High Electric Fields on Microorganisms. 1. Killing of Bacteria and Yeasts. Biochim Biophys Acta 1967;148(3):781–788. Crossref, Google Scholar

5. Hamilton WA, Sale AJH. Effects of High Electric Fields on Microorganisms. 2. Mechanism of Action of Lethal Effect. Biochim Biophys Acta 1967;148(3):789–800. Crossref, Google Scholar

6. Neumann E, Rosenheck K. Permeability changes induced by electric impulses in vesicular membranes. J Membr Biol 1972;10(3):279–290. Crossref, Medline, Google Scholar

7. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1982;1(7):841–845. Crossref, Medline, Google Scholar

8. Zimmermann U. Electric field-mediated fusion and related electrical phenomena. Biochim Biophys Acta 1982;694(3):227–277. Crossref, Medline, Google Scholar

9. Okino M, Mohri H. Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors. Jpn J Cancer Res 1987;78(12):1319–1321. Medline, Google Scholar

10. Davalos RV, Mir IL, Rubinsky B. Tissue ablation with irreversible electroporation. Ann Biomed Eng 2005;33(2):223–231. Crossref, Medline, Google Scholar

11. Yarmush ML, Golberg A, Serša G, Kotnik T, Miklavčič D. Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng 2014;16(1):295–320. Crossref, Medline, Google Scholar

12. Kotnik T, Miklavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophys J 2006;90(2):480–491. Crossref, Medline, Google Scholar

13. Kotnik T, Rems L, Tarek M, Miklavčič D. Membrane Electroporation and Electropermeabilization: Mechanisms and Models. Annu Rev Biophys 2019;48(1):63–91. Crossref, Medline, Google Scholar

14. Jarm T, Cemazar M, Miklavcic D, Sersa G. Antivascular effects of electrochemotherapy: implications in treatment of bleeding metastases. Expert Rev Anticancer Ther 2010;10(5):729–746. Crossref, Medline, Google Scholar

15. Markelc B, Sersa G, Cemazar M. Differential mechanisms associated with vascular disrupting action of electrochemotherapy: intravital microscopy on the level of single normal and tumor blood vessels. PLoS One 2013;8(3):e59557. Crossref, Google Scholar

16. Markelc B, Bellard E, Sersa G et al. Increased permeability of blood vessels after reversible electroporation is facilitated by alterations in endothelial cell-to-cell junctions. J Control Release 2018;276:30–41. Crossref, Medline, Google Scholar

17. Gehl J, Skovsgaard T, Mir LM. Vascular reactions to in vivo electroporation: characterization and consequences for drug and gene delivery. Biochim Biophys Acta 2002;1569(1-3):51–58. Crossref, Medline, Google Scholar

18. Rubinsky B, Onik G, Mikus P. Irreversible electroporation: a new ablation modality--clinical implications. Technol Cancer Res Treat 2007;6(1):37–48. Crossref, Medline, Google Scholar

19. Ringel-Scaia VM, Beitel-White N, Lorenzo MF et al. High-frequency irreversible electroporation is an effective tumor ablation strategy that induces immunologic cell death and promotes systemic anti-tumor immunity. EBioMedicine 2019;44:112–125. Crossref, Medline, Google Scholar

20. Gissel H, Lee RC, Gehl J. Electroporation and Cellular Physiology. In: Kee ST, Gehl J, Lee EW, eds. Clinical Aspects of Electroporation. New York, NY: Springer, 2011; 9–17. Crossref, Google Scholar

21. Vogel JA, van Veldhuisen E, Agnass P et al. Time-Dependent Impact of Irreversible Electroporation on Pancreas, Liver, Blood Vessels and Nerves: A Systematic Review of Experimental Studies. PLoS One 2016;11(11):e0166987 [Published correction appears in PLoS One 2017;12(3):e0174018.] doi.org/10.1371/journal.pone.0166987. Crossref, Medline, Google Scholar

22. Srimathveeravalli G, Cornelis F, Wimmer T et al. Normal Porcine Ureter Retains Lumen Wall Integrity but Not Patency Following Catheter-Directed Irreversible Electroporation: Imaging and Histologic Assessment over 28 Days. J Vasc Interv Radiol 2017;28(6):913–919.e1. Crossref, Medline, Google Scholar

