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Electrochemotherapy, a new antitumor treatment. First clinical phase I‐II trial
First published: 15 December 1993
Cited by: 211
Abstract
Background. Electrochemotherapy is a new antitumor treatment consisting of electrical pulses administered to the tumor several minutes after intravenous injection of bleomycin. In mice, important antitumor effects were observed on subcutaneously transplanted tumors and on spontaneously occurring mammary carcinomas. Cures were obtained after one single treatment combining bleomycin and electric pulses. In humans, permeation nodules seemed an adequate oncologic situation to assay this new procedure. The authors report the first Phase I‐II trial of electrochemotherapy.
Methods. Eight patients with 40 permeation nodules of head and neck squamous cell carcinomas were treated with 10 mg/m2 bleomycin intravenous bolus, followed by four or eight short (100 μseconds) and intense (1300 V/cm) pulses administered through two external electrodes located on each side of the treated nodule.
Results. An instantaneous painless contraction of the underlying muscles was regularly observed. Neither local nor general side effects were observed, and electrochemotherapy was well tolerated. In addition, a clear local antitumor efficacy was found: 23 (57%) nodules were in clinical complete response within a few days.
Conclusion. The absence of toxicity, the good tolerance by the patients, and the net antitumor effects observed are encouraging for additional electrochemotherapy developments in clinical oncology.
Citing Literature
Number of times cited: 211
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- Tei‐ichiro Ueki, Hiroji Uemura, Yoji Nagashima, Shinsuke Ohta, Hitoshi Ishiguro and Yoshinobu Kubota, Antitumour effect of electrochemotherapy with bleomycin on human prostate cancer xenograft, BJU International, 102, 10, (1467-1471), (2008).
- Rainer A. Böckmann, Bert L. de Groot, Sergej Kakorin, Eberhard Neumann and Helmut Grubmüller, Kinetics, Statistics, and Energetics of Lipid Membrane Electroporation Studied by Molecular Dynamics Simulations, Biophysical Journal, 10.1529/biophysj.108.129437, 95, 4, (1837-1850), (2008).
- Mira Sadadcharam, Declan M. Soden and Gerald C. O'sullivan, Electrochemotherapy: An emerging cancer treatment, International Journal of Hyperthermia, 24, 3, (263), (2008).
- John O. Larkin, Christopher G. Collins, Simon Aarons, Mark Tangney, Maria Whelan, Seamus O??Reily, Oscar Breathnach, Declan M. Soden and Gerald C. O??Sullivan, Electrochemotherapy, Annals of Surgery, 245, 3, (469), (2007).
- Yoshitaka Isaka and Enyu Imai, Electroporation-mediated gene therapy, Expert Opinion on Drug Delivery, 10.1517/17425247.4.5.561, 4, 5, (561-571), (2007).
- Shirley W.I. Siu and Rainer A. Böckmann, Electric field effects on membranes: Gramicidin A as a test ground, Journal of Structural Biology, 157, 3, (545), (2007).
- Erim Bešić, Physical mechanisms and methods employed in drug delivery to tumors, Acta Pharmaceutica, 57, 3, (2007).
- Alain Luxembourg, Claire F Evans and Drew Hannaman, Electroporation-based DNA immunisation: translation to the clinic, Expert Opinion on Biological Therapy, 10.1517/14712598.7.11.1647, 7, 11, (1647-1664), (2007).
- Bassim Al-Sakere, Franck André, Claire Bernat, Elisabeth Connault, Paule Opolon, Rafael V. Davalos, Boris Rubinsky, Lluis M. Mir and Mark Isalan, Tumor Ablation with Irreversible Electroporation, PLoS ONE, 2, 11, (e1135), (2007).
- David Cukjati, Danute Batiuskaite, Franck André, Damijan Miklavčič and Lluis M. Mir, Real time electroporation control for accurate and safe in vivo non-viral gene therapy, Bioelectrochemistry, 70, 2, (501), (2007).
