462
Views
23
CrossRef citations to date
0
Altmetric
Review

Mechanistic view of skin electroporation – models and dosimetry for successful applications: an expert review

ORCID Icon, &
Pages 689-704 | Received 05 Nov 2019, Accepted 18 Mar 2020, Published online: 08 Apr 2020

References

  • Kotnik T, Rems L, Tarek M, et al. Membrane electroporation and electropermeabilization: mechanisms and models. Annu Rev Biophys. 2019;48: 63–91.
  • Pliquett UF, Vanbever R, Preat V, et al. Local transport regions (LTRs) in human stratum corneum due to long and short `high voltage’ pulses. Bioelectrochem Bioenerg. 1998;47:151–161.
  • Pliquett UF, Zewert TE, Chen T, et al. Imaging of fluorescent molecule and small ion transport through human stratum corneum during high voltage pulsing: localized transport regions are involved. Biophys Chem. 1996;58:185–204.
  • Gowrishankar TR, Herndon TO, Vaughan TE, et al. Spatially constrained localized transport regions due to skin electroporation. J Control Release. 1999;60:101–110.
  • Gupta R, Rai B Electroporation of skin stratum corneum lipid bilayer and molecular mechanism of drug transport: a molecular dynamics study. Langmuir. 2018;34:5860–5870.
  • Dermol-Černe J, Miklavčič D From cell to tissue properties—modeling skin electroporation with pore and local transport region formation. IEEE Trans Biomed Eng. 2018;65:458–468.
  • Pavšelj N, Miklavčič D Numerical models of skin electropermeabilization taking into account conductivity changes and the presence of local transport regions. IEEE Trans Plasma Sci. 2008;36:1650–1658.
  • Denet A-R, Vanbever R, Préat V Skin electroporation for transdermal and topical delivery. Adv Drug Deliv Rev. 2004;56:659–674.
  • Zorec B, Préat V, Miklavčič D, et al. Active enhancement methods for intra- and transdermal drug delivery: a review. Zdravniški vestnik. 2013;82:339–356.
  • Lambricht L, Lopes A, Kos Š, et al. Clinical potential of electroporation for gene therapy and DNA vaccine delivery. Expert Opin Drug Deliv. 2016;13:295–310.
  • Kos Š, Blagus T, Čemažar M, et al. Electrotransfer parameters as a tool for controlled and targeted gene expression in skin. Mol Ther Nucleic Acids. 2016;5:e356.
  • Prausnitz MR, Langer R Transdermal drug delivery. Nat Biotechnol. 2008;26:1261–1268.
  • Ita K Perspectives on transdermal electroporation. Pharmaceutics. 2016;8:9.
  • Schoellhammer CM, Blankschtein D, Langer R Skin permeabilization for transdermal drug delivery: recent advances and future prospects. Expert Opin Drug Deliv. 2014;11:393–407.
  • Zasada M, Markiewicz A, Drożdż Z, et al. Preliminary randomized controlled trial of antiaging effects of L‐ascorbic acid applied in combination with no‐needle and microneedle mesotherapy. J Cosmet Dermatol. 2019;18:843–849.
  • Thappa D, Konda D Mesotherapy: what is new? Indian J Dermatol Venereol Leprol. 2013;79:127.
  • Zhang L, Lerner S, Rustrum WV, et al. Electroporation-mediated topical delivery of vitamin C for cosmetic applications. Bioelectrochem Bioenerg. 1999;48:453–461.
  • Golberg A, Villiger M, Felix Broelsch G, et al. Skin regeneration with all accessory organs following ablation with irreversible electroporation: skin regeneration following irreversible electroporation. J Tissue Eng Regen Med. 2018;12:98–113.
  • Golberg A, Broelsch GF, Vecchio D, et al. Pulsed electric fields for burn wound disinfection in a Murine model: J Burn Care Res. 2015;36:7–13.
  • Novickij V, Zinkevičienė A, Perminaitė E, et al. Non-invasive nanosecond electroporation for biocontrol of surface infections: an in vivo study. Sci Rep. 2018;8:14516.
  • Gehl J, Serša G, Matthiessen LW, et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta Oncol. 2018;57:874–882.
  • Campana LG, Miklavčič D, Bertino G, et al. Electrochemotherapy of superficial tumors – current status: Semin Oncol. 2019;46:173–191.