23. Faroja M, Ahmed M, Appelbaum L et al. Irreversible electroporation ablation: is all the damage nonthermal? Radiology 2013;266(2):462–470. Link, Google Scholar

24. Garcia PA, Davalos RV, Miklavcic D. A numerical investigation of the electric and thermal cell kill distributions in electroporation-based therapies in tissue. PLoS One 2014;9(8):e103083. Crossref, Medline, Google Scholar

25. O’Brien TJ, Bonakdar M, Bhonsle S et al. Effects of internal electrode cooling on irreversible electroporation using a perfused organ model. Int J Hyperthermia 2018;35(1):44–55. Crossref, Medline, Google Scholar

26. Thomson KR, Cheung W, Ellis SJ et al. Investigation of the safety of irreversible electroporation in humans. J Vasc Interv Radiol 2011;22(5):611–621. Crossref, Medline, Google Scholar

27. Scheffer HJ, Nielsen K, van Tilborg AAJM et al. Ablation of colorectal liver metastases by irreversible electroporation: results of the COLDFIRE-I ablate-and-resect study. Eur Radiol 2014;24(10):2467–2475. Crossref, Medline, Google Scholar

28. Kourounis G, Paul Tabet P, Moris D et al. Irreversible electroporation (Nanoknife® treatment) in the field of hepatobiliary surgery: Current status and future perspectives. J BUON 2017;22(1):141–149. Medline, Google Scholar

29. Silk MT, Wimmer T, Lee KS et al. Percutaneous ablation of peribiliary tumors with irreversible electroporation. J Vasc Interv Radiol 2014;25(1):112–118. Crossref, Medline, Google Scholar

30. Scheffer HJ, Nielsen K, de Jong MC et al. Irreversible electroporation for nonthermal tumor ablation in the clinical setting: a systematic review of safety and efficacy. J Vasc Interv Radiol 2014;25(7):997–1011; quiz 1011. Crossref, Medline, Google Scholar

31. Ruarus AH, Vroomen LGPH, Puijk RS et al. Irreversible Electroporation in Hepatopancreaticobiliary Tumours. Can Assoc Radiol J 2018;69(1):38–50. Crossref, Medline, Google Scholar

32. Scheffer HJ, Vroomen LG, Nielsen K et al. Colorectal liver metastatic disease: efficacy of irreversible electroporation--a single-arm phase II clinical trial (COLDFIRE-2 trial). BMC Cancer 2015;15(1):772. Crossref, Medline, Google Scholar

33. Shady W, Petre EN, Gonen M et al. Percutaneous Radiofrequency Ablation of Colorectal Cancer Liver Metastases: Factors Affecting Outcomes--A 10-year Experience at a Single Center. Radiology 2016;278(2):601–611. Link, Google Scholar

34. Solbiati L, Ahmed M, Cova L, Ierace T, Brioschi M, Goldberg SN. Small liver colorectal metastases treated with percutaneous radiofrequency ablation: local response rate and long-term survival with up to 10-year follow-up. Radiology 2012;265(3):958–968. Link, Google Scholar

35. Moris D, Machairas N, Tsilimigras DI et al. Systematic Review of Surgical and Percutaneous Irreversible Electroporation in the Treatment of Locally Advanced Pancreatic Cancer. Ann Surg Oncol 2019;26(6):1657–1668. Crossref, Medline, Google Scholar

36. Narayanan G, Hosein PJ, Beulaygue IC et al. Percutaneous Image-Guided Irreversible Electroporation for the Treatment of Unresectable, Locally Advanced Pancreatic Adenocarcinoma. J Vasc Interv Radiol 2017;28(3):342–348. Crossref, Medline, Google Scholar

37. Leen E, Picard J, Stebbing J, Abel M, Dhillon T, Wasan H. Percutaneous irreversible electroporation with systemic treatment for locally advanced pancreatic adenocarcinoma. J Gastrointest Oncol 2018;9(2):275–281. Crossref, Medline, Google Scholar

38. Martin RC 2nd, 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(3):486–494; discussion 492–494. Crossref, Medline, Google Scholar

