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Efficiency of novel processing technologies for the control of Listeria monocytogenes in food products
Journal Pre-proof Efficiency of non-conventional processing technologies for the control of Listeria monocytogenes in food products Akbar Bahrami, Zahra Moaddabdoost Baboli, Keith Schimmel, Leonard Williams, Seid Mahdi Jafari PII:
S0924-2244(19)30392-9
DOI:
https://doi.org/10.1016/j.tifs.2019.12.009
Reference:
TIFS 2680
To appear in:
Trends in Food Science & Technology
Received Date: 17 May 2019 Revised Date:
23 October 2019
Accepted Date: 9 December 2019
Please cite this article as: Bahrami, A., Baboli, Z.M., Schimmel, K., Williams, L., Jafari, S.M., Efficiency of non-conventional processing technologies for the control of Listeria monocytogenes in food products, Trends in Food Science & Technology (2020), doi: https://doi.org/10.1016/j.tifs.2019.12.009. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.
The most studied novel processing technologies to control Listeria monocytogenes in foods
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Efficiency of non-conventional processing technologies for the control of Listeria
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monocytogenes in food products
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Running title: Control of L. monocytogenes in food products
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Akbar Bahrami1, Zahra Moaddabdoost Baboli1, Keith Schimmel2, Leonard Williams3*, Seid
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Mahdi Jafari4*
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1
Program of Applied Science and Technology, Center for Excellence in Post-Harvest Technologies, North
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Carolina Agricultural and Technical State University, North Carolina Research Campus, Kannapolis, NC
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28081, USA
9
2
10 11
1601 East Market Street, Greensboro, NC 27411, USA 3
12 13 14
Program of Applied Science and Technology, North Carolina Agricultural and Technical State University,
Center for Excellence in Post-Harvest Technologies, North Carolina Agricultural and Technical State University, North Carolina Research Campus, Kannapolis, NC 28081, USA
4
Department of Food Materials and Process Design Engineering, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
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*Corresponding authors: L. Williams, Tel (704) 250-5700, Email: [email protected];
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S.M. Jafari, Tel./fax: +98 17 32426432, Email: [email protected]
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Abstract
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Background: Commercial heat sterilization has been used in the food industry for decades to produce safe
19
foods. However, this technology can have potential detrimental effects on the organoleptic and nutritional
20
quality of foods; so numerous innovative technologies have been developed to destroy pathogens potentially
21
present in foods as well as maintaining the sensory properties. Among pathogenic bacteria, L.
22
monocytogenes is of great importance for optimization of advanced technologies.
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Scope and approach: It is estimated that L. monocytogenes alone is globally responsible for 23,150
24
sicknesses and 5463 deaths per year and its inactivation is vital for ensuring microbiologically safe food
25
products. In addition, its high resistance to most processes, compared to other pathogenic bacteria has made
26
L. monocytogenes to be one of good indicators for examining the efficiency of food processing technologies.
27
This review focuses on the efficiency of mild food processing technologies and their antimicrobial
28
mechanisms to inactivate L. monocytogenes.
29
Key findings and conclusions: Non-conventional technologies of high hydrostatic pressure, ultrasound, and
30
microwave can be considered as efficient as commercial sterilization methods in destroying L.
31
monocytogenes and potentially other foodborne pathogens. The composition and characteristics of foods,
32
processing conditions, and the resistance of L. monocytogenes (in species level) against the processing are
33
among diverse determining factors affecting the efficiency of these advanced processes. This study provides
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a comprehensive summary on efficiency of newer technologies to conventional heating which could be
35
helpful for industries as well as researchers to select the best applicable treatment for food product.
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Keywords: Food processing; Listeria monocytogenes; Pathogenic bacteria; Food safety; New processes. 1
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1. Introduction
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L. monocytogenes, the cause of listeriosis, is an important pathogen having a mortality rate of up
39
to 30%, is a Gram positive psychrotrophic bacterium which is the only pathogenic species for
40
human among six species belonging to Listeria spp. (Benlloch-Tinoco, Pina-Perez et al. 2014). The
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gastroenteritis, meningitis, and septicemia have reported as the main clinical manifestation of L.
42
monocytogenes. Tracking associated outbreaks to L. monocytogenes and its shown capacity to resist
43
harsh processing conditions such as high and cold temperatures, modified atmosphere, and even
44
establishment in food processing environments, indicates potential continuous contamination of
45
foods by L. monocytogenes during processing and post-processing (Magalhães, Ferreira et al. 2016).
46
Conventional thermal processing has been used for a long time to provide stable and safe food
47
products. However, from researcher’s perspective, conventional thermal treatments are not
48
considered as the preferred solution anymore, mainly due to their significant impact on the loss of
49
sensory and nutritious quality of final foods. In this regard, food products that contain chemical
50
preservatives are rejected by consumers as well.
51
This approach has resulted in the introduction of new decontamination processing methods such
52
as high-hydrostatic pressure, sonication, microwave, irradiation, ohmic heating, ozonation, pulsed
53
electric fields, and cold plasma. These technologies not only have presented the capacity to meet the
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requirements of commercial sterilization techniques to be used in food processing, they may also
55
efficiently bring the merit of keeping the nutritional and sensorial properties of food products better
56
than conventional thermal processing. L. monocytogenes was selected as the focus of this study to
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assess the efficacy of new food processing technologies due to its high resistance to food processing
58
(compared with other pathogenic bacteria) and its high virulence capacity based on a
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comprehensive literature review and database research (Pilevar, Hosseini et al. 2019). For example,
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according to many studies and researches for food outbreaks, related to pathogenic bacteria hazards,
61
and their resistance level against pasteurization in milk products, L. monocytogenes, has been
62
selected and declared as the target pathogen to be controlled in the sterilization process of several 2
63
dairy foods (EuropeanCommission 2016, Ukuku, Onwulata et al. 2017, Schottroff, Gratz et al.