- K.C. Smith, T.R. Gowrishankar, A.T. Esser, D.A. Stewart and J.C. Weaver, The Spatially Distributed Dynamic Transmembrane Voltage of Cells and Organelles due to 10 ns Pulses: Meshed Transport Networks, IEEE Transactions on Plasma Science, 34, 4, (1394), (2006).
- Enrico P. Spugnini, Alfonso Baldi, Bruno Vincenzi, Franco Bongiorni, Corrado Bellelli, Gennaro Citro and Alessandro Porrello, Intraoperative versus postoperative electrochemotherapy in high grade soft tissue sarcomas: a preliminary study in a spontaneous feline model, Cancer Chemotherapy and Pharmacology, 59, 3, (375), (2006).
- R. Giardino, M. Fini, V. Bonazzi, R. Cadossi, A Nicolini and A. Carpi, Electrochemotherapy a novel approach to the treatment of metastatic nodules on the skin and subcutaneous tissues, Biomedicine & Pharmacotherapy, 10.1016/j.biopha.2006.07.016, 60, 8, (458-462), (2006).
- Declan M. Soden, John O. Larkin, Christopher G. Collins, Mark Tangney, Simon Aarons, John Piggott, Anthony Morrissey, Colum Dunne and Gerald C. O'Sullivan, Successful application of targeted electrochemotherapy using novel flexible electrodes and low dose bleomycin to solid tumours, Cancer Letters, 232, 2, (300), (2006).
- Ayman Al-Hendy and Salama Salama, Gene therapy and uterine leiomyoma: a review, Human Reproduction Update, 12, 4, (385), (2006).
- L.M. Mir, Bases and rationale of the electrochemotherapy, European Journal of Cancer Supplements, 4, 11, (38), (2006).
- Gregor Sersa, The state-of-the-art of electrochemotherapy before the ESOPE study; advantages and clinical uses, European Journal of Cancer Supplements, 4, 11, (52), (2006).
- Christopher M Byrne and John F Thompson, Role of electrochemotherapy in the treatment of metastatic melanoma and other metastatic and primary skin tumors, Expert Review of Anticancer Therapy, 6, 5, (671), (2006).
- Marie-Pierre Rols, Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1758, 3, (423), (2006).
- B.M. Tijink, R. De Bree, G.A.M.S. Van Dongen and C.R. Leemans, How we do it: Chemo‐electroporation in the head and neck for otherwise untreatable patients, Clinical Otolaryngology, 31, 5, (447-451), (2006).
- Maria C. Whelan, John O. Larkin, Christopher G. Collins, James Cashman, Oscar Breathnach, Declan M. Soden and Gerald C. O’Sullivan, Effective treatment of an extensive recurrent breast cancer which was refractory to multimodal therapy by multiple applications of electrochemotherapy, European Journal of Cancer Supplements, 4, 11, (32), (2006).
- Mahmut Tokmakçı, A High-Voltage Pulse Generation Instrument for Electrochemotherapy Method, Journal of Medical Systems, 30, 3, (145), (2006).
- Gustav Grafström, Per Engström, Leif G. Salford and Bertil R.R. Persson, 99m Tc-DTPA Uptake and Electrical Impedance Measurements in Verification of In Vivo Electropermeabilization Efficiency in Rat Muscle , Cancer Biotherapy & Radiopharmaceuticals, 10.1089/cbr.2006.21.623, 21, 6, (623-635), (2006).
- Gintautas Saulis, Remigijus Lapė, Rita Pranevičiūtė and Donatas Mickevičius, Changes of the solution pH due to exposure by high-voltage electric pulses, Bioelectrochemistry, 67, 1, (101), (2005).
- J. Teissie, M. Golzio and M.P. Rols, Mechanisms of cell membrane electropermeabilization: A minireview of our present (lack of ?) knowledge, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/j.bbagen.2005.05.006, 1724, 3, (270-280), (2005).