  • Manca G, Pandolfi P, Gregorelli C, et al. Treatment of keloids and hypertrophic scars with bleomycin and electroporation: Plast Reconstr Surg. 2013;132:621e–630e.
  • Becker SM, Kuznetsov AV Local temperature rises influence In vivo electroporation pore development: a numerical stratum corneum lipid phase transition model. J Biomech Eng. 2007;129:712–721.
  • Becker SM, Kuznetsov AV Numerical assessment of thermal response associated with In vivo skin electroporation: the importance of the composite skin model. J Biomech Eng. 2007;129:330.
  • Chizmadzhev YA, Indenbom AV, Kuzmin PI, et al. Electrical properties of skin at moderate voltages: contribution of appendageal macropores. Biophys J. 1998;74:843–856.
  • Pavšelj N, Préat V, Miklavčič D A numerical model of skin electropermeabilization based on In vivo experiments. Ann Biomed Eng. 2007;35:2138–2144.
  • Pavšelj N, Miklavčič D A numerical model of permeabilized skin with local transport regions. IEEE Trans Biomed Eng. 2008;55:1927–1930.
  • Pavšelj N, Bregar Z, Cukjati D, et al. The course of tissue permeabilization studied on a mathematical model of a subcutaneous tumor in small animals. IEEE Trans Biomed Eng. 2005;52:1373–1381.
  • Pawlowski P, Gallo SA, Johnson PG, et al. Electrorheological modeling of the permeabilization of the stratum corneum: theory and experiment. Biophys J. 1998;75:2721–2731.
  • Nickfarjam A, Firoozabadi SMP Parametric study of irreversible electroporation with different needle electrodes: electrical and thermal analysis. Int J Hyperthermia. 2014;30:335–347.
  • Becker S Transport modeling of skin electroporation and the thermal behavior of the stratum corneum. Int J Ther Sci. 2012;54:48–61.
  • Becker SM, Kuznetsov AV Thermal in vivo skin electroporation pore development and charged macromolecule transdermal delivery: A numerical study of the influence of chemically enhanced lower lipid phase transition temperatures. Int J Heat Mass Transfer. 2008;51:2060–2074.
  • Martin GT, Pliquett UF, Weaver JC Theoretical analysis of localized heating in human skin subjected to high voltage pulses. Bioelectrochemistry. 2002;57:55–64.
  • Pavšelj N, Miklavčič D Resistive heating and electropermeabilization of skin tissue during in vivo electroporation: A coupled nonlinear finite element model. Int J Heat Mass Transfer. 2011;54:2294–2302.
  • Becker SM, Kuznetsov AV Thermal damage reduction associated with in vivo skin electroporation: A numerical investigation justifying aggressive pre-cooling. Int J Heat Mass Transfer. 2007;50:105–116.
  • Pliquett U, Nuccitelli R Measurement and simulation of Joule heating during treatment of B-16 melanoma tumors in mice with nanosecond pulsed electric fields. Bioelectrochemistry. 2014;100:62–68.
  • Pliquett U, Gusbeth C, Nuccitelli R A propagating heat wave model of skin electroporation. J Theor Biol. 2008;251:195–201.
  • Vanbever R, Pliquett UF, Préat V, et al. Comparison of the effects of short, high-voltage and long, medium-voltage pulses on skin electrical and transport properties. J Control Release. 1999;60:35–47.
  • Daugimont L, Baron N, Vandermeulen G, et al. Hollow microneedle arrays for intradermal drug delivery and DNA electroporation. J Membrane Biol. 2010;236:117–125.
  • Mi Y, Peng W, Rui S, et al. Multiparametric finite-element simulation and experiment on thermal effects in skin tumor exposed to high-frequency nanosecond pulse bursts. IEEE Trans Plasma Sci. 2019;47:924–934.
  • Čorović S, Županič A, Miklavčič D Numerical modeling and optimization of electric field distribution in subcutaneous tumor treated with electrochemotherapy using needle electrodes. IEEE Trans Plasma Sci. 2008;36:1665–1672.
  • Cornelis FH, Cindrič H, Kos B, et al. Peri-tumoral metallic implants reduce the efficacy of irreversible electroporation for the ablation of colorectal liver metastases. Cardiovasc Intervent Radiol [Internet]. 2019. [cited 2019 Oct 18]. Available from: http://link.springer.com/10.1007/s00270-019-02300-y.
