The role of irreversible electroporation (IRE) for locally advanced pancreatic cancer: a systematic review of safety and efficacy

References

• Bergenfeldt M, Andrén-Sandberg Å. Surgical treatment of pancreatic cancer. Eur Oncol Haematol. 2011;7:36–42.
   Google Scholar
• Balaban EP, Mangu PB, Khorana AA, et al. Locally advanced, unresectable pancreatic cancer: American Society of Clinical Oncology Clinical Practice Guideline. JCO. 2016;34:2654–2668.
   PubMed Web of Science ®Google Scholar
• D'Onofrio M, Barbi E, Girelli R, et al. Radiofrequency ablation of locally advanced pancreatic adenocarcinoma: an overview. World J Gastroenterol. 2010;16:3478–3483.
   PubMed Web of Science ®Google Scholar
• Girelli R, Frigerio I, Salvia R, et al. Feasibility and safety of radiofrequency ablation for locally advanced pancreatic cancer. Br J Surg. 2010;97:220–225.
   PubMed Web of Science ®Google Scholar
• Varshney S, Sewkani A, Sharma S, et al. Radiofrequency ablation of unresectable pancreatic carcinoma: feasibility, efficacy and safety. JOP. 2006;7:74–78.
   PubMedGoogle Scholar
• Wu Y, Tang Z, Fang H, et al. High operative risk of cool-tip radiofrequency ablation for unresectable pancreatic head cancer. J Surg Oncol. 2006;94:392–395.
   PubMed Web of Science ®Google Scholar
• Elias D, Baton O, Sideris L, et al. Necrotizing pancreatitis after radiofrequency destruction of pancreatic tumours. Eur J Surg Oncol. 2004;30:85–87.
   PubMed Web of Science ®Google Scholar
• Mann CD, Metcalfe MS, Lloyd DM, et al. The safety and efficacy of ablative techniques adjacent to the hepatic vasculature and biliary system. ANZ J Surg. 2010;80:41–49.
   PubMed Web of Science ®Google Scholar
• Zorbas G, Samaras T. A study of the sink effect by blood vessels in radiofrequency ablation. Comput Biol Med. 2015;57:182–186.
   PubMed Web of Science ®Google Scholar
• Davalos RV, Mir IL, Rubinsky B. Tissue ablation with irreversible electroporation. Ann Biomed Eng. 2005;33:223–231.
   PubMed Web of Science ®Google Scholar
• Bertacchini C, Margotti PM, Bergamini E, et al. Design of an irreversible electroporation system for clinical use. Technol Cancer Res Treat. 2007;6:313–320.
   PubMed Web of Science ®Google Scholar
• Bower M, Sherwood L, Li Y, et al. Irreversible electroporation of the pancreas: definitive local therapy without systemic effects. J Surg Oncol. 2011;104:22–28.
   PubMed Web of Science ®Google Scholar
• Choi JW, Lu DS, Osuagwu F, et al. Assessment of chronological effects of irreversible electroporation on hilar bile ducts in a porcine model. Cardiovasc Intervent Radiol. 2014;37:224–230.
   PubMed Web of Science ®Google Scholar
• Phillips M, Maor E, Rubinsky B. Nonthermal irreversible electroporation for tissue decellularization. J Biomech Eng. 2010;132:091003.
   PubMed Web of Science ®Google Scholar
• Charpentier KP, Wolf F, Noble L, et al. Irreversible electroporation of the pancreas in swine: a pilot study. HPB (Oxford). 2010;12:348–351.
   PubMed Web of Science ®Google Scholar
• Fritz S, Sommer CM, Vollherbst D, et al. Irreversible electroporation of the pancreas is feasible and safe in a porcine survival model. Pancreas. 2015;44:791–798.
   PubMed Web of Science ®Google Scholar
• Jose A, Sobrevals L, Ivorra A, et al. Irreversible electroporation shows efficacy against pancreatic carcinoma without systemic toxicity in mouse models. Cancer Lett. 2012;317:16–23.
   PubMed Web of Science ®Google Scholar
• Philips P, Li Y, Li S, et al. Efficacy of irreversible electroporation in human pancreatic adenocarcinoma: advanced murine model. Mol Ther Methods Clin Dev. 2015;2:15001.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, PRISMA Group, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.
   PubMed Web of Science ®Google Scholar
• National Institutes of Health/National Cancer Institute Common Terminology Criteria for Adverse Events (CTCAE) Version 4.03 https://evs.nci.nih.gov/ftp1/CTCAE/CTCAE_4.03_2010-06-14_QuickReference_8.5x11.pdf2010.
   Google Scholar
• 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;28:342–348.
