Trends in Food Science & Technology 99 (2020) 650–659

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Trends in Food Science & Technology

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Microbial inactivation by ohmic heating: Literature review and influence of T

different process variables
Wagner Augusto Müller, Ligia Damasceno Ferreira Marczak, Júlia Ribeiro Sarkis∗
Federal University of Rio Grande do Sul (UFRGS), Chemical Engineering Department, Rua Ramiro Barcelos, 2777, 90037-007, Porto Alegre, RS, Brazil

ARTICLE INFO ABSTRACT

Keywords: Background: The elimination of microbial cells is one of the most critical steps in food processing. Conventional
Emergent technologies heating is the application of diffusive and convective heat mechanisms and is traditionally applied to assure food
Food spoilage safety. However, such process is also harmful to others thermosensitive compounds, compromising desirable
Electroporation sensorial characteristics. The large temperature gradients caused by conventional heating result in lower thermal
D value
efficiency, overheated zones and high processing times. To overcome these limitations, emergent technologies
Ohmic heating
have been studied in the past years, such as ohmic heating.
Scope and approach: The aim of this review was to analyse the state of the art of microbial inactivation by ohmic
heating. This study emphasizes comparisons of ohmic and conventional heating, as well as comparisons of ohmic
heating in several distinct scenarios (such as variations in the frequency and electric field).
Key findings and conclusions: The literature analysis shows that the most analysed microbial species was
Escherichia coli and studies dealing with fungi were less numerous comparing with studies dealing with bacteria.
Concerning the lethality of conventional and ohmic heating, authors have shown that ohmic treated foods had
smaller D values in various temperatures. The effect of frequency lacks of experimental data to explain the real
impact of this parameter in the inactivation rate, once different authors have found divergent results. Moreover,
increases in the electric field and salt content and decreases in the pH, fat and solid content have demonstrated
higher heating rates and, therefore, higher inactivation rates.

1. Introduction is commonly provided by water steam or liquid water at high tem-

Among all the possible causes of food deterioration, the dis-
semination of microorganisms in foodstuffs is of special relevance to the
food industry. In addition to the food waste caused by discarding
contaminated products, some microorganisms can also pose public
health problems. These problems are related to pathologies caused by
the microorganism itself or toxins that are synthesized by some species.
Thus, the inactivation of microorganisms down to an acceptable
number is one of the most critical concerns in the food processing field
(Biranjia-Hurdoyal & Latouche, 2016).
1.1. Traditional approaches for microbiological inactivation and its
limitations
Traditionally, microbiological inactivation processes occur through
heat application to the product. In conventional heating (CH), heat is
transferred mainly by conductive and convective mechanisms. The heat
peratures. The most important parameter in thermal processes is the
time/temperature binomial, which establishes the time in which food
must be kept at a fixed temperature in order to obtain the desired de-
gree of microbial reduction (Ibarz & Barbosa-Cánovas, 2003).
Conventional thermal processing causes large thermal gradients
inside the product. Thus, it is necessary to ensure that the coldest spot
in the product (critical point) has reached the time/temperature bino-
mial (i.e., the binomial must be calculated based on the coldest point of
the product). The thermal effect on microbial lethality is mainly due to
the denaturation of tertiary and quaternary structures of proteins
(Molugu et al., 2016). This causes inactivation of enzymes that are
needed for microbial metabolism. Moreover, heat application also af-
fects the genetic code of microorganisms and promotes cell wall dis-
ruption (cell lysis). Heat application also negatively impacts other food
constituents and thermosensitive compounds (e.g., vitamin C and cal-
cium), and compounds responsible for sensorial characteristics are the
most affected (Jaeschke, Marczack, & Mercali, 2016; Marszałek,

∗
Corresponding author.
E-mail addresses: wagner.a.muller@hotmail.com (W.A. Müller), ligia@enq.ufrgs.br (L.D. Ferreira Marczak), julia@enq.ufrgs.br,
juliasarkis@gmail.com (J.R. Sarkis).

https://doi.org/10.1016/j.tifs.2020.03.021
Received 16 May 2019; Received in revised form 2 March 2020; Accepted 15 March 2020
Available online 19 March 2020
0924-2244/ © 2020 Elsevier Ltd. All rights reserved.
W.A. Müller, et al. Trends in Food Science & Technology 99 (2020) 650–659