- Emilie Phez, Cécile Faurie, Muriel Golzio, Justin Teissié and Marie-Pierre Rols, New insights in the visualization of membrane permeabilization and DNA/membrane interaction of cells submitted to electric pulses, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/j.bbagen.2005.04.005, 1724, 3, (248-254), (2005).
- S.
M. Becker, Numerical Modeling of
In Vivo Plate Electroporation Thermal Dose Assessment, Journal of Biomechanical Engineering, 128, 1, (76), (2005). - C. Faurie, M. Golzio, E. Phez, J. Teissié and M.‐P. Rols, Electric Field‐Induced Cell Membrane Permeabilization and Gene Transfer: Theory and Experiments, Engineering in Life Sciences, 5, 2, (179-186), (2005).
- S. Šatkauskas, D. Batiuškaitė, S. Šalomskaitė-Davalgienė and M.S. Venslauskas, Effectiveness of tumor electrochemotherapy as a function of electric pulse strength and duration, Bioelectrochemistry, 65, 2, (105), (2005).
- Kenichi Isobe, Tominaga Shimizu, Toshio Nikaido and Kunio Takaoka, Low-Voltage Electrochemotherapy with Low-Dose Methotrexate Enhances Survival in Mice with Osteosarcoma, Clinical Orthopaedics and Related Research, 426, (226), (2004).
- F André and L M Mir, DNA electrotransfer: its principles and an updated review of its therapeutic applications, Gene Therapy, 10.1038/sj.gt.3302367, 11, S1, (S33-S42), (2004).
- Mateja Gabrijel, Urška Repnik, Marko Kreft, Sonja Grilc, Matjaž Jeras and Robert Zorec, Quantification of cell hybridoma yields with confocal microscopy and flow cytometry, Biochemical and Biophysical Research Communications, 10.1016/j.bbrc.2003.12.154, 314, 3, (717-723), (2004).
- Jody A. White, Peter F. Blackmore, Karl H. Schoenbach and Stephen J. Beebe, Stimulation of Capacitative Calcium Entry in HL-60 Cells by Nanosecond Pulsed Electric Fields, Journal of Biological Chemistry, 279, 22, (22964), (2004).
- Anita Gothelf, Lluis M Mir and Julie Gehl, Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation, Cancer Treatment Reviews, 29, 5, (371), (2003).
- Tominaga Shimizu, Toshio Nikaido, Hiroki Gomyo, Yasuo Yoshimura, Akiko Horiuchi, Kenichi Isobe, Sohei Ebara, Kunio Takaoka and Sohei Ebara, Electrochemotherapy for digital chondrosarcoma, Journal of Orthopaedic Science, 8, 2, (248), (2003).
- Stephen J. Beebe, Jody White, Peter F. Blackmore, Yuping Deng, Kenneth Somers and Karl H. Schoenbach, Diverse Effects of Nanosecond Pulsed Electric Fields on Cells and Tissues, DNA and Cell Biology, 22, 12, (785), (2003).
- Leaf Huang and Vivian Wai-Yan Lui, Nonviral Approaches for Cancer Gene Therapy, Pharmaceutical Gene Delivery Systems, 10.1201/9780203912331.ch11, (2009).
- J. Gehl, Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research, Acta Physiologica Scandinavica, 177, 4, (437-447), (2003).
- R. Gopal, A.A. Narkar, K.P. Mishra, A.M. Samuel and N. Nair, Electroporation: a novel approach to enhance the radioiodine uptake in a human thyroid cancer cell line, Applied Radiation and Isotopes, 59, 5-6, (305), (2003).
- Ann E. O. Trezise, In VivoDNA Electrotransfer, DNA and Cell Biology, 21, 12, (869), (2002).
- Julie Gehl, Torben Skovsgaard and Lluis M Mir, Vascular reactions to in vivo electroporation: characterization and consequences for drug and gene delivery, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/S0304-4165(01)00233-1, 1569, 1-3, (51-58), (2002).
