Modeling electroporation of the non-treated and vacuum impregnated heterogeneous tissue of spinach leaves

Uniform electroporation of the heterogeneous structure of spinach leaf cross section is a technological challenge that is addressed in this investigation. Three dimensional models were created with cells arranged in specific tissue types, considering a leaf with its air fraction and a leaf where the air fraction was replaced by a solution of known properties using vacuum impregnation. The models were validated before electroporation, in the frequency domain, where alternating voltage and current signal at frequencies from 20 Hz to I MHz were used to measure conductivity of the tissue. They were also validated through measurements of current during electroporation when a single 250 mu s rectangular pulse with amplitudes ranging from 50 to 500 V was applied. Model validations show that both the frequency dependent conductivity and electroporation are well predicted. The importance of the wax layer and stomata in the model is thoroughly discussed. Industrial relevance: Our aim was to investigate electroporation of the spinach leaf by developing a model which would enable us to meet the technological challenge of achieving uniform electroporation in a highly heterogeneous structure in the context of a process aimed at improving freezing stability of plant foods. Pulsed electric field treatment may be used to introduce the cryoprotectant molecules into the cells, and hence improve the structure and properties of frozen food plants. (C) 2014 Elsevier Ltd. All rights reserved. (Less)

[1]  Damijan Miklavčič,et al.  Electroporation in Biological Cell and Tissue: An Overview , 2009 .

[2]  W. Krassowska,et al.  Modeling electroporation in a single cell. , 2007, Biophysical journal.

[3]  Damijan Miklavčič,et al.  Patient-specific treatment planning of electrochemotherapy: procedure design and possible pitfalls. , 2012, Bioelectrochemistry.

[4]  Petr Dejmek,et al.  Pulsed electric field in combination with vacuum impregnation with trehalose improves the freezing tolerance of spinach leaves , 2008 .

[5]  W. Krassowska,et al.  Modeling electroporation in a single cell. I. Effects Of field strength and rest potential. , 1999, Biophysical journal.

[6]  Damijan Miklavčič,et al.  Numerical modeling in electroporation-based biomedical applications , 2008 .

[7]  D. Miklavčič,et al.  Resistive heating and electropermeabilization of skin tissue during in vivo electroporation: A coupled nonlinear finite element model , 2011 .

[8]  S. Talele,et al.  Modelling Control of Pore Number and Radii Distribution in Single-Cell Electroporation , 2010 .

[9]  Damijan Miklavcic,et al.  A Time-Dependent Numerical Model of Transmembrane Voltage Inducement and Electroporation of Irregularly Shaped Cells , 2009, IEEE Transactions on Biomedical Engineering.

[10]  Damijan Miklavčič,et al.  Skin electroporation for transdermal drug delivery: the influence of the order of different square wave electric pulses. , 2013, International journal of pharmaceutics.

[11]  C. Jones,et al.  RAPID QUANTIFICATION OF SPINACH LEAF CUTICULAR WAX USING FOURIER TRANSFORM INFRARED ATTENUATED TOTAL REFLECTANCE SPECTROSCOPY , 2013 .

[12]  Paul Gaynor,et al.  Modelling single cell electroporation with bipolar pulse parameters and dynamic pore radii , 2010 .

[13]  Daniela O. H. Suzuki,et al.  Theoretical and Experimental Analysis of Electroporated Membrane Conductance in Cell Suspension , 2011, IEEE Transactions on Biomedical Engineering.

[14]  A. T. Esser,et al.  Microdosimetry for conventional and supra-electroporation in cells with organelles. , 2006, Biochemical and biophysical research communications.

[15]  E. Neumann,et al.  Gene transfer into mouse lyoma cells by electroporation in high electric fields. , 1982, The EMBO journal.

[16]  Petr Dejmek,et al.  Microscopic studies providing insight into the mechanisms of mass transfer in vacuum impregnation , 2013 .

[17]  Damijan Miklavcic,et al.  Electroporation of Intracellular Liposomes Using Nanosecond Electric Pulses—A Theoretical Study , 2013, IEEE Transactions on Biomedical Engineering.

[18]  L. Schreiber,et al.  Protecting against water loss: analysis of the barrier properties of plant cuticles. , 2001, Journal of experimental botany.

[19]  G. Saulis,et al.  Pore disappearance in a cell after electroporation: theoretical simulation and comparison with experiments. , 1997, Biophysical journal.