Woźniak, Skąpska, & Mitek, 2016; Wawire et al., 2016). As aforemen-
tioned, the time/temperature binomial selection must take into account
the coldest spot within the product, which causes a natural tendency to
overheat some regions, resulting in critical losses of desirable com-
pounds, high processing times and low energetic efficiency.
1.2. Emergent technologies for microbial inactivation - ohmic heating
In an attempt to overcome these drawbacks, less aggressive methods
to nutritional and sensorial properties have been researched; these
methods are known as emergent technologies. Microwaves, radio-
frequency, high pressure, pulsed electric fields and ultrasound are some
examples. Among the emergent technologies, ohmic heating (OH) has
been extensively researched in recent years (Cappato et al., 2018; Gally
et al., 2017; Parmar, Singh, Meena, Borad, & Raju, 2018; Silva, Santos,
& Silva, 2017).
During OH, microbial inactivation also occurs due to thermal me-
chanisms. However, the physical principle involved is fundamentally
different from the CH. OH consists of the passage of alternated electrical
current through the foodstuff, which acts as an electrical resistance,
generating thermal energy by Joule's effect. For this purpose, two
electrodes are inserted into the extremities of an ohmic cell, which
contains the food product. Unlike the CH method, the heating is due to
volumetric internal energy generation as a result of the (re)orientation
of ions in response to the alternated current (Ruan, Ye, Chen, Doona, &
Taub, 2002).
The following advantages are attributed to OH: faster heating, the
possibility of uniform heating of biphasic foods (provided that the
phases have similar electric conductivities), high energetic efficiency
and more independence from the thermophysical properties and ex-
ternal convective coefficient. Furthermore, as the heat is generated
volumetrically, the food tends to warm up more uniformly. Superheat,
losses of electrode material (by corrosion at certain frequencies and by
erosion) and the strong dependence on electric conductivity are lim-
itations of this technology (Kaur & Singh, 2016). In addition to mi-
crobiological inactivation, OH processing has several other applica-
tions. Table 1 shows some examples of these applications.
1.3. Ohmic heating applied for microbiological inactivation
Initially, it was believed that the microbiological parameters of
ohmic and conventional heating were essentially equal (Cho, Yousef, &
Sastry, 1999). However, recent studies have suggested the existence of
secondary non-thermal inactivation phenomena during OH. These
phenomena are attributed to electrical effects and can result in an ad-
ditional advantage of this process. Nevertheless, different authors have
found controversial results depending on the microorganism and the
process conditions applied. Considering the importance of micro-
biological safety and the broad number of OH applications, these con-
tradictory results justify the necessity to gather different data in order
to search for patterns common to several authors. In this context, the
objective of the present work was to perform a literature review re-
garding the more important studies involving microbiological in-
activation kinetics using OH.
Several authors have revised aspects concerning OH applications in
the food industry, both in articles and in books (Cappato et al., 2017;
Gavahian, Tiwari, Chu, Ting, & Farahnaky, 2019; Kaur & Singh, 2016;
Knirsch, Santos, Vicente, & Penna, 2010; Ramaswamy, Marcotte,
Sastry, & Abdelrahim, 2014; Ruan, Ye, Cheen, & Doona, 2002; Sakr &
Liu, 2014; Tian, Yu, Wu, & Dai, 2018; Varghese, Pandey, Radhakrishna,
& Bawa, 2014). A microbiological section or chapter was presented in
most of these studies. However, to the best of our knowledge, the
previous literature did not cover the subject in its entirety. In addition,
most of them focused only on comparisons between OH and CH and left
out analyses concerning OH under different conditions, which is also of
great importance. Recently, Tian et al. (2018) performed a review fo-
cusing on microbial inactivation by OH, dealing with the process
parameters and some general aspects of this technology, such as hurdle
technologies, prospects and benefits of this technology and the appli-
cation of moderated electric fields for microbiological growth. In con-
trast, the present work focused more on kinetic information, meth-
odologies that assure an adequate comparison between CH and OH, the
application of OH at different conditions and the mechanisms that ex-
plain the observed effects.

Table 1
Ohmic heating applications and limitations suggested by each author.
OH application Benefits of use Limitations Reference(s)

Solution concentration
Texture modification
Proofing of bread dough
Blanching
Cooking
Heat source for desalination
processes
Enzyme inactivation
Thawing
Ethanol distillation
Ohmic assisted hydrodistillation
Package of food for long-duration
space missions
Extraction
Product with higher quality at the end of the
process.
Achieve a predefined texture in shorter time
and more uniform texture profile.
Reduction in time needed to reach the desired
expansion due to higher heat rates.
Reduction in processing time, reduction of
leaching and improvement of quality of the
final product.
Diminution of energy consumption and slight
reduction in the cooking time.
Improvement of plant reliability and
duration, reducing the necessity of chemicals
and maintenance activities.
Enhancement of inactivation rate of enzymes
in determined conditions.
Reduction in thawing time and more uniform
temperature profile.
Reduction in processing time and better
process control.
Better process control, reduced distillation
costs and shorter processing time.
Enable the heating of foods in space missions.
Higher energy efficiency and process
reliability.
Lack of knowledge about different types of electrodes (Icier & Ilicali, 2005;
on energy loss. Parmar et al. (2018)
Non-uniform heating of some materials in continuous Gavahian et al. (2019)
operation; electrode corrosion and its potential
negative effects on consumer health.
Lack of knowledge about the quality of proofing when Gally et al. (2017)
using OH (porosity, texture and crumb structure).
High dependency on the products' composition Xin, Zhang, Xu, Adhikari, and Sun
because of the electrical conductivity. (2015)
Difficulty in providing good contact among the food (Ho & Farid, 2004;
surface and electrodes. Kanjanapongkul, 2017)
Higher colour changes in high electric fields, Assiry, Gaily, Alsamee, and
depending on the products' concentration. Sarifudin (2010)
Electrode corrosion and its potential negative effects Jakób et al. (2010)
on consumer health.
Difficulty in providing good contact among the food Bozkurt and Içier (2012)
surface and electrodes.
Safety considerations for high concentration mixtures Gavahian, Farahnaky, and Sastry
because of the risks associated with sparks and (2016)
flammability.
Lack of economic studies for scale up and high Gavahian and Farahnaky (2018)
dependency on products' composition.
Modifications of the package for homogeneous Sastry et al. (2009)
sterilization.
Necessity of a detailed techno-economic analysis for (Pereira, Rodrigues, Genisheva,
scale up. Teixeira, & Freitas, 2016)