64
2019). Similarly, L. monocytogenes was declared as one of main target microorganisms for the
65
microbiological safety of cooked ready to eat meat products (Teixeira, Repkova et al. 2018).
66
Therefore, due to such considerations, outlooks, and because of the generally higher resistant level
67
of Gram positive bacteria to sterilization processing, inactivation of L. monocytogenes in food
68
products through different advanced technologies was studied. The successful inactivation of L.
69
monocytogenes by employing any new method can indicate its high potential in inactivation of all
70
other pathogenic bacteria. This review provides essential information on comparing the efficiency
71
of non-conventional food processing methods and presents a comprehensive source for food
72
industries to select the best applicable method for their specific product.
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2. Conventional thermal treatment to reduce L. monocytogenes in foods
74
Thermal processing as a principal and traditional method for inactivation of microorganisms is
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still the most common treatment for pasteurization and elimination of foodborne pathogens as well
76
as spoilage microorganisms in food products. But heat can adversely affect the quality of food and
77
degrade the nutritional value of the product (Tafti, Peighambardoust et al. 2013, Tafti, Peighardoust
78
et al. 2013). Moreover, mild thermal processing can sub-lethally injure the bacteria, which may
79
allow them to recover and grow during storage. This is the main concern to the safety of thermal
80
processed food (Wang, Uyttendaele et al. 2016). The time needed to reduce the microbial
81
concentration by one log is known as D-value, which shows the thermal resistance of bacteria and it
82
can be derived from bacteria survival curve during treatment. That is because log-linear method has
83
been considered as the easiest method for fitting and predicting the microorganism behavior under
84
thermal treatment (Dufort, Sogin et al. 2017, Wang, Devlieghere et al. 2017, Taylor, Tsai et al.
85
2018), although log-linear always is not the best fit (Rachon, Penaloza et al. 2016).
86
Shell and tube or plate heat exchangers, hot water bath, and direct hot steam/air are usually used
87
for thermal processes (Taylor, Tsai et al. 2018). In conventional thermal treating, heat transfers into
88
the product via convection and conduction, therefore, there is a time lag, called come-up time, for 3
89
products to reach the target temperature (Delgado Suárez, Chairéz Espinosa et al. 2015, Rachon,
90
Penaloza et al. 2016). The come-up time depends on the heating rate and heat transfer
91
characteristics of products (Jafari, Jabari et al. 2017, Jafari, Saramnejad et al. 2018). The difference
92
between temperature set-point and actual temperature of the products can be the main reason for
93
failure of microbial inactivation by mild heat treatment (Benlloch-Tinoco, Igual et al. 2015).
94
Table 1 presents a summary of recent studies on applying conventional heat treatment for
95
inactivating Listeria spp. As for modeling the survival curves, Rachon, Penaloza et al. (2016)
96
indicated that at higher temperatures, the microbial curves showed non-linearity especially when
97
come-up time can cause microbial inactivation. In their study, Weibull model was considered as an
98
appropriate fitting. The works conducted on wheat (Taylor, Tsai et al. 2018) and tomato puree
99
(Dufort, Sogin et al. 2017) at lower temperatures, showed that log-linear model can provide a
100
precise fitting. However, Wang, Devlieghere et al. (2017) mentioned that when inactivation curves
101
were obtained from non-selective media, inactivation curve depicted a shoulder, which indicated the
102
nonlinearity of the curve. [Table 1]
103 104
L. monocytogenes has adaptation ability to the environmental stresses which can enhance its
105
resistance to heat treatment (Aryani, den Besten et al. 2015). Decreasing water activity (Taylor, Tsai
106
et al. 2018), increasing salt content (Poimenidou, Chatzithoma et al. 2016, Wang, Uyttendaele et al.
107
2016, Li, Huang et al. 2017), decreasing fat and fiber content (Mate, Periago et al. 2017), higher
108
acidity (Aryani, den Besten et al. 2015, Dufort, Sogin et al. 2017) can enhance the heat resistance of
109
L. monocytogenes due to adaptive response to stress and starvation and result in cross protection
110
(Aryani, den Besten et al. 2015, Poimenidou, Chatzithoma et al. 2016). Increase in heat tolerance of
111
L. monocytogenes was related to upregulation of genes and their recovery levels (Omori, Miake et
112
al. 2017). Omori, Miake et al. (2017) suggested ClpE, ClpB as genes associated with enhanced heat
113
resistance of some L. monocytogenes strains while Pontinen, Aalto-Araneda et al. (2017) mentioned
114
ClpL as a potential predictor for that purpose. 4
115
As for different strains, Aryani, den Besten et al. (2015) determined that among 20 different
116
strains of L. monocytogenes, isolated from different sources, the most thermal resistant strain had a
117
D60 = 4.1 in the range of 55-65 °C and also indicated that for all strains, cells in exponential phase
118
were much less heat resistant compared to stationary phase. Meanwhile, some other studies have
119
shown that the heat tolerance of strains is dependent on the heating temperature (Monu, Valladares
120
et al. 2015, Li, Huang et al. 2017). Monu, Valladares et al. (2015) showed that among five strains of
121
L. monocytogenes studied in their work, L. monocytogenes Scott A presented the lowest D value at
122
lower temperatures, 56°C (D56 = 2.69), and the highest D value, at higher temperature of 60 °C (D60
123
= 0.66) was obtained for this strain. Investigating on the sub-lethal effect of thermal inactivation,
124
Wang, Devlieghere et al. (2017) demonstrated that the portion of sub-lethal injury was increased at
125
higher temperatures and times, and also the cells treated on agar surface were more resistant that
126
those in broth.