- M.J Jaroszeski, D Coppola, C Pottinger, K Benson, R.A Gilbert and R Heller, Treatment of hepatocellular carcinoma in a rat model using electrochemotherapy, European Journal of Cancer, 37, 3, (422), (2001).
- Jukka Hartikka, Loretta Sukhu, Carol Buchner, Diane Hazard, Vesselina Bozoukova, Michal Margalith, Walter K. Nishioka, Carl J. Wheeler, Marston Manthorp and Michael Sawdey, Electroporation-Facilitated Delivery of Plasmid DNA in Skeletal Muscle: Plasmid Dependence of Muscle Damage and Effect of Poloxamer 188, Molecular Therapy, 10.1006/mthe.2001.0483, 4, 5, (407-415), (2001).
- Sergio Rodrı́guez-Cuevas, Sinuhe Barroso-Bravo, Javier Almanza-Estrada, Lourdes Cristóbal-Martı́nez and Enrique González-Rodrı́guez, Electrochemotherapy in Primary and Metastatic Skin Tumors, Archives of Medical Research, 32, 4, (273), (2001).
- Yasuo Shinoda, Takeshi Suzuki, Minako Sugawara-Yokoo, Shinya Nagamatsu, Hiroyuki Kuwano and Kuniaki Takata, Expression of Sugar Transporters by In Vivo Electroporation and Particle Gun Methods in the Rat Liver: Localization to Specific Membrane Domains., ACTA HISTOCHEMICA ET CYTOCHEMICA, 34, 1, (15), (2001).
- Makiya Nishikawa and Leaf Huang, Nonviral Vectors in the New Millennium: Delivery Barriers in Gene Transfer, Human Gene Therapy, 12, 8, (861), (2001).
- Joseph P. Allegretti and William R. Panje, Electroporation Therapy for Head and Neck Cancer Including Carotid Artery Involvement, The Laryngoscope, 111, 1, (52-56), (2009).
- Minoru Tomizawa, Masaaki Ebara, Hiromitsu Saisho, Shigeru Sakiyama and Masatoshi Tagawa, Irradiation with ultrasound of low output intensity increased chemosensitivity of subcutaneous solid tumors to an anti-cancer agent, Cancer Letters, 173, 1, (31), (2001).
- Lluis M Mir, Therapeutic perspectives of in vivo cell electropermeabilization, Bioelectrochemistry, 53, 1, (1), (2001).
- M. Lee Lucas, Mark J. Jaroszeski, Richard Gilbert and Richard Heller, In VivoElectroporation Using an Exponentially Enhanced Pulse: A New Waveform, DNA and Cell Biology, 20, 3, (183), (2001).
- M.J. Jaroszeski, D. Coppola, G. Nesmith, C. Pottinger, M. Hyacinthe, K. Benson, R. Gilbert and R. Heller, Effects of electrochemotherapy with bleomycin on normal liver tissue in a rat model, European Journal of Cancer, 37, 3, (414), (2001).
- Akiko Horiuchi, Toshio Nikaido, Junji Mitsushita, Toshihiko Toki, Ikuo Konishi and Shingo Fujii, Enhancement of antitumor effect of bleomycin by low‐voltage in vivo electroporation: A study of human uterine leiomyosarcomas in nude mice, International Journal of Cancer, 88, 4, (640-644), (2000).
- Stella Somiari, Jill Glasspool-Malone, Joseph J. Drabick, Richard A. Gilbert, Richard Heller, Mark J. Jaroszeski and Robert W. Malone, Theory and in Vivo Application of Electroporative Gene Delivery, Molecular Therapy, 2, 3, (178), (2000).
- Toru Horikoshi, Hirofumi Naganuma, Yasuhiro Ohashi, Takehiko Ueno and Hideaki Nukui, Enhancing effect of electric stimulation on cytotoxicity of anticancer agents against rat and human glioma cells, Brain Research Bulletin, 51, 5, (371), (2000).