651
W.A. Müller, et al.
1.4. Methodology and manuscript organization
To elaborate the present review, a survey of published papers was
accomplished using the keywords “ohmic heating” and “microbial in-
activation” as well as their synonyms (e.g., “joule heating” and “re-
sistive heating” as synonyms for ohmic heating and “microbiological
inactivation”, “bacterial inactivation” and “fungi inactivation” as sy-
nonyms for “microbial inactivation”). The articles selected were pub-
lished in scientific journals that apply a peer review system and per-
formed a parametric analysis of microorganism inactivation. Articles
that only analysed the overall performance of microbial inactivation at
the end of the process and did not provide kinetic parameters for
comparison were not included.
The manuscript is divided into five sections. The first section in-
vestigates general aspects from a preliminary article analysis dealing
with microbiology and OH, such as the number of publications, mi-
croorganisms and culture medium used and processing parameters
studied. The second section deals with the comparison of the tem-
perature effects in both OH and CH. As OH was conceived as an al-
ternative to CH, special attention is given to this topic. The temperature
effects are discussed in three subsections: vegetative species, spores and
aspects concerning spores and vegetative cells. The third, fourth and
fifth sections are related to the effects of frequency, electric field and
composition in microbial inactivation, respectively. All the comparisons
were made by analysing the microbiological parameters of the in-
activation models.
2. General aspects
In total, 32 articles were found, and Table 2 shows their most re-
levant information. As can be observed, the most analysed micro-
organism was Escherichia coli (16 of the 32 analysed studies), followed
by Salmonella typhimurium (11 works) and Listeria monocytogenes (9
works). In general, authors justified the choice of these specific three
microorganisms due to their high level of potential pathogenicity. In
fact, food outbreaks caused by these microorganisms are frequently
found in the literature (Crook et al., 2003; Dong, Yang, & Chen, 2010;
Schoder, Stessl, Szakmary-Brändle, Rossmanith, & Wagner, 2014). It is
important to highlight that just three of the studies (Hashemi et al.,
2019; Won, Chungyung, Ki-Myung, & Cherl-Ho, 2002; Yildiz & Baysal,
2006) analysed fungal inactivation.
Concerning the culture media, 16 studies focused on fruit and ve-
getable juices, demonstrating that the study of their spoilage by mi-
croorganisms is still a relevant issue. Santos et al. (2018) showed that
several juices presented spore contamination at unacceptable levels,
even after pasteurization. Rico-Munoz (2017) points out that the in-
gredients and packaging materials are also sources of contamination
since they can carry a range of microbial species, and this needs to be
considered to assure final product security.
Relating to the state of the microorganisms, studies dealing with
spores were less numerous than studies that analysed vegetative bac-
terial cells (13 against 21 articles). In the spore form, the thermal re-
sistance of the microorganisms tends to rise dramatically, with higher
temperatures being necessary to inactivate them (Tranquillini,
Scaramuzza, & Berni, 2017).
All the authors performed experiments using kinetic curves of mi-
croorganism survival over time, and the temperature was the most
analysed variable (20 of the 32 works). Thirteen papers analysed dif-
ferent electric fields, and 5 investigated different frequency ranges. The
composition parameters °Brix, fat and salt content were studied in one
paper each, while the pH effect was studied in two papers. As can be
observed, works that analysed spore inactivation used higher tem-
peratures (next to or even above 100 °C). Finally, a comparison with CH
was performed in 22 articles.
Table 3 shows the effective parameters considered for analysis in
this paper, as well as some of the research needs raised for each
652
Trends in Food Science & Technology 99 (2020) 650–659
parameter. It can be seen that there are still many questions to be ad-
dressed in OH microbial inactivation studies, which will be discussed in
more detail in the next sections.
3. Temperature effects
The present section analyses articles comparing OH and CH.
Somavat, Mohamed, Chung, Yousef, and Sastry (2012) suggested some
procedures that need to be followed in microbiological studies for
adequate comparisons. Among the suggested procedures, the most re-
levant is the equality of the temperature profiles in both heating pro-
cesses. Similar heating curves are of key importance to investigate the
electrical effects on microbial inactivation. This is endorsed by Peleg
(2006), who demonstrated that subpopulations of one specific micro-
bial species can adapt differently depending on the thermal profile
applied. In the works by Kim et al. (1996), Uemura and Isobe (2003),
Park and Kang (2013), Tola and Ramaswamy (2014), Lee, Kim, and
Kang (2015), Kim and Kang (2015a), Kim and Kang (2015b), Ryang
et al. (2016) and Inmane et al. (2019), the methodology sections failed
to specify if the temperature profiles were matched. Therefore, even
though they showed good results concerning the application of OH,
these works will not be considered in the subsequent discussion.
3.1. Aspects concerning vegetative species
The temperature profiles were matched in three studies in order to
investigate the effects of this variable on the inactivation of vegetative
species. Pereira, Martins, Mateus, Teixeira, and Vicente (2007) found
lower D values in OH processing in all temperatures except at the
lowest analysed (55 °C), in which the D value was higher. The result at
55 °C was justified by the fact that OH processing at conditions close to
the ideal reproduction temperature stimulates microorganism growth
despite its inactivation, as previously demonstrated in the literature
(Cho, Yousef, & Sastry, 1996). Himoto et al. (2008) found lower D
values for OH at all analysed temperatures for the total viable aerobes
(D values varied from 0.44 to 11.25 min in CH and from 0.38 to
8.64 min in OH) and for Streptococcus thermophilus inactivation (var-
iation from 0.2 to 7.54 min in CH and 0.16–6.59 min in OH). Rodrigues
et al. (2018) found higher inactivation rates for Staphylococcus aureus
for all temperatures investigated: the D values varied from 3.41 to
15.06 min at 57.5 °C and from 0.53 to 1.42 min at 65 °C in OH and CH,
respectively. In the case of E. coli, significantly different values were
found only for the lowest temperature analysed. However, it is im-
portant to emphasize that the D values of E. coli were relatively low in
all of the analysed scenarios (magnitude of 10−1 min). This fact sug-
gests that the processes with high temperatures tend to have similar
inactivation results under both types of heating, but this is dependent
on the microorganism species and its form. The proposed mechanism is
illustrated in Fig. 1, in which thermal (mostly due to protein dena-
turation) and nonthermal effects (electroporation) are visualized at
lower temperatures and only the thermal effects are pictured at higher
temperatures.
The results concerning vegetative species showed that OH tends to
accelerate inactivation in certain scenarios, even if the food is sub-
mitted to the same temperature profile. This finding suggests that the
application of an electric field can promote nonthermal mechanisms of
inactivation. However, these effects are often secondary (and not re-
levant in some cases, as in the aforementioned E. coli example) to the
thermal effect, even in the presence of nonthermal mechanisms.
The most preponderant nonthermal mechanism, at least for vege-
tative forms, is electroporation. Microorganisms have electrically
charged intracellular compounds, such as cations (e.g., K+ and Na+)
and negatively charged proteins (Madigan, Bender, Buckley, Sattley, &
Stahl, 2017). The presence of an external electric field provokes a
transmembrane potential in the phospholipidic membrane, whereby
negatively charged intracellular compounds will be attracted by the
W.A. Müller, et al. Trends in Food Science & Technology 99 (2020) 650–659