127 128
3. New strategies to control the growth of L. monocytogenes in food products To enhance the safety and shelf-life of food products, the use of non-thermal treatments that
129
do not increase the temperature of food products for bacterial inactivation, instead other
130
mechanisms are engaged, is receiving attention. These technologies are applied mainly to reduce
131
the total microbial population, and to destroy pathogenic bacteria such as L. monocytogenes
132
potentially present in food products. The non-thermal strategies can be used before packaging or in
133
post packaging step based on the nature of technology. Although the use of these technologies do
134
not involve heating of foods, they should have the capacity to provide lethality of the target
135
microbes, as well as preserving sensory properties, nutritional, and functional characteristics of food
136
products (Mahdi Jafari, Masoudi et al. 2019, Pilevar, Bahrami et al. 2019). The mechanism of
137
microbial inactivation of newer processing technologies is presented in Fig. 1. For applying
138
optimum conditions of a specific processing technology in terms of safety and quality of foods,
139
diverse parameters should be countered (Fig. 2) which will be covered throughout the manuscript.
140
Such treatments should not have negative impacts on the barrier features of the packaging if they 5
141
are used in post-packaging step. However, the possibility of commercial use of a post-packaging
142
decontamination technology, beside its effectiveness also depends greatly on its installation and
143
maintenances costs. In the following subsections, these non-conventional technologies and their
144
influence on L. monocytogenes will be discussed.
145
Fig. 1
146
Fig. 2
147
3.1.
High Hydrostatic Pressure (HHP) processing
148
The variations in the pressure (a thermodynamic property of physical systems such as
149
biological systems), can be associated with the lower degree of negative effects in use of other
150
property, temperature, which has been commonly used. That was shown that by controlling
151
pressure, we can induce significant impacts on diverse systems. The major and progressively
152
increasing use of HPP in food industries, has been its application as the non-thermal pasteurization
153
of food products, which can enhance the shelf-life of foods, without imposing significant
154
modification in their nutritional, functional and sensory characteristics as it is applied at room
155
temperatures (Zhao, Zhang et al. 2017). HHP processing is performed through applying pressures
156
above 100 MPa to the product through mechanically pressurized liquids, usually water. The
157
behavior of food product changes based on the Le Chatelier’s principle as applying pressure causes
158
a shift in the system equilibrium toward occupying smallest volumes, and in microscopic scale, at
159
constant temperature, it increases the degree of ordering molecules of a given substance. In
160
addition, the pressure is exerted instantly and uniformly throughout the product independent of its
161
size and geometry (Zacconi, Giosue et al. 2015).
162
Effects of HHP on inactivating L. monocytogenes depends on the processing parameters such as
163
applied pressure (Huang, Lung et al. 2015, Zacconi, Giosue et al. 2015, Mukhopadhyay, Sokorai et
164
al. 2016, Kaur and Rao 2017, Liu, Li et al. 2017), temperature (Pinho, Oliveira et al. 2015, Ates,
165
Rode et al. 2016, Mukhopadhyay, Sokorai et al. 2016) and holding time (Mukhopadhyay, Sokorai
166
et al. 2016, Liu, Li et al. 2017, Alcantara-Zayala, Serment-Moreno et al. 2018), composition and 6
167
properties of the matrix such as pH and water activity (Bover-Cid, Belletti et al. 2015, Stratakos,
168
Linton et al. 2016, Rubio, Possas et al. 2018) and the sensitivity of L. monocytogenes strain (Evert-
169
Arriagada, Trujillo et al. 2018). The mechanism of microbial inactivation by HHP consists of
170
unfolding the protein structure, denaturing cell membrane, changing the fluidity in cell membrane,
171
loss of intracellular pH and membrane integrity, and eventually cell disruption. Pressure also causes
172
dissociation of the microorganism ribosomes and limits cell viability (Georget, Sevenich et al. 2015,
173
Lung, Cheng et al. 2015). Depending on the conditions, HHP might not always lead to cell death
174
and may just sub-lethally damage it. Therefore, during storage period, bacteria may repair the
175
injuries and get recovered, especially if the treatment was not severe enough or the storage went
176
under abuse temperature (Li and Ganzle 2016, Lebow, DesRocher et al. 2017, Balamurugan,
177
Inmanee et al. 2018, Misiou, van Nassau et al. 2018).
178
Table 2 provides a summary of studies conducted on inactivation of L. monocytogenes by
179
HHP in different products with or without any additives from 2015 to 2018. In general, HHP is
180
more successful in culture media and liquid foods than solid ones (Bover-Cid, Belletti et al. 2015);
181
under pressures more than 600 MPa and temperatures higher than 40 °C, the rate of sub-lethal
182
damages decreases to more lethal ones (Ates, Rode et al. 2017). The sub-lethal injury has been
183
determined by comparing the difference in viable count of L. monocytogenes population on
184
selective and non-selective media (Ates, Rode et al. 2016, Balamurugan, Inmanee et al. 2018). The
185
cell morphology analysis of L. monocytogenes depicted that HHP caused external changes to
186
cellular structures (Huang, Lung et al. 2015, Liu, Li et al. 2017) and fluorescence micrograph
187
indicated the membrane damage as well as intercellular release especially at pressures higher than
188
400 MPa (Huang, Lung et al. 2015, Scolari, Zacconi et al. 2015). However, HHP might not
189
consistently satisfy in meeting FDA requirement for 5-log reduction of pathogenic bacteria,
190
especially in ready to eat products; so combining other hurdles for microbial growth can assure
191
sufficient reduction and extend the shelf-life. For example, increasing temperature and addition of
192
natural antimicrobials are some of those hurdles (Ahmed, Mulla et al. 2017, Lebow, DesRocher et 7
193
al. 2017, Liu, Li et al. 2017, Castro, Silva et al. 2018, Misiou, van Nassau et al. 2018, Teixeira,
194
Repkova et al. 2018).