[20]  P. Murugavel,et al.  Effect of relative humidity and sea level pressure on electrical conductivity of air over Indian Ocean , 2009 .

[21]  E. Neumann,et al.  Permeability changes induced by electric impulses in vesicular membranes , 1972, The Journal of Membrane Biology.

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

[23]  K. Mott,et al.  Stomatal Responses to Flooding of the Intercellular Air Spaces Suggest a Vapor-Phase Signal Between the Mesophyll and the Guard Cells1[OA] , 2010, Plant Physiology.

[24]  Petr Dejmek,et al.  Influence of Pulsed Electric Field Protocols on the Reversible Permeabilization of Rucola Leaves , 2014, Food and Bioprocess Technology.

[25]  Damijan Miklavcic,et al.  Electrochemotherapy: technological advancements for efficient electroporation-based treatment of internal tumors , 2012, Medical and Biological Engineering and Computing.

[26]  Neil B. McLaughlin,et al.  In vivo plant impedance measurements and characterization of membrane electrical properties: the influence of cold acclimation , 1987 .

[27]  Douglas B. Kell,et al.  The radio-frequency dielectric properties of yeast cells measured with a rapid, automated, frequency-domain dielectric spectrometer , 1983 .

[28]  P. Wanichapichart,et al.  Determination of Cell Dielectric Properties Using Dielectrophoretic Technique , 2002 .

[29]  Gustavo V. Barbosa-Cánovas,et al.  Innovative food science and emerging technologies , 2000 .

[30]  L. G. Hector,et al.  The Dielectric Constant of Air at Radiofrequencies , 1936 .

[31]  Shima Shayanfar,et al.  The interaction of pulsed electric fields and texturizing ‐ antifreezing agents in quality retention of defrosted potato strips , 2013 .

[32]  D. Robinson,et al.  Subcellular volumes and metabolite concentrations in spinach leaves , 1994, Planta.

[33]  Damijan Miklavčič,et al.  Electroporation-based technologies for medicine: principles, applications, and challenges. , 2014, Annual review of biomedical engineering.

[34]  A. Heredia,et al.  Electrical conductivity of differently treated isolated cuticular membranes by impedance spectroscopy. , 1993, Archives of biochemistry and biophysics.

[35]  L. Chernomordik,et al.  Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. , 1988, Biochimica et biophysica acta.

[36]  U. Zimmermann,et al.  Electric field-induced cell-to-cell fusion , 2005, The Journal of Membrane Biology.

[37]  Boris Rubinsky,et al.  Electrical field and temperature model of nonthermal irreversible electroporation in heterogeneous tissues. , 2009, Journal of biomechanical engineering.

[38]  R. D. Warmbrodt,et al.  Leaf of Spinacia oleracea (spinach): ultrastructure, and plasmodesmatal distribution and frequency, in relation to sieve-tube loading. , 1990 .

[39]  Ulrich Zimmermann,et al.  Dielectric Breakdown of Cell Membranes , 1974 .

[40]  J. Schönherr Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. , 2006, Journal of experimental botany.

[41]  O. Farish,et al.  Pulsed electric field inactivation of diarrhoeagenic Bacillus cereus through irreversible electroporation , 2000, Letters in applied microbiology.

[42]  Damijan Miklavcic,et al.  The influence of skeletal muscle anisotropy on electroporation: in vivo study and numerical modeling , 2010, Medical & Biological Engineering & Computing.

[43]  R. Arora,et al.  A loss in the plasma membrane ATPase activity and its recovery coincides with incipient freeze-thaw injury and postthaw recovery in onion bulb scale tissue. , 1991, Plant physiology.

[44]  N. Gavish,et al.  Dependence of the dielectric constant of electrolyte solutions on ionic concentration: A microfield approach. , 2012, Physical review. E.

[45]  Mojca Pavlin,et al.  A numerical analysis of multicellular environment for modeling tissue electroporation , 2012 .

[46]  D. Miklavčič,et al.  Cell membrane electroporation- Part 1: The phenomenon , 2012, IEEE Electrical Insulation Magazine.

[47]  B. Rubinsky,et al.  Principles of Tissue Engineering With Nonthermal Irreversible Electroporation , 2011 .

[48]  Koji Asami,et al.  Dielectric Approach to Suspensions of Ellipsoidal Particles Covered with a Shell in Particular Reference to Biological Cells , 1980 .