   PubMed Web of Science ®Google Scholar
• Mansson C, Brahmstaedt R, Nilsson A, et al. Percutaneous irreversible electroporation for treatment of locally advanced pancreatic cancer following chemotherapy or radiochemotherapy. Eur J Surg Oncol. 2016;42:1401–1406.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Belfiore MP, Ronza FM, Romano F, et al. Percutaneous CT-guided irreversible electroporation followed by chemotherapy as a novel neoadjuvant protocol in locally advanced pancreatic cancer: our preliminary experience. Int J Surg. 2015;21 Suppl 1:S34–S39.
   PubMed Web of Science ®Google Scholar
• 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;262:486–494. Discussion 92–4.
   PubMed Web of Science ®Google Scholar
• 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;23:1736–1743.
   PubMed Web of Science ®Google Scholar
• 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;63:269–273.
   PubMed Web of Science ®Google Scholar
• Yan L, Chen YL, Su M, et al. A single-institution experience with open irreversible electroporation for locally advanced pancreatic carcinoma. Chin Med J. 2016;129:2920–2925.
   PubMed Web of Science ®Google Scholar
• 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:e12–ee4.
   PubMedGoogle Scholar
• 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;282:585–597.
   PubMed Web of Science ®Google Scholar
• Dunki-Jacobs EM, Philips P, Martin RC 2nd. Evaluation of thermal injury to liver, pancreas and kidney during irreversible electroporation in an in vivo experimental model. Br J Surg. 2014;101:1113–1121.
   PubMed Web of Science ®Google Scholar
• Faroja M, Ahmed M, Appelbaum L, et al. Irreversible electroporation ablation: is all the damage nonthermal? Radiology. 2013;266:462–470.
   PubMed Web of Science ®Google Scholar
• Ball C, Thomson KR, Kavnoudias H. Irreversible electroporation: a new challenge in “out of operating theater” anesthesia. Anesth Analg. 2010;110:1305–1309.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mansson C, Nilsson A, Karlson BM. Severe complications with irreversible electroporation of the pancreas in the presence of a metallic stent: a warning of a procedure that never should be performed. Acta Radiol Short Rep. 2014;3:2047981614556409.
   PubMedGoogle Scholar
• Dunki-Jacobs EM, Philips P, Martin RC 2nd. Evaluation of resistance as a measure of successful tumor ablation during irreversible electroporation of the pancreas. J Am Coll Surg. 2014;218:179–187.
   PubMed Web of Science ®Google Scholar
• Ivorra A, Al-Sakere B, Rubinsky B, et al. In vivo electrical conductivity measurements during and after tumor electroporation: conductivity changes reflect the treatment outcome. Phys Med Biol. 2009;54:5949–5963.
   PubMed Web of Science ®Google Scholar
• Cantore M, Girelli R, Mambrini A, et al. Combined modality treatment for patients with locally advanced pancreatic adenocarcinoma. Br J Surg. 2012;99:1083–1088.
   PubMed Web of Science ®Google Scholar
• Frigerio I, Girelli R, Giardino A, et al. Short term chemotherapy followed by radiofrequency ablation in stage III pancreatic cancer: results from a single center. J Hepatobiliary Pancreat Sci. 2013;20:574–577.
   PubMed Web of Science ®Google Scholar
• Matsui Y, Nakagawa A, Kamiyama Y, et al. Selective thermocoagulation of unresectable pancreatic cancers by using radiofrequency capacitive heating. Pancreas. 2000;20:14–20.
   PubMed Web of Science ®Google Scholar
• Spiliotis JD, Datsis AC, Michalopoulos NV, et al. Radiofrequency ablation combined with palliative surgery may prolong survival of patients with advanced cancer of the pancreas. Langenbecks Arch Surg. 2007;392:55–60.
   PubMed Web of Science ®Google Scholar
• Dholakia AS, Chaudhry M, Leal JP, et al. Baseline metabolic tumor volume and total lesion glycolysis are associated with survival outcomes in patients with locally advanced pancreatic cancer receiving stereotactic body radiation therapy. Int J Radiat Oncol Biol Phys. 2014;89:539–546.
   PubMed Web of Science ®Google Scholar
• Mahadevan A, Miksad R, Goldstein M, et al. Induction gemcitabine and stereotactic body radiotherapy for locally advanced nonmetastatic pancreas cancer. Int J Radiat Oncol Biol Phys. 2011;81:e615–e622.
   PubMed Web of Science ®Google Scholar
• Rwigema JC, Parikh SD, Heron DE, et al. Stereotactic body radiotherapy in the treatment of advanced adenocarcinoma of the pancreas. Am J Clin Oncol. 2011;34:63–69.