Table 2
Analysed articles and relevant microbiological information (studied microorganism and its state, analysed food media, process parameters and presence of com-
parisons with CH).
Reference Microorganism(s) Microorganism's state Culture medium Process parameters Comparison with CH
at same condition

Kim et al. (1996) Bacillus Sporulated Meatball Temperature (118, 123, 125, No
stearothermophilus 128 and 132 °C)
Composition (salt content)
Cho et al. (1999) Bacillus subtilis Sporulated Saline water Temperature (88, 92.3, 95 and Yes
97 °C)
Uemura and Isobe (2002) Escherichia coli Vegetative Saline water Electric field (7, 9, 11 14, Yes
16 kV/cm)
Won et al. (2002) Saccharomyces cerevisiae Vegetative Phosphate buffer Heating ramp (50–90 °C) Yes
suspension Frequency (60, 600, 6,000 and
60,000 Hz)
Electric field (10, 15 and 20V/
cm)
Uemura and Isobe (2003) Bacillus subtilis Sporulated Orange Juice Temperature (121 °C for OH No
and 100 °C for CH)
Yildiz and Baysal (2006) Aspergillus niger Vegetative Tomato Electric field (36, 48, 68 and No
108 V/cm)
Pereira et al. (2007) Escherichia coli Vegetative E. coli and Goat milk for E. coli and For E. coli: Temperature (55, Yes
Bacillus licheniformis sporulated B. licheniformis cloudberry jam for B. 60, 63, 65, 67 and 75 °C)
licheniformis For B. licheniformis:
Temperature (70, 75, 80, 85
and 90 °C)
Himoto et al. (2008) Streptococcus Vegetative Milk Temperature (57,60, 72 °C for Yes
thermophilus viable aerobes and 70, 75 and
Viable aerobes 80 °C for S. thermophilus)
Baysal and Icier (2010) Alicyclobacillus Sporulated Orange Juice Temperature (70, 80 and Yes
acidoterrestris 90 °C)
Electric field (30, 40 and 50 V/
cm)
Sagong et al. (2011) Escherichia coli O157:H7 Vegetative Orange juice Electric Field (10, 15 and No
Salmonella Typhimurium Tomato juice 20 V/cm)
Listeria monocytogenes
Somavat et al. (2012) Geobacillus Sporulated Tomato juice Temperature (121, 125 and Yes
stearothermophilus 130 °C)
Frequency (60 Hz and 10 kHz)
Park and Kang (2013) Escherichia coli O157:H7 Vegetative Buffered peptone water Temperature (55, 58 and Yes
Salmonella Typhimurium Apple juice 60 °C)
Listeria monocytogenes
Lee et al. (2013) Escherichia coli O157:H7 Vegetative Salsa Frequency (60, 100, 300, 500, No
Salmonella Typhimurium 1,000, 10,000 and 20,000 Hz)
Tola and Ramaswamy (2014) Bacillus licheniformis Sporulated Carrot juice Temperature (87, 92 and Yes
95 °C) pH (4.5, 5.5 and 6.2)
Somavat et al. (2013) Bacillus coagulans Sporulated Tomato juice Temperature (95, 100, 105 and Yes
110 °C)
Frequency (60 Hz and 10 kHz)
Lee et al. (2015) Escherichia coli O157:H7 Vegetative Orange juice Temperature (50, 55 and No
Salmonella Typhimurium 60 °C) pH (2.5, 3.5 and 4.5)
Listeria monocytogenes
Kim and Kang (2015a) Escherichia coli O157:H7 Vegetative Skim milk Temperature (55, 60, 65 and Yes
Salmonella Typhimurium Milk cream 70 °C)
Listeria monocytogenes
Kim and Kang (2015b) Escherichia coli O157:H7 Vegetative Milk cream Fat content (0, 3, 7 and 10% Yes
Salmonella Typhimurium (w/w))
Listeria monocytogenes
Ryang et al. (2016) Bacillus cereus Sporulated Tsuyu sauce Temperature (95, 105, 115 and No
125 °C)
Park et al. (2017) Escherichia coli O157:H7 Vegetative Apple juice Electric field (30, 40, 50 and No
Salmonella Typhimurium 60 V/cm)
Listeria monocytogenes Brix (18, 24, 36, 48 and
72°Brix)
Kim, Choi, et al. (2017) Escherichia coli O157:H7 Vegetative Buffered peptone water Frequency (60, 200, 500 and No
Salmonella Typhimurium Tomato juice 1000 Hz)
Listeria monocytogenes
MS-2 phage
Kim, Choi, et al. (2017) Alicyclobacillus Sporulated Apple juice Temperature (85, 90, 95 and Yes
acidoterrestris 100 °C)
Murashita, Kawamura, and Koseki Bacillus subtilis Sporulated Sodium chloride Electric field (5, 10 and 20 V/ Yes
(2017) solution cm)
Frequency (20, 40 and 60 kHz)
Rodrigues et al. (2018) Staphylococcus aureus Vegetative Infant formula Temperature (57.5, 60, 62.5 Yes
Escherichia coli and 65 °C)
(continued on next page)

