Temperature enhanced electroporation under the pulsed electric field treatment of food tissue

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Journal of Food Engineering 69 (2005) 177–184

Temperature enhanced electroporation under the pulsedelectric field treatment of food tissue

Nikolai I. Lebovka a,b, Iurie Praporscic a, Sami Ghnimi a, Eugene Vorobiev a,*

a Departement de Genie Chimique, Universite de Technologie de Compiegne, Centre de Recherche de Royallieu,

B.P. 20529-60205 Compiegne Cedex, Franceb Institute of Biocolloidal Chemistry named after F.D. Ovcharenko, NAS of Ukraine, 42, blvr. Vernadskogo, Kyiv 03142, Ukraine

Received 24 May 2004; accepted 6 August 2004

Abstract

The temperature dependence of effects exerted by pulsed electric fields (PEF) on the electrical conductivity and textural relaxation

of potato tissue was investigated in the interval of 22–50�C. The pronounced decrease of the characteristic electrical damage time swith increase of both temperature T and electric field strength E was observed. Textural data reveal the essential temperature influ-

ence on tissue softening after the PEF treatment. The investigation of thermally induced damage at temperatures within 45–60 �Cshows that effects observed below 50 �C are not related to any noticeable irreversible damage of the cellular membranes and reflectonly effect of structural transitions in membranes on electroporation. It is of practical importance that PEF treatment under the

mild thermal conditions (below 50 �C) allows to reach high tissue disintegration degree at moderate electric field strength (below100V/cm).

� 2004 Elsevier Ltd. All rights reserved.

Keywords: Electroporation; Temperature dependence; Pulsed electric field; Texture; Characteristic damage time; Potato

1. Introduction

It is known for decades that pulsed electric fields

(PEF) can cause electroporation or complete damage

of the cell membranes in biological objects (Weaver &

Chizmadzhev, 1996; Zimmermann, 1986). Recently this

interesting phenomenon allowed to develop different

promising modern processing methods for food indus-try. For example, PEF application for microbial inacti-

vation, juice extraction, dehydration and drying were

reported in (Barbosa-Canovas, Gongora-Nieto, Potha-

kamury, & Swanson, 1998; Bajgai & Hashinaga, 2001;

Barsotti & Cheftel, 1998; Bazhal, Lebovka, & Vorobiev,

2001; Bazhal & Vorobiev, 2000; Taiwo, Angersbach, &

0260-8774/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jfoodeng.2004.08.037

* Corresponding author. Tel.: +33 3 4423 5273; fax: +33 3 4423

1980.

E-mail address: [email protected] (E. Vorobiev).

Knorr, 2002; Vorobiev, Bazhal, & Lebovka, 2001;

Wouters & Smelt, 1997). PEF treatment destroys cell

membranes, removes the cellular turgor component of

the texture and exert an estimable influence on the visco-

elastic properties of plant tissue (Fincan & Dejmek,

2003; Lebovka, Praporscic, & Vorobiev, 2003). The

combined pressure-PEF treatment allows to enhance

the solid–liquid expression of different biological tissuesand to increase the juice yield (Vorobiev, Jemai,

Bouzrara, Lebovka, & Bazhal, 2004). The effective plant

tissue disintegration under the PEF treatment can be

achieved at moderate electric fields of 500–1000V/cm,

short treatment time within 10�4–10�2 s and room tem-

perature (Lebovka, Bazhal, & Vorobiev, 2001, 2002).

This method can be a good alternative to the traditional

thermal methods of plant tissue treatment, which inducelosses of product quality, including partial disintegra-

tion of pigments, vitamins and flavouring agents.