39. Ruarus AH, Vroomen LGPH, Geboers B et al. Percutaneous Irreversible Electroporation in Locally Advanced and Recurrent Pancreatic Cancer (PANFIRE-2): A Multicenter, Prospective, Single-Arm, Phase II Study. Radiology 2020;294(1):212–220. Link, Google Scholar

40. Scheffer HJ, Vroomen LG, de Jong MC et al. Ablation of Locally Advanced Pancreatic Cancer with Percutaneous Irreversible Electroporation: Results of the Phase I/II PANFIRE Study. Radiology 2017;282(2):585–597. Link, Google Scholar

41. Rombouts SJ, Walma MS, Vogel JA et al. Systematic Review of Resection Rates and Clinical Outcomes After FOLFIRINOX-Based Treatment in Patients with Locally Advanced Pancreatic Cancer. Ann Surg Oncol 2016;23(13):4352–4360. Crossref, Medline, Google Scholar

42. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet 2011;378(9791):607–620. Crossref, Medline, Google Scholar

43. Månsson C, Brahmstaedt R, Nygren P, Nilsson A, Urdzik J, Karlson BM. Percutaneous Irreversible Electroporation as First-line Treatment of Locally Advanced Pancreatic Cancer. Anticancer Res 2019;39(5):2509–2512. Crossref, Medline, Google Scholar

44. CROSSFIRE Trial: Comparing the Efficacy of Irreversible Electroporation With Radiotherapy. ClinicalTrials.gov/show/NCT02791503. Published June 6, 2016. Updated June 9, 2016. Accessed June 4, 2019. Google Scholar

45. Wendler JJ, Pech M, Köllermann J et al. Upper-Urinary-Tract Effects After Irreversible Electroporation (IRE) of Human Localised Renal-Cell Carcinoma (RCC) in the IRENE Pilot Phase 2a Ablate-and-Resect Study. Cardiovasc Intervent Radiol 2018;41(3):466–476. Crossref, Medline, Google Scholar

46. Buijs M, Zondervan PJ, de Bruin DM, van Lienden KP, Bex A, van Delden OM. Feasibility and safety of irreversible electroporation (IRE) in patients with small renal masses: Results of a prospective study. Urol Oncol 2019;37(3):183.e1–183.e8. Crossref, Google Scholar

47. Onik G, Rubinsky B. Irreversible Electroporation: First Patient Experience Focal Therapy of Prostate Cancer. In: Rubinsky B, ed. Irreversible Electroporation. Series in Biomedical Engineering. Berlin, Germany: Springer, 2010. Crossref, Google Scholar

48. Ting F, Tran M, Böhm M et al. Focal irreversible electroporation for prostate cancer: functional outcomes and short-term oncological control. Prostate Cancer Prostatic Dis 2016;19(1):46–52. Crossref, Medline, Google Scholar

49. 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(4):343–347. Crossref, Medline, Google Scholar

50. van den Bos W, Scheltema MJ, Siriwardana AR et al. Focal irreversible electroporation as primary treatment for localized prostate cancer. BJU Int 2018;121(5):716–724. Crossref, Medline, Google Scholar

51. Guenther E, Klein N, Zapf S et al. Prostate cancer treatment with Irreversible Electroporation (IRE): Safety, efficacy and clinical experience in 471 treatments. PLoS One 2019;14(4):e0215093. Crossref, Medline, Google Scholar

52. van den Bos W, Jurhill RR, de Bruin DM et al. Histopathological Outcomes after Irreversible Electroporation for Prostate Cancer: Results of an Ablate and Resect Study. J Urol 2016;196(2):552–559. Crossref, Medline, Google Scholar

53. Neal RE 2nd, Garcia PA, Kavnoudias H et al. In vivo irreversible electroporation kidney ablation: experimentally correlated numerical models. IEEE Trans Biomed Eng 2015;62(2):561–569. Crossref, Medline, Google Scholar

54. Marčan M, Pavliha D, Kos B, Forjanič T, Miklavčič D. Web-based tool for visualization of electric field distribution in deep-seated body structures and planning of electroporation-based treatments. Biomed Eng Online 2015;14(Suppl 3):S4. Crossref, Medline, Google Scholar