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W.A. Müller, et al. Trends in Food Science & Technology 99 (2020) 650–659

Table 2 (continued)

Reference Microorganism(s) Microorganism's state Culture medium Process parameters Comparison with CH
at same condition

Kim, Park, and Kang (2018) Escherichia coli O157:H7 Vegetative Buffered peptone water Electric field (9.43, 10.93 and No
Salmonella Typhimurium Tomato juice 12.14 V/cm)
Listeria monocytogenes
Shao et al. (2019) Escherichia coli O157:H7 Vegetative Broth Electric field (5, 7.5 and 10 V/ Yes
cm)
Mok et al. (2019) Escherichia coli K12 Vegetative Apple juice Temperature (40 and 50 °C) Yes
Electric field (20, 40, 60 and
120 V/cm)
Shear rate (454.6, 166.8 and
2879 s−1)
Inmanee, Kamonpatana, and Pirak Listeria monocytogenes Vegetative Sausage Temperature (75 °C) Yes
(2019)
Hashemi and Roohi (2019) Escherichia coli Vegetative Blended citrus juice Voltage (150, 200, 250 V) Yes
Staphylococcus aureus
Salmonella enterica
Salmonella Typhimurium
Shigella dysenteriae
Shigella flexneri PTCC
Hashemi, Gholamhosseinpour, Escherichia coli Vegetative Cantaloupe juice Voltage (100 and 200 V) Yes
et al. (2019) Salmonella Typhimurium
Salmonella Enteritidis
Straphylococcus aureus
Hashemi, Gholamhosseinpour, Leuconostoc mesenteroides Sporulated for Byssochlamys Sour orange juice Temperature (21–86 °C) Yes
et al. (2019) Lactobacillus acidophilus fulva and vegetative for the Current (0–16 A)
Lactobacillus plantanarum others Voltage (0–300 V)
Sacharomyces cerevisae
Byssochlamys fulva
Zygosaccharomyces rouxii
Schottroff et al. (2019) Bacillus subtilis Sporulated NaSO4 solution Spore composition Yes

external positive charge, and vice versa. If the applied voltage is higher
than the membrane limit, pores will be formed in the cellular structure,
resulting in membrane lysis and, consequently, microbial death. Even
as a secondary effect in OH, in other electrical processes, such as pulsed
electric field, it is responsible for the microbial inactivation. The work
performed by Won et al. (2002) corroborated this theory, demon-
strating that the amount of exuded intracellular material for Sacchar-
omyces cerevisiae cells was greater in OH treatment compared with CH.
To illustrate these differences between treatments, Table 4 shows D
values for E. coli inactivation by CH and OH in two different food
media.
3.2. Aspects concerning spores
Somavat et al. (2012) and Somavat, Mohamed, and Sastry (2013)
compared CH and OH in two different frequencies (60 Hz and 10 kHz)
using Geobacillus stearothermophilus and Bacillus coagulans spores in
tomato juice, respectively. At 121 °C, Somavat et al. (2012) found that
the high frequency OH resulted in higher values of inactivation when
compared with low frequency OH and with CH; at 125 °C, both fre-
quencies showed better results than CH, and at 130 °C, all processes
were statistically equal. On the other hand, Somavat et al. (2013) de-
monstrated that, for temperatures of 95 and 100 °C, low frequencies
presented greater effectiveness compared with high frequency and CH;
at 105 °C, OH showed better results than CH at both frequencies, and at
110 °C, there was no significant difference between the treatments. The
discrepancies between results for low and high frequencies will be
discussed further in section 4. Interestingly, in both studies, OH de-
monstrated higher effectiveness at reducing the microbial population in
most of the analysed temperatures. However, this difference tends to
decrease as the temperature increases. In both works, at the highest
temperatures, all treatments had statistically equal values of decimal
reduction time (D value).
Pereira et al. (2007) demonstrated that Bacillus licheniformis in-
activation was faster in OH at 70, 75 and 80 °C when compared with
CH. However, at 90 °C, no difference was detected, with decimal re-
duction times of 1.57 min for CH and 1.19 min for OH (p > 0.05).
Kim, Choi, et al. (2017) and Kim, Ryang, et al. (2017) evaluated

Table 3
Analysed ohmic heating parameters and research needs.
Parameter Effect Research needs References

Temperature Higher inactivation rates in certain conditions by Lack of data for fungi; comprehension of the extension of the (Cho et al., 1999; Schottroff et al.,
electroporation (in vegetative cells) or effect in the nonthermal effects depending on the different process variables, 2019; Uemura & Isobe, 2002)
cell core (bacteria spores). such as the microorganism and foodstuff.
Electric field Increase of the nonthermal effects in some Comprehension of the mechanisms of enhanced nonthermal (Baysal & Icier, 2010; Murashita,
situations; increase in the heat rate. effects and its interaction with the process variables, such as the Kawamura, & Koseki, 2017; Raso
microorganism and foodstuff. et al., 2016)
Frequency Increase of the nonthermal effects in some Comprehension of the frequency dependency of the inactivation (Somavat et al., 2012, 2013)
situations. dynamics, since some works have demonstrated higher
inactivation rates at low frequencies and others in high
frequencies.
Food composition Increase in heat rates due to alterations in the Comprehension of the effects of some constituents (as the soluble (Moura et al., 1999; Park et al.,
electric conductivity. solid content) in the electric conductivity, since they can increase 2017)
or decrease this parameter depending on the analysed condition.