Nomenclature

d sample diameter (mm)

E PEF intensity (V/cm)E0 empirical parameter (V/cm)

F force (N)

h sample height (mm)

n number of pulses

N number of trains

R universal gas constant, 8.314 (JK�1mol�1)

t time (s)

ti pulse duration (ls)t1 effective relaxation time (s)

tPEF time of PEF treatment (s)

Dt pulse repetition time (ms)

Dtt time pause between trains (s)

T temperature (�C)um transmembrane potential (V)

u0 voltage parameter (V)

DU activation energy (kJ/mol)Z electrical conductivity disintegration index

Subscripts

E electrical

T thermal

Greeks

q correlation coefficientr electrical conductivity (Sm�1)

s characteristic damage time (s)

s1 limiting characteristic damage time (s)

Abbreviation

PEF pulsed electric fields

178 N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184

However, the application of the PEF-treatment alone

can be inefficient if any significant modifications of the

plant structure, like softening of the cell walls or viola-

tion of their integrity, are desirable. Additional soften-

ing of the plant tissues (carrots, potatoes and apples)

can be observed in combined mode of PEF treatment

at room temperature and mild thermal treatment

(Lebovka, Praporscic, & Vorobiev, 2004a, 2004b). Itwas shown that thermal softening at mild heating is

associated mainly with structural changes in the cell

walls, and, to the less extent, with damage of mem-

branes. The mild thermal and ohmic heatings allow to

improve mechanical juice extraction from plant tissues

(Lima & Sastry, 1999; Wang & Sastry, 2000, 2002;

Zhong & Lima, 2003).

In previous investigations practically all the PEFtreatment experiments were done at room temperature

(Bazhal, Lebovka, & Vorobiev, 2003; Fincan, DeVito,

& Dejmek, 2004; Fincan & Dejmek, 2002, 2003;

Lebovka, Bazhal, & Vorobiev, 2000, 2001, 2002;

Vorobiev et al., 2004) and the effect of temperature on

the PEF-induced damage phenomena of in food tissues,

practically, was not studied yet. Nevertheless, the elec-

troporation of membrane is sensible to the temperature(Zimmermann, 1986) and temperature can influence

PEF-induced damage in a plant tissue. The objective

of this work is to study temperature effect on the effi-

ciency of PEF treatment of a plant tissue.

Fig. 1. A scheme of the experimental setup. See text for details.

2. Materials and methods

As a representative object for investigation, a potato

tissue was chosen. Potatoes (Milva) of good and uni-

form quality were purchased at the local supermarket

and stored at 4 �C until required. The moisture contentwas within 83–85%.

We checked the quality of potatoes by carrying out

the stress relaxation test on fresh potatoes each time

we tested samples, to ensure that the texture did not

change. The samples were in the form of cylinders

having diameter d = 26mm, height h = 10mm in PEF

experiments and d = 10mm, h = 10mm in texturalexperiments. After preparation of the potato cylinders,

they were soaked into fresh potato juice prepared from

the same plant tissue at 20 �C. Fresh juice was chosenas a natural medium in order to reduce the degradation

of the sample.

A scheme of experimental setup is presented in Fig. 1.

The PEF treatment chamber consists of polypropylene

cylindrical glass with the inner diameter 26mm and anelectrode at the bottom. The treatment chamber, filled

with fresh potato juice, was placed to the water thermo-

10-2 10-1 100 101 102 1030

0.2

0.4

0.6

0.8

1

22 oC30 oC

τ

E=70 V/cm

Z

tPEF, s

40 oC49 oC

Fig. 2. Conductivity disintegration index Z versus time of PEF

treatment tPEF at the electric field strength E = 70V/cm and different

temperatures. Here, symbols correspond to the experimental data and

solid lines are drawn for the guidance of an eye.

N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184 179

stat kept at the desired temperature (T = 22–60 �C). Thesample was placed inside the chamber, after which the

second electrode was installed on the top of the sample

as it is shown in Fig. 1. An upper Teflon ring was used as

a thermo-isolation cover. The temperature control was

provided by a thermocouple Thermocoax type 2 (AB25 NN, ±0.1 �C) placed inside the sample. Two elec-trodes were connected to the PEF generator and LCR

meter.