55. Groselj A, Kos B, Cemazar M et al. Coupling treatment planning with navigation system: a new technological approach in treatment of head and neck tumors by electrochemotherapy. Biomed Eng Online 2015;14(Suppl 3):S2. Crossref, Medline, Google Scholar

56. Scheffer HJ, Melenhorst MC, Echenique AM et al. Irreversible Electroporation for Colorectal Liver Metastases. Tech Vasc Interv Radiol 2015;18(3):159–169. Crossref, Medline, Google Scholar

57. Appelbaum L, Ben-David E, Sosna J, Nissenbaum Y, Goldberg SN. US findings after irreversible electroporation ablation: radiologic-pathologic correlation. Radiology 2012;262(1):117–125. Link, Google Scholar

58. Vieveen JM, Bouwman RA. Anaesthetic management during irreversible electroporation procedure. In: Meijerink M, Scheffer H, Narayanan G, eds. Irreversible Electroporation in Clinical Practice. Cham, Switzerland: Springer, 2018; 97–103. Crossref, Google Scholar

59. Deodhar A, Dickfeld T, Single GW et al. Irreversible electroporation near the heart: ventricular arrhythmias can be prevented with ECG synchronization. AJR Am J Roentgenol 2011;196(3):W330–W335. Crossref, Medline, Google Scholar

60. Dong S, Wang H, Zhao Y, Sun Y, Yao C. First Human Trial of High-Frequency Irreversible Electroporation Therapy for Prostate Cancer. Technol Cancer Res Treat 2018;17:1533033818789692. Crossref, Google Scholar

61. José A, Sobrevals L, Ivorra A, Fillat C. Irreversible electroporation shows efficacy against pancreatic carcinoma without systemic toxicity in mouse models. Cancer Lett 2012;317(1):16–23. Crossref, Medline, Google Scholar

62. Mole RH. Whole body irradiation; radiobiology or medicine? Br J Radiol 1953;26(305):234–241. Crossref, Medline, Google Scholar

63. Vogl TJ, Wissniowski TT, Naguib NN et al. Activation of tumor-specific T lymphocytes after laser-induced thermotherapy in patients with colorectal liver metastases. Cancer Immunol Immunother 2009;58(10):1557–1563. Crossref, Medline, Google Scholar

64. Bulvik BE, Rozenblum N, Gourevich S et al. Irreversible Electroporation versus Radiofrequency Ablation: A Comparison of Local and Systemic Effects in a Small-Animal Model. Radiology 2016;280(2):413–424. Link, Google Scholar

65. White SB, Zhang Z, Chen J, Gogineni VR, Larson AC. Early Immunologic Response of Irreversible Electroporation versus Cryoablation in a Rodent Model of Pancreatic Cancer. J Vasc Interv Radiol 2018;29(12):1764–1769. Crossref, Medline, Google Scholar

66. Shao Q, O’Flanagan S, Lam T et al. Engineering T cell response to cancer antigens by choice of focal therapeutic conditions. Int J Hyperthermia 2019;36(1):130–138. Crossref, Medline, Google Scholar

67. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5(4):263–274. Crossref, Medline, Google Scholar

68. Scheffer HJ, Stam AGM, Geboers B et al. Irreversible electroporation of locally advanced pancreatic cancer transiently alleviates immune suppression and creates a window for antitumor T cell activation. OncoImmunology 2019;8(11):1652532. Crossref, Medline, Google Scholar

69. Pandit H, Hong YK, Li Y et al. Evaluating the Regulatory Immunomodulation Effect of Irreversible Electroporation (IRE) in Pancreatic Adenocarcinoma. Ann Surg Oncol 2019;26(3):800–806. Crossref, Medline, Google Scholar

70. Miklavčič D, Mali B, Kos B, Heller R, Serša G. Electrochemotherapy: from the drawing board into medical practice. Biomed Eng Online 2014;13(1):29. Crossref, Medline, Google Scholar

71. Sersa G, Jarm T, Kotnik T et al. Vascular disrupting action of electroporation and electrochemotherapy with bleomycin in murine sarcoma. Br J Cancer 2008;98(2):388–398. Crossref, Medline, Google Scholar