- J. M. Vicat, S. Boisseau, P. Jourdes, M. Laine, D. Wion, R. Bouali-Benazzouz, A. L. Benabid and F. Berger, Brief Report: Muscle Transfection by Electroporation with High-Voltage and Short-Pulse Currents Provides High-Level and Long-Lasting Gene Expression, Human Gene Therapy, 11, 6, (909), (2000).
- T. Goto, T. Nishi, T. Tamura, S. B. Dev, H. Takeshima, M. Kochi, K. Yoshizato, J.-i. Kuratsu, T. Sakata, G. A. Hofmann and Y. Ushio, Highly efficient electro-gene therapy of solid tumor by using an expression plasmid for the herpes simplex virus thymidine kinase gene, Proceedings of the National Academy of Sciences, 97, 1, (354), (2000).
- Mark J Jaroszeski, Vu Dang, Carlos Pottinger, Joseph Hickey, Richard Gilbert and Richard Heller, Toxicity of anticancer agents mediated by electroporation in vitro, Anti-Cancer Drugs, 11, 3, (201), (2000).
- Susumu Omura, Yoshiharu Tsuyuki, Shinsuke Ohta, Xianqi Li, Hiroki Bukawa and Kiyohide Fujita, Rapid tumor necrosis induced by electrochemotherapy with intratumoral injection of bleomycin in a hamster tongue cancer model, International Journal of Oral and Maxillofacial Surgery, 29, 2, (119), (2000).
- M. -P. Rols, J. -M. Bachaud, P. Giraud, C. Chevreau, H. Roché and J. Teissié, Electrochemotherapy of cutaneous metastases in malignant melanoma, Melanoma Research, 10, 5, (468), (2000).
- S.B. Dev, D.P. Rabussay, G. Widera and G.A. Hofmann, Medical applications of electroporation, IEEE Transactions on Plasma Science, 28, 1, (206), (2000).
- J.C. Weaver, Electroporation of cells and tissues, IEEE Transactions on Plasma Science, 10.1109/27.842820, 28, 1, (24-33), (2000).
- J. Michie, D. Janssens, J. Cilliers, B.J. Smit and L. Böhm, Assessment of electroporation by flow cytometry, Cytometry, 41, 2, (96-101), (2000).
- Micheline Hyacinthe, Mark J. Jaroszeski, Vu V. Dang, Domenico Coppola, Richard C. Karl, Richard A. Gilbert and Richard Heller, Electrically enhanced drug delivery for the treatment of soft tissue sarcoma , Cancer, 85, 2, (409-417), (2000).
- Rita Vanbever and Véronique Préat, In vivo efficacy and safety of skin electroporation, Advanced Drug Delivery Reviews, 35, 1, (77), (1999).
- Lluis M Mir and Stéphane Orlowski, Mechanisms of electrochemotherapy, Advanced Drug Delivery Reviews, 35, 1, (107), (1999).
- Per E. Engström, Bertil R.R. Persson and Leif G. Salford, Studies of in vivo electropermeabilization by gamma camera measurements of 99mTc-DTPA, Biochimica et Biophysica Acta (BBA) - General Subjects, 1473, 2-3, (321), (1999).
- Mark J Jaroszeski, Richard Gilbert, Claude Nicolau and Richard Heller, In vivo gene delivery by electroporation, Advanced Drug Delivery Reviews, 35, 1, (131), (1999).
- Naoto Uemura, Koichi Nakamura, Yoko Ishii, Seiichiro Matsukubo, Seiji Nyu and Shigeyuki Nakano, Electrical Stimulation Prolongs the Survival Days of Leukemic Mice Treated With Methotrexate., The Japanese Journal of Pharmacology, 79, 3, (269), (1999).
- Mark R Prausnitz, A practical assessment of transdermal drug delivery by skin electroporation, Advanced Drug Delivery Reviews, 35, 1, (61), (1999).