The PEF generator, 1500V–20A (Service Electro-

nique UTC, France) provided the monopolar pulses of

near-rectangular shape (Lebovka et al., 2003). The

trains of pulses were used for PEF treatment. An indi-

vidual train consisted of n pulses with pulse duration tiand pulse repetition time Dt. There was a pause of Dttafter each train and then polarity of the next train was

changed to the opposite (Fig. 1). Preliminary experi-

ments had shown that such scheme of the PEF treat-

ment with the reversible polarity eliminated the

polarizing effects, which can be important at long dura-

tion of the PEF treatment at small fields (E < 100V/cm).

At long duration of the PEF treatment, an ohmic heat-ing of sample may occur, and to avoid the ohmic heating

effects, we used a longer inter-train pause time Dtt be-tween PEF trains. All experiments were carried out

using the electric field strength E not exceeding

500Vcm�1, number of pulses n = 1–30,000, pulse dura-

tion ti = 10�5–10�3 s, pulse repetition time Dt = 10�2 s,

number of trains N = 1–1000, and inter-train time

Dtt = 2–25s. The PEF treatment time during one trainis nti and the total PEF treatment time was calculated

as tPEF = nNti. The electrical conductivity was measured

with a LCR Meter HP 4284A (Hewlett-Packard) at the

frequency of 1000Hz selected as optimal for purposes of

removing the polarizing effects on the electrodes and tis-

sue. All the output data (current, voltage, electrical con-

ductivity and temperature) were recorded using a data

logger and software developed by Service ElectroniqueUTC, France.

After the PEF treatment the sample was immediately

removed to the cold juice for cooling and then placed in

the texture analyser to perform the stress relaxation

test. The textural measurements were performed in a

Texture Analyser (model TA-XT2, Stable Microsys-

tems, England). In the stress relaxation tests, the sample

structure non-uniformity was compensated by samplepreloading with a force of 0.1N. The speed of piston

displacement was 1mm/s and the maximum force

attained was F = Fmax = 20N. The corresponding strain

e0 was about 10%. All the stress relaxation curves

were recorded with 0.1 s resolution at the temperature

T = 22 �C.Each experiment was repeated at least three times.

For estimation of the damage degree, the electricalconductivity disintegration index Z was used (see e.g.

Lebovka et al., 2002)

Z ¼ r � rird � ri

ð1Þ

where r is the measured electrical conductivity value andthe subscripts �i� and �d� refer to the conductivities ofintact and maximally destroyed tissue, respectively.

The conductivity of the maximally destroyed material

rd was determined for the samples after the PEF treat-ment in the electric field E of 500Vcm�1 during the per-

iod tPEF of order 1s (Bazhal et al., 2003; Lebovka et al.,

2002). Application of Eq. (1) gives Z = 0 for an intacttissue and Z = 1 for a disintegrated material.

3. Results and discussion

3.1. Conductivity disintegration index and electrical

characteristic damage time

The typical curves of electrical conductivity disinte-

gration index Z versus PEF treatment time tPEF at dif-

ferent temperatures T and electric field strength E =

70V/cm are presented in Fig. 2. The values of Z grow

with time during the PEF treatment and their maximal

value is attained at Z = 1. The time of treatment tPEF,

required for attaining the maximal sample damage

(Z � 1), decreases with temperature increase.The characteristic electrical damage time sE was esti-

mated as a PEF treatment time required for Z to attain

one-half of its maximal value, i.e. Z = 0.5 (Bazhal et al.,

2003; Lebovka et al., 2002). Dependencies of the charac-

teristic electrical damage time sE versus electric field

strength E at different temperatures are presented in

100 200 300 400 500

10-4

10-3

10-2

10-1

100

101

102

103

22oC30oC

E, V/cm

τ E,s

40oC

49oC

Fig. 3. Characteristic electrical damage time sE versus electric fieldstrength E at different temperatures. Here, symbols correspond to the

experimental data and solid lines show results of the least square fitting

of experimental data using Eq. (3). The error bars represent standard

data deviations.