654
W.A. Müller, et al.
Fig. 1. Proposed mechanism for nonthermal effects as a function of the process temperature. At lower temperatures, both thermal (protein denaturation) and
nonthermal effects (electroporation) are present. At higher temperatures, just the thermal effects are significant.
Table 4
Comparison of D values for E. coli inactivation by CH and OH in two different
culture media under different temperatures.
Reference/culture Temperature (°C) D value for CH D value for OH
medium (min) (min)
Pereira et al. (2007)/ 55 10.9 ± 1.8 14.2 ± 0.2
goat milk 63 3.9 ± 0.5 1.9
65 3.5 ± 0.2 0.86
Rodrigues et al. 57.5 14.46 ± 0.5 1.77 ± 0.18
(2018)/infant 60 0.72 ± 0.02 0.7 ± 0.05
formula 62.5 0.45 ± 0.06 0.41 ± 0.03
65 0.33 ± 0.01 0. 33 ± 0.01
different temperatures for Alicyclobacillus acidoterrestris spore inactiva-
tion at 25 Hz in apple juice; at the lowest temperatures (85 and 90 °C),
the D values obtained were statistically equal, whereas the micro-
organism inactivation was more effective at the highest temperatures
(95 and 100 °C) when OH was applied. Cho et al. (1999) studied Bacillus
subtilis inactivation by continuous and intermittent OH and CH: lower D
values were obtained at 88 and 92.3 °C in OH; the comparisons were
not performed at higher temperatures because the treatments were
performed under different conditions. In addition, the authors demon-
strated that the Tyndallization effect (i.e., additional inactivation rates
due to spore germination when the products have an additional stage of
cooling) is greater during OH processing. Moreover, Baysal and Icier
(2010) compared Alicyclobacillus acidoterrestris inactivation in orange
juices and found significant differences between the two heating
methods. Lower D values were obtained with OH processing at 30 V/cm
(58.48, 12.24 and 5.97 min for 70, 80 and 90 °C, respectively) when
compared to CH (83.33, 15.11 and 7.84 min for 70, 80 and 90 °C, re-
spectively).
Since the aforementioned studies analysed different temperature
ranges, a direct comparison between kinetic parameters was not pos-
sible. However, certain behaviour patterns are observed during the
application of OH on bacterial spores. The results currently found in the
literature suggest that, at higher temperatures, electrical effects cannot
be detected, as previously described for vegetative species. In addition,
similar behaviours may exist for sporulated cells at low temperatures.
Kim, Choi, et al. (2017) , Kim, Ryang, et al. (2017), Somavat et al.
(2012) and Somavat et al. (2013) found equal D values between OH and
CH at lower temperatures depending on the applied frequency. As the
spore structure is highly resistant to low temperatures, the inactivation
would occur slowly and similarly in both thermal processes. Based on
these results, there may be an optimum temperature in which the in-
activation rate difference between the two processes is the highest.
The morphological structures of spores and vegetative species are
essentially different, and the electroporation phenomenon is not a sa-
tisfactory explanation for the nonthermal effects in spores. Somavat
et al. (2012) and Somavat et al. (2013) proposed a different mechanism:
a synergistic effect between electricity and temperature, in which a
temperature rise causes an increase in the release of ionic compounds
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Trends in Food Science & Technology 99 (2020) 650–659
(such as calcium-dipicolinic acid (Ca-DPA) complex) from the cell nu-
cleus. According to Madigan et al. (2017), the DPA, which comprises
5–15% of the spores' dry weight, is one of the major factors responsible
for their thermal resistance. The combination of DPA and calcium,
forming a Ca-DPA complex, is directly related to the core dehydration,
which is characteristic of the sporulation process. The authors hy-
pothesize that the interaction of these compounds with the electric field
provokes a rise in the spores’ electric conductivity, making them more
susceptible to electric effects. As these structures are not present in
vegetative cells, these effects would not exist in such microorganisms.
To clarify the mechanism of nonthermal spore inactivation,
Schottroff et al. (2019) studied the inactivation of Bacillus subtilis en-
dospores, focusing on determining which components of the spore cell
were more affected by the electric field. The authors prepared three
mutant species lacking different components known to contribute to
spore heat resistance: (i) small-acid soluble proteins that protect the
DNA; (ii) the coat covering the spore; (iii) the spore germination en-
zyme SleB. Mutant inactivation was compared with the results obtained
for the wild-type microorganism (with all the constituents intact) sub-
mitted to CH and OH. The results showed that the electric field affects
the cell coat and SleB enzyme less than the cell core. This influence is
probably due to the increased release of proteins (mainly if they are not
firmly bound to DNA). Additionally, the authors demonstrated that the
DPA release from the core is similar in both CH and OH. As stated by
the authors, understanding the electrical effects on spores is a complex
issue that depends on sophisticated experimental design.
3.3. Aspects concerning spores and vegetative cells
One of the most relevant parameters in inactivation kinetics is the z
value, which represents the temperature difference needed to increase
or decrease the D value by 90%. This parameter was evaluated in both
thermal processes in the works by Pereira et al. (2007), Baysal and Icier
(2010), Somavat et al. (2012), Somavat et al. (2013) and Rodrigues
et al. (2018). ANOVA was conducted to evaluate the significant dif-
ferences between z values in OH and CH by Somavat et al. (2013) and
Baysal and Icier (2010), and no differences were observed. Somavat
et al. (2012) obtained z values for Geobacillus stearothermophilus spores
of 8.30 °C in OH at 10,000 Hz, 7.59 °C in OH at 60 Hz, and 7.42 °C in
CH; Pereira et al. (2007), working with Bacillus licheniformis spores,
found z values of 11.4 and 11.8 °C for CH and OH, respectively. It is
important to emphasize that these two works did not statistically ana-
lyse the z value. On the other hand, Rodrigues et al. (2018) obtained
considerably different values for both microorganisms used: the z va-
lues were 9.49 °C and 7.91 °C for Staphylococcus aureus and 10.13 °C
and 4.88 °C for Escherichia coli using ohmic and conventional heating,