- Julie Gehl, Thyge H. Sørensen, Kurt Nielsen, Povl Raskmark, Steen L. Nielsen, Torben Skovsgaard and Lluis M. Mir, In vivo electroporation of skeletal muscle: threshold, efficacy and relation to electric field distribution, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/S0304-4165(99)00094-X, 1428, 2-3, (233-240), (1999).
- Susumu Omura, Yoshiharu Tsuyuki, Shinsuke Ohta, Hiroki Bukawa and Kiyohide Fujita, In vivo antitumor effects of electrochemotherapy in a tongue cancer model, Journal of Oral and Maxillofacial Surgery, 57, 8, (965), (1999).
- J Teissié, N Eynard, B Gabriel and M.P Rols, Electropermeabilization of cell membranes, Advanced Drug Delivery Reviews, 10.1016/S0169-409X(98)00060-X, 35, 1, (3-19), (1999).
- Richard Heller, Richard Gilbert and Mark J Jaroszeski, Clinical applications of electrochemotherapy, Advanced Drug Delivery Reviews, 35, 1, (119), (1999).
- Géraldine Pron, Nawel Mahrour, Stéphane Orlowski, Omar Tounekti, Bruno Poddevin, Jean Belehradek and Lluis M. Mir, Internalisation of the bleomycin molecules responsible for bleomycin toxicity: a receptor-mediated endocytosis mechanism, Biochemical Pharmacology, 57, 1, (45), (1999).
- Richard Heller, Mark J. Jaroszeski, Douglas S. Reintgen, Chris A. Puleo, Ronald C. DeConti, Richard A. Gilbert and Lewis F. Glass, Treatment of cutaneous and subcutaneous tumors with electrochemotherapy using intralesional bleomycin, Cancer, 83, 1, (148-157), (2000).
- Hiroshi Hasegawa, Makoto Kano, Nobuo Hoshi, Kazuo Watanabe, Eijyu Satoh, Bin Nakayama and Toshimitsu Suzuki, An electrochemotherapy model for rat tongue carcinoma, Journal of Oral Pathology & Medicine, 27, 6, (249-254), (2007).
- J. Berendson and J. M. Olsson, Bioelectrochemical Aspects of the Treatment of Tissue with Direct Current, Electro- and Magnetobiology, 17, 1, (1), (1998).
- Damijan Miklavčič, Katarina Beravs, Dejan Šemrov, Maja Čemažar, Franci Demšar and Gregor Serša, The Importance of Electric Field Distribution for Effective in Vivo Electroporation of Tissues, Biophysical Journal, 74, 5, (2152), (1998).
- Tatsuo Muramatsu, Akihiro Nakamura and Hyi-Man Park, Basics and Applications of Gene Transfer in Animal Cells and Tissues for Production and Therapeutics., Journal of Mammalian Ova Research, 15, 1, (1), (1998).
- Maria Danfelter, Per Engström, Bertil R.R. Persson and Leif G. Salford, Effect of high voltage pulses on survival of Chinese hamster V79 lung fibroblast cells, Bioelectrochemistry and Bioenergetics, 47, 1, (97), (1998).
- Marie-Pierre Rols, Christine Delteil, Muriel Golzio and Justin Teissié, In vitro and ex vivo electrically mediated permeabilization and gene transfer in murine melanoma, Bioelectrochemistry and Bioenergetics, 47, 1, (129), (1998).
- Ajay K Banga and Mark R Prausnitz, Assessing the potential of skin electroporation for the delivery of protein- and gene-based drugs, Trends in Biotechnology, 16, 10, (408), (1998).
- A. Maĉek Lebar, N. A. Kopitar, A. Ihan, G. Serŝa and D. Miklavĉiĉ, Significance of Treatment Energy in Cell Electropermeabilization, Electro- and Magnetobiology, 17, 2, (255), (1998).