20 30 40 50

40

60

80

100

120

140

160

20 30 40 5010-5

10-4

10-3

10-2

30

40

50

60

70

80

T, ˚C

τ E,∞

,sE

o,V

/cm

∆UE

kJ/m

ol

Fig. 4. The empirical parameters sE,1, DUE, and E0 in Eq. (3) versus

temperature. Here, symbols with error bars correspond to the

experimental data and solid lines are drawn for the guidance of an eye.

180 N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184

Fig. 3. The characteristic electrical damage time sE de-creases with increase of both temperature T and electric

field strength E.Note that the characteristic electrical damage time

may be large enough (sE = 10–1000s) at small fields(E < 100V/cm) and room temperature of treatment

(T = 22 �C), and in continuous mode of the PEF treat-ment the ohmic heating is essential. The data presented

in Figs. 2 and 3 are obtained for a discontinuous mode

of treatment with a pause between trains that allows to

avoid additional heating, and temperature did not in-crease more than by 1 �C during the PEF treatment.The influence of the electric field strength E on the

characteristic electrical damage time sE can be explainedon the basis of electroporation theory (Weaver &

Chizmadzhev, 1996), as it was demonstrated in our

previous work (Lebovka et al., 2002). The characteristic

electrical damage time sE of a single membrane is:

sEðum; T Þ ¼ sE;1 expDUE

RT ð1þ ðum=u0Þ2Þ; ð2Þ

where sE,1 is a parameter (sE! sE,1 in the limit of very

high electric fields), DUE is the activation energy,

R = 8.314JK�1mol�1 is the universal gas constant, T

is the absolute temperature and u0 is the voltage param-

eter (u0 is expressed in Volts).

Experimental data obtained by Lebedeva (1987) for

the lipid membranes allow to estimate parameters inEq. (2) as sE,1 � 3.7 · 10�7 s, DUE � 270kJ/mol, and

u0 � 0.17V (Lebovka et al., 2000, 2002).

In a general case of a cellular tissue, the relation be-

tween the characteristic electrical damage time sE and

temperature T or electric field intensity E has a more

complex form (Lebovka et al., 2002; Vorobiev et al.,

2004). The transmembrane potential um in Eq. (2) is a

complex function of cell geometry and dimensions and

depends on the angle between the external field E direc-

tion and the normal to the membrane surface. For aspherical cell, the highest drop of potential occurs at

the cell poles and the transmembrane potential um is

proportional to the cell radius R and electric field inten-

sity E, um � 1.5RE (Schwan, 1957). In analogy with Eq.

(2) the following equation can be proposed for descrip-

tion of the experimental data on characteristic electrical

damage time sE versus temperature T or electric field

intensity E in a cellular tissue:

sEðE; T Þ ¼ sE;1 expDUE

RT ð1þ ðE=E0Þ2Þ; ð3Þ

where sE,1, DUE and E0 are adjustable empirical

parameters.

Solid lines in Fig. 3 show results of the least square

fitting of experimental data using Eq. (3). The empirical

equation (3) allows to obtain a rather good description

of the experimental data and the correlation coefficients

q lie in the interval of 0.98–0.99. Both the estimated acti-vation energy DUE and the limiting characteristic electri-cal damage time sE,1 decrease with increase of the

temperature T, and the empirical field strength parame-

ter E0 grows with temperature (Fig. 4).

The observed temperature changes in the empirical

parameters sE,1, DUE and E0 can reflect possible struc-

tural transition inside membrane structure with temper-

ature. The biological membranes are very complex

Fig. 5. Force versus time t curves for potatoes, freeze-thawed and

treated by PEF at the electric field strength E = 70V/cm, different time

of PEF treatment tPEF and temperatures T = 22�C (a) and T = 50�C(b). The relaxation measurements were carried out at T = 22�C.