respectively. In addition, Pereira et al. (2007) also found different va-
lues for this parameter studying Escherichia coli cells in goat milk (23.1
and 8.4 °C for CH and OH, respectively). A possible explanation for the
difference among the studies is associated with the fact that Baysal and
Icier (2010), Somavat et al. (2012) and Somavat et al. (2013) worked
W.A. Müller, et al.
with spores, while Rodrigues et al. (2018) worked with vegetative
species. Pereira et al. (2007) worked with vegetative and spore species
and demonstrated different z values just for the vegetative species.
Based on these results, vegetative microorganisms might suffer sig-
nificant alterations in the z value when submitted to OH compared with
spores, which influences this parameter to a lesser degree. It is im-
portant to point out that this is just a hypothesis and requires future
research for validation.
In addition, it must be stated that the comparisons performed in the
present work were isothermal, since only papers that equalized the
temperature profiles were considered. However, a comparison of mi-
crobial inactivation during the heating ramp (time until the food
reaches the analysed temperature) is also important, as observed by
Somavat et al. (2013) and Won et al. (2002). Their results have shown
that OH inactivates a higher number of cells during this process. This
fact should be considered an additional advantage of the OH process.
4. Frequency effects
Concerning the frequency effects during OH, as previously discussed
in subsection 3.2, the works of Somavat et al. (2012) and Somavat et al.
(2013) have shown divergent D values. Somavat et al. (2012) showed
better results for high frequency OH, whereas Somavat et al. (2013)
found lower D values for low frequencies. Lee, Ryu, and Kang (2013)
also studied frequency effects and observed a gradual decrease in pro-
cessing time as the frequency increased from 60 to 500 Hz; no con-
siderable differences were observed between 500 Hz and 20 kHz. Mi-
crobiological effects aside, the authors pointed out that the use of high
frequency during OH tends to reduce the corrosion of electrodes. Won
et al. (2002) demonstrated that the amount of intracellular material
exuded by Saccharomyces cerevisiae cells was higher at the highest fre-
quency. Moreover, Murashita, Kawamura, and Koseki (2017) and Kim,
Choi, and Kang (2017) did not find significant differences between
frequencies in the kinetic parameters for bacterial species. However,
Kim, Choi, et al. (2017) demonstrated that at lower frequencies, the
number of sub-lethally injured cells decreased, and the MS-2 bacter-
iophage inactivation increased.
Somavat et al. (2013) explained the ambiguous results concerning
the frequency effects obtained by different authors by stating that some
microbial intracellular compounds can be impacted differently due to
changes in the electric field oscillation. The extent of this effect is de-
pendent on the species morphology. The high inactivation rates ob-
served at low frequencies have already been discussed by different
authors (Kim, Choi, & Kang, 2017; Lakkakula, Lima, & Walker, 2004;
Lima & Sastry, 1999). They proposed that at low frequencies, the
transmembrane potential is less oscillatory, extending the time for in-
tracellular ions to conform to the electric field. Thus, the number of ions
joined at the inner cell wall is higher, increasing the nonthermal effect.
On the other hand, at high frequencies, the inactivation mechanisms
remain unclear. Since the field oscillates more times per second, a
greater number of collisions between the ions and membrane walls may
occur, which could cause more cell damage. It is important to empha-
size that the suggested mechanism lacks experimental data for ver-
ification. The preponderance of these low or high frequency effects
depends on the microorganism morphology (for example, its ionic
content) and on the characteristics of the analysed food, as previously
stated by Somavat et al. (2013).
5. Electric field effects
The effects of the electric field on the inactivation rate can be par-
tially explained using the mathematical definition of heat generation by
OH:
Q= . E2 (1)
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Trends in Food Science & Technology 99 (2020) 650–659
where Q is the volumetric rate of heat generation (W.m−3), is the
electric conductivity (S.m−1) and E is the applied electric field
(V.m−1). The heat generation is proportional to the square of the
electric field, which explains why foodstuffs heat faster under high
electric fields, decreasing processing time. Moreover, the aforemen-
tioned nonthermal effects tend to increase considerably as the applied
electric field increases.
Sagong, Park, Choi, Ryu, and Kang (2011) showed that the pro-
cessing time for a 5D reduction diminished approximately 75% when
the applied field was two-fold higher (from 10 to 20 V/cm). Park, Ha,
and Kang (2017) demonstrated that none of the analysed species could
resist more than 30 s of OH with an electric field of 60 V/cm; when a
30 V/cm field was applied, a high number of viable cells was observed
even after 60 s of processing. On the other hand, the same authors
stated that the conversion of electricity into thermal energy within the
food product was higher when an electric field of 30 V/cm was used in
comparison with 60 V/cm. This can be a positive economic factor
concerning the utilization of low electric fields. Several authors have
compared the effects of using high and low electric fields on micro-
organism inactivation. Won et al. (2002), Uemura and Isobe (2002),
Yildiz and Baysal (2006), Kim, Park, and Kang (2018), Hashemi,
Gholamhosseinpour, and Niakousari (2019) and Hashemi and Roohi
(2019) found significant reductions in viable cells at higher electric
fields; this behaviour was also observed by Shao et al. (2019). More-
over, the latter authors showed that the recovery of injured cells is
slower at higher voltages. The lag phase duration showed a rise of 75%
when the electric field was applied.
Mok, Pyatkovskyy, Yousef, and Sastry (2019) evaluated the com-
bination of an electric field with shear stress using rotating electrodes
and found a positive synergistic effect. The greater the electric field and
shear rate, the lower the inactivation time for a 5-log reduction.
Moreover, Hashemi, Gholamhosseinpour, et al. (2019) and Hashemi,
Mahmoudi, et al. (2019) demonstrated that an increase in the electric