- Maurice Chazal, Daniel Benchimol, Patrick Baqué, Valéry Pierrefite, Gérard Milano and André Bourgeon, Treatment of hepatic metastases of colorectal cancer by electrochemotherapy: An experimental study in the rat, Surgery, 124, 3, (536), (1998).
- Per E. Engström, Bertil R.R. Persson and Leif G. Salford, Effect of high voltage electrical pulses on subcutaneous glioma tumours on rats, Bioelectrochemistry and Bioenergetics, 47, 1, (163), (1998).
- Maja Čemažar, Damijan Miklavčič and Gregor Serša, Intrinsic Sensitivity of Tumor Cells to Bleomycin as an Indicator of Tumor Response to Electrochemotherapy, Japanese Journal of Cancer Research, 89, 3, (328-333), (2005).
- Harimoto, Sugimura, Lee, Kuratsukuri and Kishimoto, In vivo gene transfer methods in the bladder without viral vectors, British Journal of Urology, 81, 6, (870-874), (2001).
- Takeshi Suzuki, Bo-Chul Shin, Keiko Fujikura, Toshiyuki Matsuzaki and Kuniaki Takata, Direct gene transfer into rat liver cells by in vivo electroporation, FEBS Letters, 425, 3, (436-440), (1998).
- Marie-Pierre Rols, Christine Delteil, Muriel Golzio, Patrick Dumond, Suzie Cros and Justin Teissie, In vivo electrically mediated protein and gene transfer in murine melanoma, Nature Biotechnology, 16, 2, (168), (1998).
- Per E. Engström, Bertil R.R. Persson and Leif G. Salford, Dynamic gamma camera studies of –bleomycin complex in normal and glioma bearing rats after in vivo electropermeabilization using exponential high-voltage pulses, Bioelectrochemistry and Bioenergetics, 46, 2, (241), (1998).
- Su Wang, M. Kara and T. R. Krishnan, Topical Delivery of Cyclosporin a Coevaporate Using Electroporation Technique, Drug Development and Industrial Pharmacy, 23, 7, (657), (1997).
- Lewis F. Glass, M. Jaroszeski, Richard Gilbert, Douglas S. Reintgen and Richard Heller, Intralesional bleomycin-mediated electrochemotherapy in 20 patients with basal cell carcinoma, Journal of the American Academy of Dermatology, 37, 4, (596), (1997).
- Gregor Sersˇa, Damijan Miklavcˇicˇ, Maja Cˇemazˇar, Jean Belehradek, Tomazˇ Jarm and Lluis M. Mir, Electrochemotherapy with CDDP on LPB sarcoma: comparison of the anti-tumor effectiveness in immunocompotent and immunodeficient mice, Bioelectrochemistry and Bioenergetics, 43, 2, (279), (1997).
- S. B. Dev, G. S. Nanda, Z. An, X. Wang, R. M. Hoffman and G. A. Hofmann, Effective Electroporation Therapy of Human Pancreatic Tumors Implanted in Nude Mice, Drug Delivery, 4, 4, (293), (1997).
- Toyoji Tada, Koichi Matsumoto and Hiroshi Suzuki, Electrochemotherapy significantly inhibits the growth of colon 26 tumors in mice, Surgery Today, 27, 6, (506), (1997).
- Mark J Jaroszeski, Richard Gilbert and Richard Heller, Electrochemotherapy: an emerging drug delivery method for the treatment of cancer, Advanced Drug Delivery Reviews, 26, 2-3, (185), (1997).
- Ming Zeng, George J. Cerniglia, Stephen L. Eck and Craig W. Stevens, High-Efficiency Stable Gene Transfer of Adenovirus into Mammalian Cells Using Ionizing Radiation, Human Gene Therapy, 8, 9, (1025), (1997).
- Mark J Jaroszeski, Richard A Gilbert and Richard Heller, In vivo antitumor effects of electrochemotherapy in a hepatoma model, Biochimica et Biophysica Acta (BBA) - General Subjects, 1334, 1, (15), (1997).