195
[Table 2]
196
In products such as smoothie (Scolari, Zacconi et al. 2015, Ates, Rode et al. 2016), fruit
197
puree (Blazquez, Burgos et al. 2017), milk (Huang, Lung et al. 2015, Liu, Li et al. 2017, Misiou,
198
van Nassau et al. 2018), cantaloupe puree (Mukhopadhyay, Sokorai et al. 2016), and soup (Ates,
199
Rode et al. 2016), application of 300-500 MPa for 5 min resulted in a 5-log reduction in population
200
of Listeria spp. in water or buffer solution (Pyatkovskyy, Shynkaryk et al. 2018). However, for
201
chorizo sausage (Rubio, Possas et al. 2018), shrimp (Kaur and Rao 2017), and salmon products
202
(Lebow, DesRocher et al. 2017, Misiou, van Nassau et al. 2018), even pressures higher than 500
203
MPa or longer holding times did not cause sufficient bacterial reduction.
204
In some cases, although the initial reduction in number of L. monocytogenes right after
205
treatment were 5-log or more, during storage a number of surviving cell grew and their count
206
reached to higher than the acceptance limit, in some products such as milk (Liu, Li et al. 2017,
207
Misiou, van Nassau et al. 2018), cheese (Evert-Arriagada, Trujillo et al. 2018), cooked sausage
208
(Balamurugan, Inmanee et al. 2018), and cured meat (Valdramidis, Patterson et al. 2015), which
209
indicated a high number of cells were sub-lethally damaged than being completely inactivated.
210
3.2.
Ultrasound processing
211
Ultrasound technology which is composed of sound waves with frequency beyond the limit
212
of human hearing (20 kHz), due to being relatively cheap, simple and energy saving, is introduced
213
as an emerging technology for processing food products. Ultrasound is being progressively applied
214
in diverse processes such as homogenization, emulsification, extraction, crystallization, cutting,
215
hydrolysis, and microbial inactivation. For example, while, low power ultrasound can be used for
216
physicochemical characterization of food ingredients, high power ultrasound through cavitation can
217
induce diverse physical and chemical/ biochemical changes during food processing. In most cases,
218
the ultrasonic source consists essentially of a plane surface oscillating with simple harmonic motion 8
219
at a single frequency, like a piston in the cylinder of an engine but at a much smaller amplitude and
220
at much higher frequency (Jamalabadi, Saremnezhad et al. , Anese, Maifreni et al. 2015, Gabriel
221
2015). Ultrasound treatments can be classified by their frequency ranges to power ultrasound (16-
222
100 kHz), high-frequency ultrasound (100 kHz -1 MHz), and diagnostic ultrasound (1-10 MHz)
223
(Luo and Oh 2016, Ozcan and Demirel Zorba 2016).
224
The mechanism of ultrasound in inactivation of microorganism is associated with a
225
phenomena called cavitation (Gabriel 2014, Hamann, Tonkiel et al. 2018) , which means formation,
226
growth, and collapse of microbubbles within an aqueous solution (Jamalabadi, Saremnezhad et al.).
227
Over a number of acoustic cycles, the bubbles grow until they reach a critical size, where the
228
ultrasonic energy fails to retain the increasing vapor phase in the bubble; so bubbles become
229
unstable and collapse violently results in creating shock waves with a huge amount of energy
230
(Gabriel 2014). Cavitation can cause severe damage to the cell walls, pit on their surface, erode
231
them and result in microbial inactivation. Under the localized extreme temperature conditions
232
generated by cavitation, the water molecules dissociate to free radicals including hydroxyl and
233
hydrogen. The free radicals may cause DNA damage, disrupt enzymatic activity and damage
234
liposomes and cell membrane by disrupting the structural and functional components up to cell lysis
235
(Gabriel 2014). The radicals formed in this reaction are also highly reactive and responsible for a
236
chemical reaction by ultrasonic irradiation (Anese, Maifreni et al. 2015). During the high-frequency
237
sonication, the number of cavitation events is more, compared to low-frequency, but with smaller
238
bubbles, so the micro-stream has not enough energy for the physical force but the total energy
239
release is sufficient to break the chemical bonds of water molecules (Lee, Kim et al. 2014, Franco-
240
Vega, Ramirez-Corona et al. 2015).
241
The lethal effect of ultrasound depends on the applied power per volume, frequency,
242
treatment time, temperature and geometry of reactor. Table 3 represents a summary of applying
243
ultrasound for inactivating L. monocytogenes in different food products. In general, based on
244
several studies, ultrasound was not successful to inactivate L. monocytogenes sufficiently unless 9
245
under mild temperatures (> 60 °C) (Anese, Maifreni et al. 2015, Franco-Vega, Ramirez-Corona et
246
al. 2015, Gabriel 2015) or by adding additives (Wu and Narsimhan 2017, Dolan, Bastarrachea et al.
247
2018). The efficiency of ultrasound on inactivation of L. monocytogenes is engaged with the
248
cavitation rate, so it is more effective in liquid media, such as juices (Gabriel 2014), broth (Franco-
249
Vega, Ramirez-Corona et al. 2015, Dolan, Bastarrachea et al. 2018), or milk (Gabriel 2015) , but it
250
has a limitation for pre-packaged foods. Moreover, since cavitation happens at a high-pressure zone,
251
the geometry and volume of reactor play important roles.
252
[Table 3]
253
As Table 3 shows, recently researchers are focusing on potential of ultrasound for
254
decontamination of fresh or ready-to-eat products. In the studies on disinfecting lettuce or the water
255
for removing Listeria spp. through use of bath ultrasound reactor, sonication could not inactivate
256
the microbial content more than 2.5 logs (Lee, Kim et al. 2014), even in the present of additives
257
such as peroxyacetic acid (Gómez-López, Gil et al. 2015) or Tween-20 and sodium dodecyl sulfate
258
(SDS) (Huang, Wrenn et al. 2018). Only Anese, Maifreni et al. (2015) showed that under
259
uncontrolled continuous sonication, L. monocytogenes count in wastewater of fresh-cut lettuce
260
reduced by 5-log for samples treated for 5 min. In this study, the temperature increased
261
continuously and reached to 60° after 5 min.