  • Becker SM Skin electroporation with passive transdermal transport theory: a review and a suggestion for future numerical model development. J Heat Transfer. 2011;133:011011.
  • Chizmadzhev YA, Zarnitsin VG, Weaver JC, et al. Mechanism of electro induced ionic species transport through a multilamellar lipid system. Biophys J. 1995;68:749–765.
  • Becker S, Zorec B, Miklavčič D, et al. Transdermal transport pathway creation: electroporation pulse order. Math Biosci. 2014;257:60–68.
  • Edwards DA, Prausnitz MR, Langer R, et al. Analysis of enhanced transdermal transport by skin electroporation. J Control Release. 1995;34:211–221.
  • Mahnič-Kalamiza S, Vorobiev E Dual-porosity model of liquid extraction by pressing from biological tissue modified by electroporation. J Food Eng. 2014;137:76–87.
  • Hirsch AC, Upasani RS, Banga AK Factorial design approach to evaluate interactions between electrically assisted enhancement and skin stripping for delivery of tacrine. J Control Release. 2005;103:113–121.
  • Gothelf A, Mahmood F, Dagnaes-Hansen F, et al. Efficacy of transgene expression in porcine skin as a function of electrode choice. Bioelectrochemistry. 2011;82:95–102.
  • Forjanič T, Miklavčič D Numerical study of gene electrotransfer efficiency based on electroporation volume and electrophoretic movement of plasmid DNA. Biomed Eng Online [Internet]. 2018;17. [cited 2018 Jul 13]. Available from: https://biomedical-engineering-online.biomedcentral.com/articles/10.1186/s12938-018-0515-3
  • Forjanič T, Markelc B, Marčan M, et al. Electroporation-induced stress response and its effect on gene electrotransfer efficacy: In vivo imaging and numerical modeling. IEEE Trans Biomed Eng. 2019;66:2671–2683.
  • Čorović S, Markelc B, Dolinar M, et al. Modeling of microvascular permeability changes after electroporation. Schneditz D, editor. PLoS One. 2015;10:e0121370.
  • Vargas Luna JL, Krenn M, Cortés Ramírez JA, et al. Dynamic impedance model of the skin-electrode interface for transcutaneous electrical stimulation. PLoS ONE. 2015;10:e0125609.
  • Gothelf A, Gehl J Gene electrotransfer to skin; review of existing literature and clinical perspectives. CGT. 2010;10:287–299.
  • Mossop BJ, Barr RC, Henshaw JW, et al. Electric fields in tumors exposed to external voltage sources: implication for electric field-mediated drug and gene delivery. Ann Biomed Eng. 2006;34:1564–1572.
  • Caliper Electrodes for Electroporation Applications [Internet]. [cited 2019 Oct 10]. Available from: https://www.btxonline.com/caliper-electrodes.html
  • Heller LC, Jaroszeski MJ, Coppola D, et al. Optimization of cutaneous electrically mediated plasmid DNA delivery using novel electrode. Gene Ther. 2007;14:275–280.
  • Golberg A, Bei M, Sheridan RL, et al. Regeneration and control of human fibroblast cell density by intermittently delivered pulsed electric fields. Biotechnol Bioeng. 2013;110:1759–1768.
  • Petri Pulser Electroporation Applicator [Internet]. [cited 2019 Oct 10]. Available from: https://www.btxonline.com/petri-pulser.html
  • Accessories ElectroVet [Internet]. Leroy biotech. [cited 2019 Oct 10]. Available from: https://www.leroybiotech.com/electrovet-ez/accessories/
  • Mazères S, Šel D, Golzio M, et al. Non invasive contact electrodes for in vivo localized cutaneous electropulsation and associated drug and nucleic acid delivery. J Control Release. 2009;134:125–131.
  • Guo S, Donate A, Basu G, et al. Electro-gene transfer to skin using a noninvasive multielectrode array. J Control Release. 2011;151:256–262.
  • Heller R, Cruz Y, Heller LC, et al. Electrically mediated delivery of plasmid DNA to the skin, using a multielectrode array. Hum Gene Ther. 2010;21:357–362.
  • Donate A, Coppola D, Cruz Y, et al. Evaluation of a novel non-penetrating electrode for use in DNA vaccination. Rubinsky B, editor. PLoS One. 2011;6:e19181.