72. Campana LG, Miklavčič D, Bertino G et al. Electrochemotherapy of superficial tumors - Current status: Basic principles, operating procedures, shared indications, and emerging applications. Semin Oncol 2019;46(2):173–191. Crossref, Medline, Google Scholar

73. Calvet CY, Mir LM. The promising alliance of anti-cancer electrochemotherapy with immunotherapy. Cancer Metastasis Rev 2016;35(2):165–177. Crossref, Medline, Google Scholar

74. Sersa G. The state-of-the-art of electrochemotherapy before the ESOPE study; advantages and clinical uses. Eur J Cancer Suppl 2006;4(11):52–59. Crossref, Google Scholar

75. Marty M, Sersa G, Garbay JR et al. Electrochemotherapy – An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. Eur J Cancer Suppl 2006;4(11):3–13. Crossref, Google Scholar

76. Gehl J, Sersa G, Matthiessen LW et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta Oncol 2018;57(7):874–882. Crossref, Medline, Google Scholar

77. Mali B, Jarm T, Snoj M, Sersa G, Miklavcic D. Antitumor effectiveness of electrochemotherapy: a systematic review and meta-analysis. Eur J Surg Oncol 2013;39(1):4–16. Crossref, Medline, Google Scholar

78. Miklavčič D, Serša G, Brecelj E et al. Electrochemotherapy: technological advancements for efficient electroporation-based treatment of internal tumors. Med Biol Eng Comput 2012;50(12):1213–1225. Crossref, Medline, Google Scholar

79. Garbe C, Peris K, Hauschild A et al. Diagnosis and treatment of melanoma. European consensus-based interdisciplinary guideline - Update 2016. Eur J Cancer 2016;63:201–217. Crossref, Medline, Google Scholar

80. Stratigos A, Garbe C, Lebbe C et al. Diagnosis and treatment of invasive squamous cell carcinoma of the skin: European consensus-based interdisciplinary guideline. Eur J Cancer 2015;51(14):1989–2007. Crossref, Medline, Google Scholar

81. Edhemovic I, Brecelj E, Gasljevic G et al. Intraoperative electrochemotherapy of colorectal liver metastases. J Surg Oncol 2014;110(3):320–327. Crossref, Medline, Google Scholar

82. Bertino G, Sersa G, De Terlizzi F et al. European Research on Electrochemotherapy in Head and Neck Cancer (EURECA) project: Results of the treatment of skin cancer. Eur J Cancer 2016;63:41–52. Crossref, Medline, Google Scholar

83. Probst U, Fuhrmann I, Beyer L, Wiggermann P. Electrochemotherapy as a New Modality in Interventional Oncology: A Review. Technol Cancer Res Treat 2018;17:1533033818785329. Crossref, Google Scholar

84. Granata V, Fusco R, Setola SV et al. Early radiological assessment of locally advanced pancreatic cancer treated with electrochemotherapy. World J Gastroenterol 2017;23(26):4767–4778. Crossref, Medline, Google Scholar

85. Tarantino L, Busto G, Nasto A et al. Electrochemotherapy of cholangiocellular carcinoma at hepatic hilum: A feasibility study. Eur J Surg Oncol 2018;44(10):1603–1609. Crossref, Medline, Google Scholar

86. Coletti L, Battaglia V, De Simone P, Turturici L, Bartolozzi C, Filipponi F. Safety and feasibility of electrochemotherapy in patients with unresectable colorectal liver metastases: A pilot study. Int J Surg 2017;44:26–32. Crossref, Medline, Google Scholar

87. Djokic M, Cemazar M, Popovic P et al. Electrochemotherapy as treatment option for hepatocellular carcinoma, a prospective pilot study. Eur J Surg Oncol 2018;44(5):651–657. Crossref, Medline, Google Scholar

88. Gasljevic G, Edhemovic I, Cemazar M et al. Histopathological findings in colorectal liver metastases after electrochemotherapy. PLoS One 2017;12(7):e0180709. Crossref, Medline, Google Scholar

89. Edhemovic I, Gadzijev EM, Brecelj E et al. Electrochemotherapy: a new technological approach in treatment of metastases in the liver. Technol Cancer Res Treat 2011;10(5):475–485. Crossref, Medline, Google Scholar