N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184 181

aggregates formed by different lipid species and there are

possible phase transitions in the temperature interval

20–55 �C (Exerova & Nikolova, 1992; Mouritsen &

Jørgensen, 1997) that influence heat capacity, compressi-

bility and elasticity of membranes (Heimburg, 1998,

2000). In the vicinity of phase transition, the fluctuationsof the thermodynamical properties are high, and pores

arise in the membrane structure more easily. So, electro-

poration and PEF-induced damage can be very sensible

to the structural changes in membranes. For example, it

is known that for a single membrane the breakdown

voltage appreciably decreases in the temperature inter-

val 20–50 �C (Zimmermann, 1986). But despite the con-siderable progress achieved in the theory ofelectroporation (Weaver & Chizmadzhev, 1996), the

physical mechanisms of thermal influence on electropo-

ration are not well understood yet.

3.2. Textural relaxation of PEF-treated potatoes

Fig. 5a and b present the force relaxation curves for

potatoes treated by PEF at the electric field strengthE = 70V/cm and temperatures 22 �C (a) and 50 �C (b).

The PEF treatment does not result in the textural state

of a freeze-thawed apple tissue. As it was demonstrated

in (Lebovka et al., 2004a), even in the case of a rather

high electric field strength (E = 1100V/cm) and long

PEF treatment duration (tPEF = 0.1s), the observed tex-

ture of potato is stronger than that for the freeze-thawed

tissue.Different approaches were proposed for description

of the complex force relaxation behaviour of plant

tissues with inhomogeneous structure (Bouzrara &

Vorobiev, 2003; Hort & Grys, 2001; Fincan & Dejmek,

2003; Kaur, Singh, Sodhi, & Gujral, 2002; Peleg &

Normand, 1983). In this work we use the simplified

method proposed in Lebovka et al. (2004a, 2004b),

which approximate the initial portion of the relaxationcurve in the time interval t < 100s by the logarithmic

equation:

F ¼ F 0ð1� log10t=log10t1Þ; ð4Þwhere F0 is a fitting parameter and t1 is the effective

relaxation time corresponding to the hypothetical time

of complete tissue relaxation (F = 0) if the relaxationbehaviour is supposed to remain logarithmic. The more

is the tissue damage, the less is the effective relaxation

time t1. In the numerical fitting procedure the loading

portion of the stress history was removed and time

count begins from the point where the force reaches its

maximum F = Fmax = 20N (Lebovka et al., 2004a,

2004b).

Fig. 6 presents the effective relaxation time t1 versusPEF treatment time tPEF for the potato tissues at the

electric field strength E = 70V/cm and two different tem-

peratures T = 22 �C and T = 50 �C. As it can be seen

from Fig. 6, the temperature influences significantly

the PEF treatment duration tPEF. The effective relaxa-

tion time t1 substantially decreases in the interval tPEF10–103s at T = 22 �C and in the interval tPEF � 10�2–

1s at T = 50 �C. These data are in accordance with thebehaviour of the conductivity disintegration index Z

versus PEF treatment time tPEF at the same electric field

strength E = 70V/cm as presented in Fig. 2. The effective

relaxation time t1 at long duration of the PEF treat-

ment is still larger then that of completely damaged

freeze-thawed tissue, but additional softening was ob-served for the treatment at higher temperature

T = 50 �C. Additional thermal softening at T = 50 �Cmay be associated with different factors, such as a loss

10-2

10-1

100

101

102

103101

102

103

104

Freeze-thawed

tPEF, s

t ∞,s

E=70 V/cm

T=50 ˚C 22 ˚C

Fig. 6. Effective relaxation time t1 versus PEF treatment time tPEF for

the potato samples at different temperatures T. Dashed horizontal line

shows limiting values for freeze-thawed potatoes.

0.0029 0.003 0.0031 0.0032101

102

103

104

105 4070 5060

1/T, K-1

T, ˚C

τ T,s

Fig. 7. Arrhenius plot of the characteristic thermal damage time sTversus inverse temperature 1/T for the potatoes. Points are the

experimental data, solid line is the result of the linear least mean square

fitting.

182 N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184

of turgor, separation of cells in the region of the middle

lamella, change in the cell geometry, swelling of cell

walls, trapped air expulsion, etc. (Aguilera & Stanley,

1990).