262
Although the effect of additives such as cinnamon oil (Ozcan and Demirel Zorba 2016,
263
Park, Kang et al. 2018), SDS, peroxyacetic acid, or benzalkonium chloride did not improve the
264
lethal effect of ultrasound on L. monocytogenes, peracetic acid (Hamann, Tonkiel et al. 2018),
265
antimicrobial peptide (Wu and Narsimhan 2017), or zinc oxide (Dolan, Bastarrachea et al. 2018)
266
had sufficient synergic effects with ultrasound depending on the concentration used.
267
Although ultrasound has shown capacity to bring beneficial modifications in different
268
aspects including pasteurization, the physicochemical impacts of ultrasound processing might also
269
cause food quality problems by making off-flavors, variations in physical parameters and
270
decomposition of compounds. For example, cavitation can produce radicals in liquid mediums that 10
271
can be cause of initiating the degradation of products as well trigger the radical chain reactions and
272
make significant quality defects in food products (Pingret, Fabiano-Tixier et al. 2013).
273
3.3.
Microwave heating
274
Microwave heating has shown a widespread application in the food sector such as cooking,
275
drying, pasteurization and preservation of food compounds. Microwave affects the dipolar and ionic
276
components of foods by exposing to oscillating electric field at frequencies of 915 or 2450 MHz
277
(Sung and Kang 2014, Benlloch-Tinoco, Igual et al. 2015). Microwave is providing several
278
advantages such as rapid heating rate (Siguemoto, Gut et al. 2018), faster heat penetration, energy
279
savings (due to volumetric heating) and reduced processing cost and time. Microwave sterilization
280
can effectively reduce the potential pathogens counts in foods, as well can inactivate the enzyme,
281
thus, preserves the nutritional properties of foods (Chen, Li et al. 2017). There are some studies
282
emphasizing on non-thermal effects of microwave radiation as well (Kim, Park et al. 2018). Despite
283
those advantages, there is a major problem with microwave heating which is related to the non-
284
uniform heat distribution as it affects microbiological safety (Kim, Sung et al. 2016). Hamoud-
285
Agha, Curet et al. (2014) conducted numerical investigation on 915 MHz microwave heating by
286
applying finite element methods and showed the surface layers of products loss heat due to
287
convection to the surrounding environment. Therefore, microwave heating leaves cold spots and hot
288
spots on the products. Kim, Sung et al. (2016) showed that the side temperature of tomato paste can
289
be 37-43°C, while the center has the temperature of 80 °C. In addition, microwave heating like
290
conventional heating can result in moisture loss. However, the solid-state power sources as a viable
291
alternative to magnetrons have shown a capacity for decreasing the problem of cold spots (Atuonwu
292
and Tassou 2018).
293
In general, the microbial inactivation efficiency of microwave heating depends on the
294
applied power, frequency of electric field, treatment time, as well as geometry and dielectric
295
properties of the product. Unfortunately, the number of studies on this subject is limited. Table 4
296
provides a summary of studies on microwave heating for inactivation of L. monocytogenes. By 11
297
using domestic microwave ovens with frequency of 2450 MHz, a 5-log microbial reduction was
298
met at high powers, 900-1100 W, after 75 s for Frankfurter sausage, 82 s for kiwi puree, 50 s for
299
chicken meat (Zeinali, Jamshidi et al. 2015), 120 s for chicory stem (Renna, Gonnella et al. 2017),
300
and 130 s for apple juice (Siguemoto, Gut et al. 2018). Microwave devices with a lower frequency,
301
915 KHz, are mainly used for industrial equipment (Sung and Kang 2014) and need power more
302
than 1500 W for sufficient microbial inactivation (Sung and Kang 2014, Kim, Park et al. 2018).
303
[Table 4]
304
Salt, sugar and moisture content affect the dielectric properties of the product and in turn,
305
affect the microwave heating efficiency. Song and Kang (2016) showed that water activity had a
306
direct influence on the reduction of L. monocytogenes and Kim, Park et al. (2018) demonstrated that
307
that lower sugar content of chili sauce can reduce the treatment time.
308
The geometry of product is also important since microwave heating concentrates more around the
309
geometric center of products, so it might leave focused effects on products (especially for round
310
shape foods) and make damages on the texture or quality of foods (Song and Kang 2016). That is
311
why there is a controversial dispute over the favorable effects of microwave on quality properties of
312
foods. Therefore, optimization of treatment conditions is of great importance for using microwave
313
technology. That might be the reason “smart” oven was suggested to be a solution, which still
314
requires more study.
315 316
3.4.
Irradiation
Food irradiation has received much attention as an established technology in the food sector for
317
enhancing the safety and quality of food products. While the use of irradiation in food sector is very
318
diverse, inhibition of sprouting, insect and parasite disinfestation, shelf-life extension, and
319
destroying non-spore forming pathogens are the most commonly applications of irradiation in the
320
food industry (Farkas and Mohácsi-Farkas 2011). Irradiation, a non-thermal technology, is defined
321
as the application of ionizing radiation in small doses and can be used as a decontaminant
322
technology, to enhance the safety and shelf-life of foods (Birmpa, Sfika et al. 2013, Mikš-Krajnik, 12
323
James Feng et al. 2017). For example, it can be used for fresh meat to inactivate parasites, decrease
324
the pathogenic microorganisms in several foods, or impose insect disinfestation capacity in grains
325
and fruits (Birmpa, Sfika et al. 2013, Donsì, Marchese et al. 2015). UV light, γ, X, and α rays, and
326
electron beams are the most used irradiation techniques in industry. The term of ‘irradiation’ is most
327
often inferring to the γ-irradiation. It has been shown that the UV light as a disinfection choice in
328
food facilities, has a greater germicidal potential compared to the most known chemical compounds
329
such as chlorine and hydrogen peroxide with the optimal efficiency at 254 nm wavelength (Mikš-
330
Krajnik, James Feng et al. 2017).