90. Bianchi G, Campanacci L, Ronchetti M, Donati D. Electrochemotherapy in the Treatment of Bone Metastases: A Phase II Trial. World J Surg 2016;40(12):3088–3094. Crossref, Medline, Google Scholar

91. Gasbarrini A, Campos WK, Campanacci L, Boriani S. Electrochemotherapy to Metastatic Spinal Melanoma: A Novel Treatment of Spinal Metastasis? Spine 2015;40(24):E1340–E1346. Crossref, Medline, Google Scholar

92. Calvet CY, Famin D, André FM, Mir LM. Electrochemotherapy with bleomycin induces hallmarks of immunogenic cell death in murine colon cancer cells. OncoImmunology 2014;3(4):e28131. Crossref, Medline, Google Scholar

93. Rosazza C, Meglic SH, Zumbusch A, Rols MP, Miklavcic D. Gene Electrotransfer: A Mechanistic Perspective. Curr Gene Ther 2016;16(2):98–129. Crossref, Medline, Google Scholar

94. Suschak JJ, Williams JA, Schmaljohn CS. Advancements in DNA vaccine vectors, non-mechanical delivery methods, and molecular adjuvants to increase immunogenicity. Hum Vaccin Immunother 2017;13(12):2837–2848. Crossref, Medline, Google Scholar

95. Cemazar M, Jarm T, Sersa G. Cancer electrogene therapy with interleukin-12. Curr Gene Ther 2010;10(4):300–311. Crossref, Medline, Google Scholar

96. Daud AI, DeConti RC, Andrews S et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 2008;26(36):5896–5903. Crossref, Medline, Google Scholar

97. Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat Rev Genet 2008;9(10):776–788. Crossref, Medline, Google Scholar

98. Yuan J, Ku GY, Adamow M et al. Immunologic responses to xenogeneic tyrosinase DNA vaccine administered by electroporation in patients with malignant melanoma. J Immunother Cancer 2013;1(1):20. Crossref, Medline, Google Scholar

99. Kim TJ, Jin HT, Hur SY et al. Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat Commun 2014;5(1):5317. Crossref, Medline, Google Scholar

100. Bagarazzi ML, Yan J, Morrow MP et al. Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci Transl Med 2012;4(155):155ra138. Crossref, Medline, Google Scholar

101. Eriksson F, Tötterman T, Maltais AK, Pisa P, Yachnin J. DNA vaccine coding for the rhesus prostate specific antigen delivered by intradermal electroporation in patients with relapsed prostate cancer. Vaccine 2013;31(37):3843–3848. Crossref, Medline, Google Scholar

102. Diaz CM, Chiappori A, Aurisicchio L et al. Phase 1 studies of the safety and immunogenicity of electroporated HER2/CEA DNA vaccine followed by adenoviral boost immunization in patients with solid tumors. J Transl Med 2013;11(1):62. Crossref, Medline, Google Scholar

103. Lopes A, Vandermeulen G, Préat V. Cancer DNA vaccines: current preclinical and clinical developments and future perspectives. J Exp Clin Cancer Res 2019;38(1):146. Crossref, Medline, Google Scholar

104. Rems L, Ušaj M, Kandušer M, Reberšek M, Miklavčič D, Pucihar G. Cell electrofusion using nanosecond electric pulses. Sci Rep 2013;3(1):3382. Crossref, Medline, Google Scholar

105. Rosenblatt J, Kufe D, Avigan D. Dendritic cell fusion vaccines for cancer immunotherapy. Expert Opin Biol Ther 2005;5(5):703–715. Crossref, Medline, Google Scholar

106. Datta J, Berk E, Cintolo JA, Xu S, Roses RE, Czerniecki BJ. Rationale for a Multimodality Strategy to Enhance the Efficacy of Dendritic Cell-Based Cancer Immunotherapy. Front Immunol 2015;6:271. Crossref, Medline, Google Scholar

107. Suzuki T, Fukuhara T, Tanaka M et al. Vaccination of dendritic cells loaded with interleukin-12-secreting cancer cells augments in vivo antitumor immunity: characteristics of syngeneic and allogeneic antigen-presenting cell cancer hybrid cells. Clin Cancer Res 2005;11(1):58–66. Medline, Google Scholar