current had a significant impact on reducing microbial species. This
effect was higher for Zygosaccharomyces rouxii than for the bacterial and
fungal species analysed, which may suggest that yeasts are more sus-
ceptible to electric effects. All the aforementioned works confirm the
positive relationship between electric field and inactivation rates.
However, these studies did not clarify if the temperature profiles were
matched for the electric field analysis; therefore, their results cannot
explain the nonthermal effects of OH.
Baysal and Icier (2010) and Murashita et al. (2017) were able to
analyse additional nonthermal effects by matching the temperature
profiles. The former authors studied OH at 30, 40 and 50 V/cm and
observed equal inactivation rates for all applied electric fields at 80 °C.
At 70 °C, all treatments were different, with lower D values for higher
electric fields, decreasing the processing time by 51% when 30 V/cm
was compared to CH. Finally, at 90 °C, only the 50 V/cm field was
different from the others, presenting the lowest D value. The smaller
differences observed at higher temperatures were justified by the pre-
dominance of thermal over electrical effects. Murashita et al. (2017)
studied the nonthermal effects at 101 °C and found significant differ-
ences between OH and CH only in the highest electric field considered
(20 V/cm); at the lower electric fields (5 and 10 V/cm), no significant
differences were observed.
6. Composition effects
In this subsection, the effects of food composition (pH, fat content,
salt content and solid soluble content) on microbial inactivation rate
during OH are discussed. Three different pH values were analysed by
Lee et al. (2015) during OH: 2.5, 3.5 and 4.5. The scenario with a more
acidic pH (2.5) had a greater inactivation rate compared with the
others; scenarios in which the pH values were 3.5 and 4.5 showed si-
milar values (ANOVA was not performed). The additional effect
W.A. Müller, et al.
observed in the lowest pH may not have been related to the electric
field, but rather to the hostility of such environments to bacterial spe-
cies. Similar results were found by Tola and Ramaswamy (2014), in
which increases in pH resulted in higher D values. The authors de-
monstrated that, at high temperatures, these effects were less pro-
nounced, and the thermal effects were predominant. Combinations
between OH and acidic pH can be potentially interesting for food
processing, but further research is needed concerning their application
as hurdle technologies. Raso and Barbosa-Cánovas (2003) demon-
strated that the combination of pulsed electric fields and low pH values
did not present synergistic effects (i.e., an appreciable interaction be-
tween the two variables that could result in higher inactivation rates).
Kim and Kang (2015b) considered the influence of fat content in the
heating process and found that, during CH, alterations in this parameter
did not influence the heating rate. During OH, on the other hand, an
increase in the fat content resulted in lower heating rates. According to
Equation (1), the heat generation rate is directly proportional to the
sample electric conductivity, which decreases with fat content. The
influence of this constituent on the electrical conductivity was studied
by Ramaswamy et al. (2014). The authors proposed that the fat globule
can be immersed in a zone with a high number of ions; in such a case,
the electrical current can bypass the fat molecule due to preferential
flow through the ions. Microorganisms present inside the fat globules
can be at lower temperatures in comparison with the rest of the pro-
duct, presenting a significant risk to the consumer.
Kim et al. (1996) analysed changes in electric conductivity by al-
tering the salt content of meatballs. They found that an increase from
1.2 to 1.8 S/m led to a two-fold higher lethality at the centre of the
meatball. Park et al. (2017) observed that the electric conductivity
decreased as the product's soluble solid content increased. The authors
showed that the highest analysed solid content (72°Brix) presented the
smallest heating rate and, consequently, less bacterial inactivation for a
given condition. However, the influence of the soluble solid content was
dependent on the particle size and the selected food media. Depending
on these variables, the effect can be different or even opposite
(Ramaswamy et al., 2014). An illustrative example of such behaviour
can be seen in the study of Moura, Vitali, and Hubinger (1999), which
analysed three fruit juices (pineapple, lemon and tangerine). The au-
thors demonstrated that an increase in the soluble solid content up to
30°Brix increased the electric conductivity; at values higher than
30°Brix, nevertheless, the effect was opposite (the electric conductivity
decreased).
7. Conclusions
The literature analysis showed that, concerning all articles dealing
with microbiological inactivation by ohmic heating, temperature was
the most analysed variable, E. coli was the most studied microorganism
and juices were the most analysed food media.
Concerning the comparison between CH and OH, when temperature
profiles were matched, it was possible to observe nonthermal effects in
certain temperature ranges. It is worth noting that, even in the absence
of nonthermal effects, the use of OH has some additional advantages,
such as a shorter heating time and smaller temperature gradients due to
the volumetric energy generation. The effects of high and low fre-
quencies during microbial inactivation by OH are still not agreed upon
in the literature and should be further investigated. Considering the
cited works, an increase in the electric field showed favourable results,
whereas an increase in fat and solid content, as well as pH, showed
negative results for microbial inactivation.
Based on these recent findings, it can be concluded that more stu-
dies concerning microbial inactivation during ohmic heating are of
extreme importance. The studies should focus on determining the in-
fluence of significant parameters and on helping to elucidate the mi-
crobial death dynamics. The importance of temperature profile equal-
ization to determine the real extent of nonthermal effects should be
657
Trends in Food Science & Technology 99 (2020) 650–659
emphasized.
Acknowledgments
The authors are grateful to the Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) for providing funds for this research.
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