Analysis of pulsed electric field effects on cellular tissue with Cole–Cole model: Monitoring permeabilization under inhomogeneous electrical field with bioimpedance parameter variations

Abstract Cell electropermeabilization, which is induced by the application of a pulsed electrical field (PEF), temporarily facilitates the passage of various macromolecules through the membrane. The degree of permeabilization of a cell tissue depends on the characteristics of the applied PEF, and can be characterized by the evolution of its bioimpedance. This paper presents an approach to quantify and analyze changes induced by various characteristics of PEF applied by a simple pair of metal needles inserted in a vegetal tissue, using the bioimpedance monitoring. The dependence of the Cole-Cole model with the level of permeabilization is examined and discussed. In the context of the defined protocol for PEF application, this work shows that the degree of permeabilization of a tissue can be characterized not only by the resistive part of the bioimpedance model, but also by its capacitive part, particularly in the case of a low level of permeabilization. Industrial relevance Nowadays cell tissue electropermeabilization is broadly used in food industry for the improvement of juice production, the enhancement of compound extraction from vegetables, etc.. Nevertheless, a better knowledge of both the dynamics of the permeabilization process and the elements that significantly influence the degree of permeabilization would be extremely important in the perspective of optimization of both extraction and production. This paper compares the effects of PEF characteristics on tissue permeabilization and their efficiency to achieve a desired degree of permeabilization.

[1]  I. Lackovic,et al.  Three-dimensional finite-element analysis of joule heating in electrochemotherapy and in vivo gene electrotransfer , 2009, IEEE Transactions on Dielectrics and Electrical Insulation.

[2]  Uwe Pliquett,et al.  Bioimpedance: A Review for Food Processing , 2010 .

[3]  H. Schwan Electrical properties of tissue and cell suspensions. , 1957, Advances in biological and medical physics.

[4]  L. Mir,et al.  A microfluidic device with removable packaging for the real time visualisation of intracellular effects of nanosecond electrical pulses on adherent cells. , 2012, Lab on a chip.

[5]  Rosa Villa,et al.  Bioimpedance dispersion width as a parameter to monitor living tissues , 2005, Physiological measurement.

[6]  E Neumann,et al.  Fundamentals of electroporative delivery of drugs and genes. , 1999, Bioelectrochemistry and bioenergetics.

[7]  Ahmed S. Elwakil,et al.  Numerical extraction of Cole-Cole impedance parameters from step response , 2011 .

[8]  D. Miklavčič,et al.  Feasibility study for cell electroporation detection and separation by means of dielectrophoresis. , 2007, Bioelectrochemistry.

[9]  Scott J. MacGregor,et al.  Comparison of the effectiveness of biphase and monophase rectangular pulses for the inactivation of micro-organisms using pulsed electric fields , 2002 .

[10]  Ahmed S. Elwakil,et al.  Extracting the Cole-Cole impedance model parameters without direct impedance measurement , 2010 .

[11]  H. Berendsen,et al.  Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations. , 1996, Biophysical journal.

[12]  K. Taiwo,et al.  Comparative evaluation of the effects of pulsed electric field and freezing on cell membrane permeabilisation and mass transfer during dehydration of red bell peppers , 2003 .

[13]  D. Miklavcic,et al.  Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. , 1998, British Journal of Cancer.

[14]  U. Zimmermann,et al.  Electrical breakdown, electropermeabilization and electrofusion. , 1986, Reviews of physiology, biochemistry and pharmacology.

[15]  Mounir Tarek,et al.  Membrane electroporation: a molecular dynamics simulation. , 2005, Biophysical journal.

[16]  Ling-Sheng Jang,et al.  A systematic investigation into the electrical properties of single HeLa cells via impedance measurements and COMSOL simulations. , 2009, Biosensors & bioelectronics.

[17]  A. Angersbach,et al.  Effects of pulsed electric fields on cell membranes in real food systems , 2000 .

[18]  J. Weaver,et al.  Theory of electroporation: A review , 1996 .

[19]  E. Vorobiev,et al.  Combined treatment of apples by pulsed electric fields and by heating at moderate temperature , 2004 .