108. Calvet CY, André FM, Mir LM. Dual therapeutic benefit of electroporation-mediated DNA vaccination in vivo: Enhanced gene transfer and adjuvant activity. OncoImmunology 2014;3(4):e28540. Crossref, Medline, Google Scholar

109. Tanis E, Nordlinger B, Mauer M et al. Local recurrence rates after radiofrequency ablation or resection of colorectal liver metastases. Analysis of the European Organisation for Research and Treatment of Cancer #40004 and #40983. Eur J Cancer 2014;50(5):912–919. Crossref, Medline, Google Scholar

110. Alnaggar M, Lin M, Mesmar A et al. Allogenic Natural Killer Cell Immunotherapy Combined with Irreversible Electroporation for Stage IV Hepatocellular Carcinoma: Survival Outcome. Cell Physiol Biochem 2018;48(5):1882–1893. Crossref, Medline, Google Scholar

111. Yang Y, Qin Z, Du D et al. Safety and Short-Term Efficacy of Irreversible Electroporation and Allogenic Natural Killer Cell Immunotherapy Combination in the Treatment of Patients with Unresectable Primary Liver Cancer. Cardiovasc Intervent Radiol 2019;42(1):48–59. Crossref, Medline, Google Scholar

112. Lin M, Liang S, Wang X et al. Percutaneous irreversible electroporation combined with allogeneic natural killer cell immunotherapy for patients with unresectable (stage III/IV) pancreatic cancer: a promising treatment. J Cancer Res Clin Oncol 2017;143(12):2607–2618. Crossref, Medline, Google Scholar

113. Zhao J, Wen X, Tian L et al. Irreversible electroporation reverses resistance to immune checkpoint blockade in pancreatic cancer. Nat Commun 2019;10(1):899. Crossref, Medline, Google Scholar

114. Belfiore G, Belfiore MP, Reginelli A et al. Concurrent chemotherapy alone versus irreversible electroporation followed by chemotherapy on survival in patients with locally advanced pancreatic cancer. Med Oncol 2017;34(3):38. Crossref, Medline, Google Scholar

115. Flak RV, Stender MT, Jensen TM et al. Treatment of locally advanced pancreatic cancer with irreversible electroporation - a Danish single center study of safety and feasibility. Scand J Gastroenterol 2019;54(2):252–258. Crossref, Medline, Google Scholar

116. Kluger MD, Epelboym I, Schrope BA et al. Single-Institution Experience with Irreversible Electroporation for T4 Pancreatic Cancer: First 50 Patients. Ann Surg Oncol 2016;23(5):1736–1743. Crossref, Medline, Google Scholar

117. Lambert L, Horejs J, Krska Z et al. Treatment of locally advanced pancreatic cancer by percutaneous and intraoperative irreversible electroporation: general hospital cancer center experience. Neoplasma 2016;63(2):269–273. Medline, Google Scholar

118. Månsson C, Brahmstaedt R, Nilsson A, Nygren P, Karlson BM. Percutaneous irreversible electroporation for treatment of locally advanced pancreatic cancer following chemotherapy or radiochemotherapy. Eur J Surg Oncol 2016;42(9):1401–1406. Crossref, Medline, Google Scholar

119. 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(2):90–97. Crossref, Medline, Google Scholar

120. Sugimoto K, Moriyasu F, Tsuchiya T et al. Irreversible Electroporation for Nonthermal Tumor Ablation in Patients with Locally Advanced Pancreatic Cancer: Initial Clinical Experience in Japan. Intern Med 2018;57(22):3225–3231. Crossref, Medline, Google Scholar

121. Vogel JA, Rombouts SJ, de Rooij T et al. Induction Chemotherapy Followed by Resection or Irreversible Electroporation in Locally Advanced Pancreatic Cancer (IMPALA): A Prospective Cohort Study. Ann Surg Oncol 2017;24(9):2734–2743. Crossref, Medline, Google Scholar