- Igor Serša, Katarina Beravs, Nick J. F. Dodd, Sha Zhao, Damijan Miklavčič and Franci Demsar, Electric current density imaging of mice tumors, Magnetic Resonance in Medicine, 37, 3, (404-409), (2005).
- Tatsuo Muramatsu, Osamu Shibata, Satoru Ryoki, Yasushige Ohmori and Jun-ichi Okumura, Foreign Gene Expression in the Mouse Testis by Localizedin VivoGene Transfer, Biochemical and Biophysical Research Communications, 233, 1, (45), (1997).
- Richard A Gilbert, Mark J Jaroszeski and Richard Heller, Novel electrode designs for electrochemotherapy, Biochimica et Biophysica Acta (BBA) - General Subjects, 1334, 1, (9), (1997).
- Christian Domenge, Stéphane Orlowski, Bernard Luboinski, Thierry De Baere, Guy Schwaab, Jean Belehradek and Lluis M. Mir, Antitumor electrochemotherapy: New advances in the clinical protocol, Cancer, 77, 5, (956-963), (1998).
- Richard Heller, Mark J. Jaroszeski, L. Frank Glass, Jane L. Messina, David P. Rapaport, Ronald C. DeConti, Neil A. Fenske, Richard A. Gilbert, Lluis M. Mir and Douglas S. Reintgen, Phase I/II trial for the treatment of cutaneous and subcutaneous tumors using electrochemotherapy, Cancer, 77, 5, (964-971), (1998).
- Gregor Serša, Maja Čemažar, Dejan Šemrov and Damijan Miklavčič, Changing electrode orientation improves the efficacy of electrochemotherapy of solid tumors in mice, Bioelectrochemistry and Bioenergetics, 39, 1, (61), (1996).
- L.M. Mir, O. Tounekti and S. Orlowski, Bleomycin: Revival of an old drug, General Pharmacology: The Vascular System, 27, 5, (745), (1996).
- L.Frank Glass, Neil A Fenske, M Jaroszeski, R Perrott, David T Harvey, Douglas S Reintgen and Richard Heller, Bleomycin-mediated electrochemotherapy of basal cell carcinoma, Journal of the American Academy of Dermatology, 34, 1, (82), (1996).
- Philippe Giraud, Jean-Marc Bachaud, Justin Teissie and Marie-Pierre Rols, Effects of electrochemotherapy on cutaneous metastases of human malignant melanoma, International Journal of Radiation Oncology*Biology*Physics, 36, 5, (1285), (1996).
- H. Garner, G.A. Hofmann, S.B. Dev and G.S. Nanda, Electrochemotherapy: transition from laboratory to the clinic, IEEE Engineering in Medicine and Biology Magazine, 15, 6, (124), (1996).
- L.M. Mir, S. Orlowski, J. Belehradek, J. Teissié, M.P. Rols, G. Serša, D. Miklavčič, R. Gilbert and R. Heller, Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy, Bioelectrochemistry and Bioenergetics, 38, 1, (203), (1995).
- R. Heller, M. Jaroszeski, J. Leo-Messina, R. Perrot, N. Van Voorhis, D. Reintgen and R. Gilbert, Treatment of B16 mouse melanoma with the combination of electropermeabilization and chemotherapy, Bioelectrochemistry and Bioenergetics, 36, 1, (83), (1995).
- Gregor Serša, Maja Čemažar, Damijan Miklavčič and Lluis M. Mir, Electrochemotherapy: variable anti-tumor effect on different tumor models, Bioelectrochemistry and Bioenergetics, 35, 1-2, (23), (1994).
- D. C. Knottenbelt, A. H. Watson, J. W. Hotchkiss, S. Chopra and A. J. Higgins, A pilot study on the use of ultra‐deformable liposomes containing bleomycin in the treatment of equine sarcoid, Equine Veterinary Education, , (2018).