[20]  Rafael V. Davalos,et al.  Successful treatment of a large soft tissue sarcoma with irreversible electroporation. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[21]  Michael B. Sano,et al.  Theoretical Considerations of Tissue Electroporation With High-Frequency Bipolar Pulses , 2011, IEEE Transactions on Biomedical Engineering.

[22]  Hywel Morgan,et al.  Single-cell microfluidic impedance cytometry: a review , 2010 .

[23]  Helmut Grubmüller,et al.  Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations. , 2008, Biophysical journal.

[24]  Claire Dalmay,et al.  A microfluidic biochip for the nanoporation of living cells. , 2011, Biosensors & bioelectronics.

[25]  U. Zimmermann,et al.  Reversible Electropermeabilization of Mammalian Cells by High-Intensity, Ultra-Short Pulses of Submicrosecond Duration , 2001, The Journal of Membrane Biology.

[26]  D. Barrett,et al.  Determination of membrane integrity in onion tissues treated by pulsed electric fields: Use of microscopic images and ion leakage measurements , 2010 .

[27]  L. Mir,et al.  Changes of cell electrical parameters induced by electroporation. A dielectrophoresis study. , 2013, Biochimica et biophysica acta.

[28]  P. Bodger,et al.  Physical modelling of electroporation in close cell-to-cell proximity environments , 2006, Physics in medicine and biology.

[29]  B. Le Pioufle,et al.  Microarray of non-connected gold pads used as high density electric traps for parallelized pairing and fusion of cells. , 2013, Biomicrofluidics.

[30]  M. Fincan,et al.  In situ visualization of the effect of a pulsed electric field on plant tissue , 2002 .

[31]  Lionel Cima,et al.  Macroscopic characterization of cell electroporation in biological tissue based on electrical measurements , 2004 .

[32]  D Miklavcic,et al.  Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part II. Reduced electrolytic contamination. , 2001, Bioelectrochemistry.

[33]  M. Rols,et al.  Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. , 2005, Biochimica et biophysica acta.

[34]  Dietrich Knorr,et al.  Impact of high-intensity electric field pulses on plant membrane permeabilization , 1998 .

[35]  T. L. Ellis,et al.  Non-Thermal Irreversible Electroporation (N-TIRE) and Adjuvant Fractionated Radiotherapeutic Multimodal Therapy for Intracranial Malignant Glioma in a Canine Patient , 2011, Technology in cancer research & treatment.

[36]  Zhaosheng Teng,et al.  Improved Cole parameter extraction based on the least absolute deviation method , 2013, Physiological measurement.

[37]  D Peter Tieleman,et al.  BMC Biochemistry BioMed Central Research article The molecular basis of electroporation , 2004 .

[38]  E. Vorobiev,et al.  Temperature enhanced electroporation under the pulsed electric field treatment of food tissue , 2005 .

[39]  Shu Xiao,et al.  Bioelectric Effects of Intense Nanosecond Pulses , 2007, IEEE Transactions on Dielectrics and Electrical Insulation.

[40]  Boris Rubinsky,et al.  In vivo results of a new focal tissue ablation technique: irreversible electroporation , 2006, IEEE Transactions on Biomedical Engineering.

[41]  L. Mir,et al.  High‐resolution analyses of cell fusion dynamics in a biochip , 2012, Electrophoresis.

[42]  L. Mir,et al.  Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part I. Increased efficiency of permeabilization. , 2001, Bioelectrochemistry.

[43]  Claire Dalmay,et al.  Design and realization of a microfluidic device devoted to the application of ultra-short pulses of electrical field to living cells , 2011 .

[44]  P. Thomas Vernier,et al.  Life Cycle of an Electropore: Field-Dependent and Field-Independent Steps in Pore Creation and Annihilation , 2010, The Journal of Membrane Biology.

[45]  D. Chang,et al.  Cell poration and cell fusion using an oscillating electric field. , 1989, Biophysical journal.

[46]  K. Schoenbach,et al.  Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electric pulse. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  D Miklavcic,et al.  Role of pulse shape in cell membrane electropermeabilization. , 2003, Biochimica et biophysica acta.