   PubMed Web of Science ®Google Scholar
• Seo Y, Kim MS, Yoo S, et al. Stereotactic body radiation therapy boost in locally advanced pancreatic cancer. Int J Radiat Oncol Biol Phys. 2009;75:1456–1461.
   PubMed Web of Science ®Google Scholar
• Gao HF, Wang K, Meng ZQ, et al. High intensity focused ultrasound treatment for patients with local advanced pancreatic cancer. Hepatogastroenterology. 2013;60:1906–1910.
   PubMedGoogle Scholar
• Xiong LL, Hwang JH, Huang XB, et al. Early clinical experience using high intensity focused ultrasound for palliation of inoperable pancreatic cancer. JOP. 2009;10:123–129.
   PubMedGoogle Scholar
• 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;21:447–452.
   PubMed Web of Science ®Google Scholar
• Burris HA 3rd, Moore MJ, Andersen J, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. JCO. 1997;15:2403–2413.
   PubMed Web of Science ®Google Scholar
• Poplin E, Feng Y, Berlin J, et al. Phase III, randomized study of gemcitabine and oxaliplatin versus gemcitabine (fixed-dose rate infusion) compared with gemcitabine (30-minute infusion) in patients with pancreatic carcinoma E6201: a trial of the Eastern Cooperative Oncology Group. JCO. 2009;27:3778–3785.
   PubMed Web of Science ®Google Scholar
• Rocha Lima CM, Green MR, Rotche R, et al. Irinotecan plus gemcitabine results in no survival advantage compared with gemcitabine monotherapy in patients with locally advanced or metastatic pancreatic cancer despite increased tumor response rate. JCO. 2004;22:3776–3783.
   PubMed Web of Science ®Google Scholar
• Conroy T, Paillot B, Francois E, et al. Irinotecan plus oxaliplatin and leucovorin-modulated fluorouracil in advanced pancreatic cancer – a Groupe Tumeurs Digestives of the Federation Nationale des Centres de Lutte Contre le Cancer study. JCO. 2005;23:1228–1236.
   PubMed Web of Science ®Google Scholar
• Von Hoff DD, Ervin T, Arena FP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369:1691–1703.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Hochster H, Stein S, et al. Gemcitabine plus nab-paclitaxel for advanced pancreatic cancer after first-line FOLFIRINOX: single institution retrospective review of efficacy and toxicity. Exp Hematol Oncol. 2015;4:29.
   PubMed Web of Science ®Google Scholar
• Gillen S, Schuster T, Meyer Zum Buschenfelde C, et al. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med. 2010;7:e1000267.
   PubMed Web of Science ®Google Scholar
• Martin RC 2nd, McFarland K, Ellis S, et al. Irreversible electroporation in locally advanced pancreatic cancer: potential improved overall survival. Ann Surg Oncol. 2013;20 Suppl 3:S443–S449.
   PubMed Web of Science ®Google Scholar
• Delpero JR, Bachellier P, Regenet N, et al. Pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: a French multicentre prospective evaluation of resection margins in 150 evaluable specimens. HPB (Oxford). 2014;16:20–33.
   PubMed Web of Science ®Google Scholar
• Esposito I, Kleeff J, Bergmann F, et al. Most pancreatic cancer resections are R1 resections. Ann Surg Oncol. 2008;15:1651–1660.
   PubMed Web of Science ®Google Scholar
• Jamieson NB, Chan NI, Foulis AK, et al. The prognostic influence of resection margin clearance following pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2013;17:511–521.
   PubMed Web of Science ®Google Scholar
• Menon KV, Gomez D, Smith AM, et al. Impact of margin status on survival following pancreatoduodenectomy for cancer: the Leeds Pathology Protocol (LEEPP). HPB (Oxford). 2009;11:18–24.
   PubMed Web of Science ®Google Scholar
• Strobel O, Hank T, Hinz U, et al. Pancreatic cancer surgery: the new R-status Counts. Ann Surg. 2017;265:565–573.
   PubMed Web of Science ®Google Scholar
• Loehrer PJ Sr, Feng Y, Cardenes H, et al. Gemcitabine alone versus gemcitabine plus radiotherapy in patients with locally advanced pancreatic cancer: an Eastern Cooperative Oncology Group trial. JCO. 2011;29:4105–4112.
   PubMed Web of Science ®Google Scholar
• Cardenes HR, Chiorean EG, Dewitt J, et al. Locally advanced pancreatic cancer: current therapeutic approach. Oncologist. 2006;11:612–623.
   PubMed Web of Science ®Google Scholar
• Neal RE 2nd, Rossmeisl JH Jr, Robertson JL, et al. Improved local and systemic anti-tumor efficacy for irreversible electroporation in immunocompetent versus immunodeficient mice. PLoS One. 2013;8:e64559.
   PubMed Web of Science ®Google Scholar