331
The cobalt-60 (Co-60) is the main source of irradiation and the dose used in diverse treatments
332
varies based on the type of target food (Suklim, Flick et al. 2014) . The impact of ionizing radiation
333
on microorganisms in general, depends on several parameters such as the dose of treatment, the
334
dose and rate of absorption, and the environmental conditions (importantly temperature and gas
335
atmosphere). The mechanism of irradiation in inactivation of bacteria is mainly through damaging
336
their DNA that leads to the prevention of proliferation.
337
The results of use of irradiation in controlling L. monocytogenes in several foods is
338
presented in Table 5. A high reduction (greater than 6.65 and 7.56 logs) in L. monocytogenes counts
339
in blue swimming crab lump meat for the irradiation treatments of 4 and 6 kGy, respectively.
340
Irradiation at 1 and 2 kGy doses provided 2.10 and 5.35 logs reduction, respectively for L.
341
monocytogenes DMST 1783, and 1.56 and 4.19 logs for L. monocytogenes DMST 4553. In
342
addition, during 28 days storage of the product after irradiation, the recovery of injured L.
343
monocytogenes was observed (Suklim, Flick et al. 2014).
344
[Table 5]
345
The reductions of 2.0, 3.50, and 45.0 log CFU/g in L. monocytogenes population in the
346
dough subjected to the electron beam treatment at 1, 2, and 3 kGy, and 1.0 and 2.2 CFU/g for the
347
samples subjected to the gamma treatment at 1.5 and 2.5 kGy, respectively. The use of doses greater
348
than 3.0 kGy for both electron beam and gamma irradiation reduced L. monocytogenes counts to 13
349
below the detection limit (Jeong and Kang 2017). Treatment of sliced cheese at a dose of 0.2 and
350
0.4 kGy of X-ray irradiation resulted in 2.28 and 3.70 log reductions in L. monocytogenes and that
351
was reduced to the less than the detectable limit (< 0.7 CFU/g) for the samples subjected by 0.6 and
352
0.8 kGy treatments.
353
Ha & Kang (2018) used krypton-chlorine excilamp irradiator for inactivation of L. monocytogenes
354
in water (Ha and Kang 2018). Generally, at higher treatment times and initial population
355
inoculated, more reduction and less reduction, in L. monocytogenes count was found, respectively
356
(Table 5). In treatment of Tahini halva through gamma radiation, by increasing irradiation dose,
357
higher reductions of L. monocytogenes was found (Osaili, Al-Nabulsi et al. 2018).
358
In coconut water subjected to a continuous-flow UV irradiator, a linear trend was found for
359
inactivation of L. monocytogenes with increase in the UV dose (Bhullar, Patras et al. 2018).
360
Antimicrobial impacts of three different UV irradiations (A, B, and C) in two different buffer
361
solutions on L. monocytogenes were studied by Jeon and Ha (2018). The wavelength of UV light
362
that is commonly used in food industry ranges from 100 to 400 nm and the wavelength range of the
363
UV-C was 200–280 nm that had the highest efficiency in inactivation of bacteria and viruses,
364
compared to UV-A or UV-B. Therefore, although irradiation doses used in this study of Jeon and
365
Ha (2018) was UV-A> UV-B > UV-C, the efficiency in destroying L. monocytogenes was not in
366
this trend (Table 5) which could be due to the great differences in mechanism of three types of UV
367
(A, B, and C) against live microorganisms. The impact of irradiation and storage on the L.
368
monocytogenes and L.innocua counts in carrot and cut tomato has also been investigated and the
369
populations of both organisms decreased by at least 2 log10 at 1 kGy dose and no re-growth during
370
storage was observed (Mohácsi-Farkas, Nyirő-Fekete et al. 2014).
371
However, there is a controversial issue over radiation use -whether or not it may lead to the
372
formation of radioactivity in foods, resulting in the harmful impacts on the body - which has made a
373
significant limitation for irritation use, in spite of its advantages (Birmpa, Sfika et al. 2013, Xuan,
374
Ding et al. 2017). In this regard, the Codex Alimentarius Commission declared that the maximum 14
375
dose of irritation use is 10 kGy (Roberts 2014). In order to use irradiation for foods, the
376
transportation of final products to an irradiation unit sounds necessary which is another limiting
377
factor for using irradiation as a post-packaging technology (Parlato, Giacomarra et al. 2014). One of
378
other main drawbacks of irradiation to control pathogenic bacteria is its low penetrating power,
379
which provides a limited efficiency, especially on foods with irregular surfaces. Therefore, it has
380
been greatly proposed that irradiation combined with other technologies and methods can be a
381
practical choice to be used against pathogenic bacteria in foods.
382
Research studies are indicating that people are showing more tendency to accept irradiated
383
foods after receiving appropriate information regarding its safety and quality which has been a
384
challenge associated with the use of this technology in food sector.
385
3.5.
Ohmic heating
386
Ohmic heating is an innovative thermal technology which provides a fast and uniform
387
heating through employing electric current flowing into the target foods during diverse processes
388
such as drying, cooking, and sterilization. This technique due to showing capacities in terms of
389
reducing heat damage and nutrient loss compared to conventional thermal treatments has gained
390
much attention. The conversion of electrical energy into thermal energy is the main principle of
391
Ohmic technology. A critical aspect in using Ohmic technology is the direct contact of foods with
392
the electrodes. The migration of metal ions into foods with a toxic potential due to electrode
393
corrosion has been one of important obstacles of extensive use of Ohmic heating in the food
394
industry for many years (Kim and Kang 2015). However, nowadays the problem has been solved in
395
some degree by introducing the inert electrodes and pulse waveforms. It has been reported that the
396
pulsed Ohmic heating, has provided the possibility of inactivating foodborne pathogens without
397
making electrode corrosion in some foods (Kim, Choi et al. 2017). The major mechanism of Ohmic
398
heating for inactivation of microorganisms is through heating effects. However, some other
399
mechanisms such as pore formation (electroporation) in the cell membrane of microorganisms have
400
been reported (Park, Ha et al. 2017, Kim, Park et al. 2018). The electroporation can lead in cell 15
401
permeability and cause membrane disruption and finally lead to the cell death (Kim and Kang 2015,
402
Kim and Kang 2017), however, it seems that the whole mechanism of antimicrobial inactivation of
403
Ohmic is not still fully understood.