3.3. Thermally induced damage of potatoes

Note that in all the previously described experiments

the PEF treatment was done under the mild thermal

conditions in the temperature interval T = 20–50 �Cand during the time not exceeded 30min. For potatoes,

the thermal damage and softening of tissue at such mildtreatment conditions are practically absent (Lebovka

et al., 2004a) and the observed effects are related to

the PEF-induced damage. But at higher temperature

or treatment time values, the cellular membranes begin

to suffer a noticeable irreversible damage (Andersson,

Gekas, Lind, Oliveira, & Oste, 1994; Thebud &

Santarius, 1982) and the effects of the thermal damage

and additional thermal softening become important(Lebovka et al., 2004a).

For control of the thermally induced damages in the

structure of potatoes, the investigation of changes in the

conductivity disintegration index Z with time t were

performed and the corresponding values of the charac-

teristic thermal damage time sT were estimated. Tissueheating and measurements of Z values were performed

in a heated potato juice. The samples used in theseexperiments had a form of a cylinder with diameter

d = 26mm and height h = 5mm; the time of temperature

relaxation after potato cylinder immersion into potato

juice was approximately 100s.

Fig. 7 presents the characteristic thermal damage

time sT of the potato tissue treated thermally at differenttemperatures. As it follows from the Arrhenius law:

sT ¼ sT;1 expðDUT=RT Þ; ð5Þthe estimated activation energy is DUT � 240kJ/mol and

the limiting characteristic thermal damage time is

sT,1 � 10�35 s.

The characteristic thermal damage time sT is ratherhigh (>1.5h) at temperatures below 50 �C, so, the ther-mally induced cell damage is unessential in the PEF-

experiments represented in previous sections.

4. Concluding remarks

The results obtained in this work indicate an essential

dependence of the electrically induced damage in plant

tissues versus temperature in the investigated interval

22–50 �C. The observed significant decrease of the char-acteristic electrical damage time sE with temperature T

increase is likely owing to the fact that electroporation

efficiency is more pronounced at high temperatures

(Zimmermann, 1986). But mechanisms of the PEF in-

duced damage in plant tissues are rather complex and

not yet completely understood (Fincan & Dejmek,

2002, 2003; Lebovka et al., 2000, 2001, 2002). The ob-

served temperature effects can reflect changes in the cellmembrane fluidity, thermal phase transitions inside the

membrane (Exerova & Nikolova, 1992; Mouritsen &

Jørgensen, 1997), thermal softening and structural

N.I. Lebovka et al. / Journal of Food Engineering 69 (2005) 177–184 183

changes in cell walls at a mild heating (Alvarez & Canet,

2001; Andersson et al., 1994; Mittal, 1994; Rao & Lund,

1986). At small electric field strengths (E < 100V/cm)

and room temperature (T � 22 �C), the noticeable elec-troporation effects in potato tissue treatment duration

of the order of 10–1000s (see Fig. 3), but the effectiveelectrical damage of tissue occurs at a treatment time

of the order of 10�2–1s at T � 50 �C. The improved elec-troporation efficiency at temperatures of the order of

T � 50 �C allows to explain the enhancement diffusion

in beet tissue during a moderate electric field treatment

at rather small fields, E < 23.9V/cm and temperature

T = 45 �C (Kulshrestha & Sastry, 2003). The combina-

tion of PEF treatment with mild ohmic heating (up toT = 50 �C) can give a unique opportunity to reach hightissue disintegration degree at moderate electric field

strengths below 100V/cm without any noticeable losses

of product quality. The optimal parameters of the com-

bined PEF processing and mild ohmic heating would de-

pend on the type of plant tissue, and factors related to

the energy consumption and should be the subject of

future investigations.

Acknowledgments

The authors would like to thank the ‘‘Pole Regional

Genie des Procedes’’ (Picardie, France) for providing

financial support. Authors also thank Dr. N.S. Pivovar-

ova for her help with preparation of the manuscript.

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