  • Zorec B, Jelenc J, Miklavčič D, et al. Ultrasound and electric pulses for transdermal drug delivery enhancement: ex vivo assessment of methods with in vivo oriented experimental protocols. Int J Pharm. 2015;490:65–73.
  • Pliquett U, Weaver JC Feasibility of an electrode-reservoir device for transdermal drug delivery by noninvasive skin electroporation. IEEE Trans Biomed Eng. 2007;54:536–538.
  • Huang D, Zhao D, Wang X, et al. Efficient delivery of nucleic acid molecules into skin by combined use of microneedle roller and flexible interdigitated electroporation array. Theranostics. 2018;8:2361–2376.
  • Maruyama H, Ataka K, Higuchi N, et al. Skin-targeted gene transfer using in vivo electroporation. Gene Ther. 2001;8:1808–1812.
  • Electrodes and accessories | IGEA [Internet]. [cited 2019 Oct 10]. Available from: https://www.igea.it/en/oncology/information-clinicians/electrodes-and-accessories
  • Platinum Needle L-Shaped Electrode for In Vivo Electroporation Applications [Internet]. [cited 2019 Oct 10]. Available from: https://www.btxonline.com/platinum-needle-l-shaped-electrode.html
  • Needle Array Electrodes for BTX AgilePulse In Vivo [Internet]. [cited 2019 Nov 5]. Available from: https://www.btxonline.com/needle-array-electrodes-for-agilepulse-in-vivo.html
  • In Vivo/In Utero/In Ovo/Ex Vivo Electroporation Electrodes [Internet]. [cited 2019 Oct 10]. Available from: http://www.nepagene.jp/e_products_nepagene_0009.html
  • Electrodes for in vivo electroporation|BEX CO., LTD. [Internet]. [cited 2019 Oct 10]. Available from: http://www.bexnet.co.jp/english/product/device/in-vivo/2.html
  • Deng Y, Chen J, Zhao Y, et al. Transdermal Delivery of siRNA through microneedle array. Sci Rep. 2016;6:21422.
  • Campana LG, Dughiero F, Forzan M, et al. A prototype of a flexible grid electrode to treat widespread superficial tumors by means of Electrochemotherapy. Radiol Oncol [Internet]. 2016 [cited 2019 Aug 26];50. Available from: https://content.sciendo.com/view/journals/raon/50/1/article-p49.xml
  • MESOFORTE Duo | AMICO GROUP [Internet]. [cited 2019 Oct 29]. Available from: https://www.amicogroup.com/specialization/dermatology/cosmetics/dr-derm/mesotherapy-mesoforte-duo.aspx
  • El-Kamary SS, Billington M, Deitz S, et al. Safety and tolerability of the easy VaxTM clinical epidermal electroporation system in healthy adults. Mol Ther. 2012;20:214–220.
  • Goldman MP, Hexsel D Cellulite: pathophysiology and treatment. Boca Raton: CRC Press; 2010.
  • Lombry C, Dujardin N, Préat V Transdermal delivery of macromolecules using skin electroporation. Pharm Res. 2000;17:32–37.
  • Orr RM Technology evaluation: electroporation therapy, Genetronics Inc. Curr Opin Mol Ther. 2000;2:205–210.
  • ACTHYDERM ® - Microlab International Srl ® [Internet]. [cited 2019 Oct 29]. Available from: http://acthyderm.mulab.net/Acthyderm01.html
  • Skrynska O, Antonova-Rafi J, Khudetskyy I. Treating skin with use of electroporation. Biomed Eng Electr. 2019;1:26–38.
  • Čorović S, Pavlin M, Miklavčič D Analytical and numerical quantification and comparison of the local electric field in the tissue for different electrode configurations. Biomed Eng Online. 2007;6:37.
  • Raso J, Frey W, Ferrari G, et al. Recommendations guidelines on the key information to be reported in studies of application of PEF technology in food and biotechnological processes. Innovative Food Sci Emerg Technol [Internet]. 2016;37:312–321. [cited 2016 Aug 30]. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1466856416301771
  • Čemažar M, Serša G, Frey W, et al. Recommendations and requirements for reporting on applications of electric pulse delivery for electroporation of biological samples. Bioelectrochemistry. 2018;122:69–76.
  • Campana LG, Clover AJP, Valpione S, et al. Recommendations for improving the quality of reporting clinical electrochemotherapy studies based on qualitative systematic review. Radiol Oncol. 2016;50:1–13.