404
The advantages of Ohmic technology which is providing a uniform and rapid heating
405
throughout product volume, depends on the conductivity of target product, the configuration and
406
properties of treatment chamber, and the composition and flow characteristics of food. Another
407
important point in using this technology is the use of electrodes as heating source instead of
408
contacting foods with hot surfaces (such as some conventional thermal technologies) which
409
possibly plays an important preventive role in production of biological, organic or inorganic
410
unwanted layers during Ohmic heating (Kim and Kang 2015, Lee, Kim et al. 2015). In Ohmic
411
technology, the heating process can be significantly shortened which can result in a higher quality
412
of final food products, while maintaining the required sterilization impact. For research-based
413
fields, batch-type is commonly used and for industry sections, the continuous-type is more
414
promising.
415
The efficiency of Ohmic heating for inactivation of L. monocytogenes in diverse foods has
416
been studied extensively, as shown in Table 6. The results of several works have revealed that L.
417
monocytogenes is more resistant to Ohmic heating than other pathogenic bacteria. For example, the
418
population of mesophilic aerobic bacteria, mold-yeast, and Staphylococcus aureus was reduced
419
significantly and even Salmonella spp. was completely eliminated from meatballs samples, while
420
Ohmic heating was not able to inactivate all L. monocytogenes cells (Sengun, Yildiz Turp et al.
421
2014). Although, for most cases, the reduction of L. monocytogenes was similar for Ohmic and
422
conventional heating (for specific times and temperatures), since Ohmic processing was able to
423
increase the temperature more rapidly (than conventional), L. monocytogenes was inactivated more
424
effectively by Ohmic heating in the fixed treatment time intervals (Kim and Kang 2015).
425
[Table 6]
16
426
The higher temperature and time of treatment led to a higher reduction of L. monocytogenes
427
at any pH value for juice samples, without making negative effects (Lee, Kim et al. 2015). The
428
efficiency of continuous-type pulsed Ohmic in reducing the inoculated L. monocytogenes on
429
buffered peptone water (BPW) and tomato juice showed that Ohmic treatment parameters such as
430
flow rate, voltage, and initial temperature are determining factors affecting efficiency of
431
continuous-type Ohmic heating in inactivation of pathogens (Kim, Park et al. 2018). In addition,
432
using preheating could help inactivation of pathogens. A 5 log reductions of L. monocytogenes was
433
observed in treating tomato juice by Ohmic heating of 12.14Vrms/cm at 0.2 L/min flow rate of
434
preheated sample to 50 °C (Kim, Park et al. 2018).
435
Several studies have addressed the effect of food composition on the efficiency of Ohmic
436
heating in reducing pathogenic bacteria such as L. monocytogenes. For example, it was shown that
437
the milk fat and lactose have inhibitory impacts on the inactivation of L. monocytogenes by Ohmic
438
heating (Kim and Kang 2015, Lee, Kim et al. 2015, Kim, Jo et al. 2017). The higher heating rate in
439
milk samples with a lower fat content may be attributed to the higher electrical conductivity of these
440
products which indicates the possibility of non-uniform heating (Lee, Kim et al. 2015). Therefore,
441
for dairy foods, in specific the milk fat content and in general the food product composition should
442
be considered as a determining factor for assessing the efficiency of Ohmic heating for
443
pasteurization process. The sugar concentration (°Brix) of apple juice is an important factor for
444
optimization of Ohmic heating for pasteurization (Park, Ha et al. 2017). When, the voltage ranged
445
from 30 to 60 V/cm and 5 different °Brix (18 to 72) was used, the 72 °Brix juice showed the lowest
446
heating rate and considering the results of all experiments, the highest performance coefficients
447
were reported for two combinations of 30 V/cm in 36 °Brix and 60 V/cm in 48 °Brix. However, a 5-
448
log reduction of L. monocytogenes was observed for 60 s treatment (30 V/cm) of juice with 36
449
°Brix, but for the juice with 48 °Brix, the Ohmic heating for 20 s at 60 V/cm achieved this level of
450
reduction (Park, Ha et al. 2017). Therefore, for juices with different concentration of sugar, to reach
451
to the best choice of Ohmic heating condition, experiments and modeling efforts is needed. 17
452
While the conventional heating rate was not significantly affected by pH level and L.
453
monocytogenes was inactivated more effectively at lower pH (Kim and Kang 2015), different result
454
was reported for Ohmic heating (Table 6). Possibly due to the higher electrical conductivity at
455
higher pH, the rapid inactivation of L. monocytogenes was observed at pH= 4.5. Thus, the change of
456
pH level should be considered in optimizing pasteurization of orange juice through Ohmic heating
457
(Kim and Kang 2015). In another work, the low frequency (0.06- 1 kHz) pulsed Ohmic heating was
458
used to inactivate L. monocytogenes in BPW and tomato juice (Kim, Choi et al. 2017). The larger
459
reductions of L. monocytogenes in BPW than tomato juice was observed, which may be due to the
460
strong acid resistance of L. monocytogenes so that this has enabled it to survive under the conditions
461
of low pH of orange juice and the protection effect of food ingredients on L. monocytogenes against
462
treatment. Based on the lower numbers of propidium iodide uptake, indicating lower cell membrane
463
damage obtained for higher frequencies, the low frequency Ohmic treatment was recommended due
464
to the reduced resuscitation level than higher frequency treatments (Kim, Choi et al. 2017). The
465
effect of voltage gradients (30-60V/cm) of Ohmic heating and °Brix of apple juice (18-72) on L.