122. Yan L, Chen YL, Su M et al. A Single-institution Experience with Open Irreversible Electroporation for Locally Advanced Pancreatic Carcinoma. Chin Med J (Engl) 2016;129(24):2920–2925. Crossref, Medline, Google Scholar

123. Zhang Y, Shi J, Zeng J et al. Percutaneous Irreversible Electroporation for Ablation of Locally Advanced Pancreatic Cancer: Experience From a Chinese Institution. Pancreas 2017;46(2):e12–e14. Crossref, Medline, Google Scholar

124. Ahmed M, Solbiati L, Brace CL et al. Image-guided tumor ablation: standardization of terminology and reporting criteria--a 10-year update. Radiology 2014;273(1):241–260. Link, Google Scholar

125. Bhutiani N, Philips P, Scoggins CR, McMasters KM, Potts MH, Martin RC. Evaluation of tolerability and efficacy of irreversible electroporation (IRE) in treatment of Child-Pugh B (7/8) hepatocellular carcinoma (HCC). HPB 2016;18(7):593–599. Crossref, Medline, Google Scholar

126. Cannon R, Ellis S, Hayes D, Narayanan G, Martin RC 2nd. Safety and early efficacy of irreversible electroporation for hepatic tumors in proximity to vital structures. J Surg Oncol 2013;107(5):544–549. Crossref, Medline, Google Scholar

127. Fruhling P, Nilsson A, Duraj F, Haglund U, Noren A. Single-center nonrandomized clinical trial to assess the safety and efficacy of irreversible electroporation (IRE) ablation of liver tumors in humans: Short to mid-term results. Eur J Surg Oncol 2017;43(4):751–757. Crossref, Medline, Google Scholar

128. Hosein PJ, Echenique A, Loaiza-Bonilla A et al. Percutaneous irreversible electroporation for the treatment of colorectal cancer liver metastases with a proposal for a new response evaluation system. J Vasc Interv Radiol 2014;25(8):1233–1239.e2. Crossref, Medline, Google Scholar

129. Kingham TP, Karkar AM, D’Angelica MI et al. Ablation of perivascular hepatic malignant tumors with irreversible electroporation. J Am Coll Surg 2012;215(3):379–387. Crossref, Medline, Google Scholar

130. Narayanan G, Bhatia S, Echenique A, Suthar R, Barbery K, Yrizarry J. Vessel patency post irreversible electroporation. Cardiovasc Intervent Radiol 2014;37(6):1523–1529. Crossref, Medline, Google Scholar

131. 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(5):694–702. Crossref, Medline, Google Scholar

132. Niessen C, Beyer LP, Pregler B et al. Percutaneous Ablation of Hepatic Tumors Using Irreversible Electroporation: A Prospective Safety and Midterm Efficacy Study in 34 Patients. J Vasc Interv Radiol 2016;27(4):480–486. Crossref, Medline, Google Scholar

133. Niessen C, Thumann S, Beyer L et al. Percutaneous Irreversible Electroporation: Long-term survival analysis of 71 patients with inoperable malignant hepatic tumors. Sci Rep 2017;7(1):43687. Crossref, Medline, Google Scholar

134. Philips P, Hays D, Martin RC. Irreversible electroporation ablation (IRE) of unresectable soft tissue tumors: learning curve evaluation in the first 150 patients treated. PLoS One 2013;8(11):e76260. Crossref, Medline, Google Scholar

135. Canvasser NE, Sorokin I, Lay AH et al. Irreversible electroporation of small renal masses: suboptimal oncologic efficacy in an early series. World J Urol 2017;35(10):1549–1555. Crossref, Medline, Google Scholar

136. 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(1):132–138. Crossref, Medline, Google Scholar

137. 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. Crossref, Medline, Google Scholar

Article History

Received: Sept 30 2019
Revision requested: Nov 18 2019
Revision received: Dec 18 2019
Accepted: Dec 23 2019
Published online: Mar 24 2020

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High-Voltage Electrical Pulses in Oncology: Irreversible Electroporation, Electrochemotherapy, Gene Electrotransfer, Electrofusion, and Electroimmunotherapy

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High-Voltage Electrical Pulses in Oncology: Irreversible Electroporation, Electrochemotherapy, Gene Electrotransfer, Electrofusion, and Electroimmunotherapy

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