  • Madi M, Rols M-P, Gibot L Efficient In vitro electropermeabilization of reconstructed human dermal tissue. J Membr Biol. 2015;248:903–908.
  • Madi M, Rols M-P, Gibot L Gene electrotransfer in 3D reconstructed human dermal tissue. Curr Gene Ther. 2016;16:75–82.
  • Bulysheva AA, Burcus N, Lundberg C, et al. Recellularized human dermis for testing gene electrotransfer ex vivo. Biomed Mater. 2016;11:035002.
  • Čorović S, Lacković I, Šuštarič P, et al. Modeling of electric field distribution in tissues during electroporation. Biomed Eng Online. 2013;12:16.
  • Pliquett U, Weaver JC Electroporation of human skin: simultaneous measurement of changes in the transport of two fluorescent molecules and in the passive electrical properties. Bioelectrochem Bioenerg. 1996;39:1–12.
  • Henshaw JW, Zaharoff DA, Mossop BJ, et al. Electric field-mediated transport of plasmid DNA in tumor interstitium in vivo. Bioelectrochemistry. 2007;71:233–242.
  • Čorović S, Mir LM, Miklavčič D In vivo muscle electroporation threshold determination: realistic numerical models and In vivo experiments. J Membr Biol. 2012;245:509–520.
  • Walpole J, Papin JA, Peirce SM Multiscale computational models of complex biological systems. Annu Rev Biomed Eng. 2013;15:137–154.
  • Reberšek M Beyond electroporation pulse parameters: from application to evaluation. In: Miklavcic D, editor. Handbook of electroporation [Internet]. Cham: Springer International Publishing; 2017. p. 1–21. DOI:10.1007/978-3-319-26779-1_222-1
  • Gabriel C, Gabriel S, Corthout E The dielectric properties of biological tissues: I. Literature Survey. Phys Med Biol. 1996;41:2231–2249.
  • Chiapperino MA, Bia P, Caratelli D, et al. Nonlinear dispersive model of electroporation for irregular nucleated cells. Bioelectromagnetics. 2019;40:331–342.
  • Scuderi M, Reberšek M, Miklavčič D, et al. The use of high-frequency short bipolar pulses in cisplatin electrochemotherapy in vitro. Radiol Oncol. 2019;53:194–205.
  • Pirc E, Reberšek M, Miklavčič D Dosimetry in electroporation-based technologies and treatments. Dosimetry in bioelectromagnetic. Boca Raton: Taylor & Francis Group, LLC; 2017. p. 233–268.
  • Cvetkoska A, Pirc E, Reberšek M, et al. Towards standardization of electroporation devices and protocols. IEEE Instrum Meas Mag. 2019;23:74–81.
  • Mori K, Hasegawa T, Sato S, et al. Effect of electric field on the enhanced skin permeation of drugs by electroporation. J Control Release. 2003;90:171–179.
  • Kotnik T, Miklavčič D, Mir LM Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part II. Reduced electrolytic contamination. Bioelectrochemistry. 2001;54:91–95.
  • Saulis G, Rodaitė-Riševičienė R, Dainauskaitė VS, et al. Electrochemical processes during high-voltage electric pulses and their importance in food processing technology. In: Rai VR, editor. Advances in food biotechnology [Internet]. Chichester, UK: John Wiley & Sons Ltd; 2015 [cited 2015 Dec 10]. 575–592. DOI:10.1002/9781118864463.ch35
  • Luján E, Marino M, Olaiz N, et al. Towards an optimal dose-response relationship in gene electrotransfer protocols. Electrochim Acta. 2019;319:1002–1011.
  • Kardos TJ, Rabussay DP Contactless magneto-permeabilization for intracellular plasmid DNA delivery in-vivo. Hum Vaccin Immunother. 2012;8:1707–1713.
  • Kranjc Brezar S, Kranjc M, Čemažar M, et al. Electrotransfer of siRNA to silence enhanced green fluorescent protein in tumor mediated by a high intensity pulsed electromagnetic field. Vaccines (Basel). 2020;8:49.
  • Kranjc S, Kranjc M, Ščančar J, et al. Electrochemotherapy by pulsed electromagnetic field treatment (PEMF) in mouse melanoma B16F10 in vivo. Radiol Oncol. 2016;50:39–48.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.