466
monocytogenes inactivation was investigated (Park, Ha et al. 2017). At all voltage levels, the 72
467
°Brix apple juice, showed the lowest heating rate. A 5-log reduction of L. monocytogenes was
468
achieved in 20 s treatment at 60 V/cm, for all °Brix samples, except 72 °Brix. Generally, it was
469
reported that the time duration required for 5-log reduction at 30 V/cm in 36 °Brix was about three
470
times longer than for 60 V/cm for all °Brix samples, except for 72 °Brix (Park, Ha et al. 2017).
471
The synergetic combination effect of Ohmic heating with various essential oils (carvone,
472
eugenol, thymol, and citral) for destroying L. monocytogenes in BPW and salsa has been studied as
473
well (Kim and Kang 2017). The combination of Ohmic heating with citral in BPW and with thymol
474
in salsa showed the most synergistic anti-Listerial effect (5.8 and 4.3 log CFU/ml reduction in L.
475
monocytogenes, respectively). Therefore, the combination of Ohmic heating and thymol treatment
476
was suggested for effective pasteurization of salsa (Kim and Kang 2017). The combination effect of
477
carvacrol and Ohmic heating for inactivation of L. monocytogenes in salsa showed a synergetic 18
478
effect after 30 and 40s treatment. While, the enumeration on resuscitation media after treatment
479
showed the inactivation of about 0.3 and 2 log for treatment by 1.3 mMol carvacrol and 12.1
480
Vms/cm Ohmic heating after 50s, respectively; the combination of them brought over 5 log
481
reduction in L. monocytogenes counts (Kim and Kang 2017).
482
3.6.
Ozonation
483
The use of ozone technology for decreasing the load of bacteria at surfaces in contact with
484
foods has attracted much attention recently. This technology involves the use of ozone or triatomic
485
oxygen (O3) which is an unstable allotrope of oxygen either in gaseous or dissolved form, to
486
decrease the load of target microorganisms in the food industry. The FDA approval of ozone as a
487
direct additive in food in 2001 triggered an increasing interest in ozone applications. Ozone has
488
shown a promising capacity to be considered as an alternative sanitizer for chlorine substances;
489
since during using ozone when it is liberating the principal product of oxygen, it will be
490
decomposed to several free radicals and leaves no residual components on foods which is an
491
important advantageous property than chlorine compounds (Akata, Torlak et al. 2015). For
492
example, in the work of treating apple juice with ozone, the concentration of residual ozone was
493
below the acceptable levels (0.4 mg/L) for all treated samples (Sung, Song et al. 2014). The use of
494
ozone requires relatively a short contact time and the treatment can take place during the process of
495
foods or on the final products (Ronholm, Lau et al. 2016).
496
Ozone has been effective against both Gram positive and Gram negative bacteria as well as
497
fungi, and even it has shown a capacity to be a virucidal agent. Among the parameters that affect
498
ozone antimicrobial properties, its solubility in water as well as the stability of its reactions with
499
organic and inorganic compounds are important. However, relative humidity (Timmermans, Groot
500
et al.), pH, temperature, food additives, and the amount of organic compounds present in food
501
formulation which can surround the cells and protect them are among important properties of foods
502
affecting the antimicrobial efficiency of ozone (Bridges, Rane et al. 2018). As well, the sensitivity
503
of target microorganisms (in strain level) to ozone, food matrix, the method of ozone treatment, the 19
504
devices and procedures for measurements of ozone are important parameters in optimization of
505
ozone treatment for specific foods (Khadre, Yousef et al. 2001, Aponte, Anastasio et al. 2018). In
506
fact, the oxidant potential of ozone can induce the reactions leading to the destruction of cell walls
507
and cytoplasmic membranes of bacteria. Ozone may attack principal components of cells such as
508
glycoproteins, glycolipids, and other amino acids and disrupt or inhibit the enzymatic reactions of
509
the cell (Sheng, Hanrahan et al. 2018). These changes can increase membrane permeability that is
510
the most important parameter of cell viability, resulting in the functional cessation of cell system
511
(Khadre, Yousef et al. 2001, Aponte, Anastasio et al. 2018).
512
The successful use of ozone in processing different food products has been reported (Crowe,
513
Skonberg et al. 2012, Muthukumar and Muthuchamy 2013, Aponte, Anastasio et al. 2018) and
514
summarized in Table 7. The use of aqueous ozone in salmon fillets (concentrations up to 1.5 mg/L)
515
efficiently reduced the initial number of aerobic bacterial populations and showed a significant
516
reduction of the L. innocua counts without making negative effects (Crowe, Skonberg et al. 2012).
517
When fresh chicken samples were dipped in deionized water, containing L. monocytogenes (for 30,
518
45 and 60 s) and were subjected to the gaseous ozone for 1 to 9 min (33 mg/min), ozone treatment
519
(at 33 mg/min for 9 min) efficiently inactivated 5-6 log CFU/g of L. monocytogenes on chicken to
520
below detection limit (Muthukumar and Muthuchamy 2013).
521 522
[Table 7] While the rate of ozone generation did not affect the efficiency of process, the time required
523
to obtain a 5 log reduction (t5d) increased at higher Brix in apple juice (Choi, Liu et al. 2012).
524
Sheng, Hanrahan et al. (2018) showed that gaseous ozone decreased L. innocua count on apple fruit
525
surfaces to ~1.0 Log10 CFU/apple after 30-week cold storage and suggested the use of ozone gas in
526
combination with the commercial cold storage to control Listeria spp. in apple fruit during storage
527
(Sheng, Hanrahan et al. 2018). (Karaca and Velioglu 2014). The efficiency of ozone was very close
528
to that of distilling and chlorinating (100 mg/L), resulted in the reduction of L. innocua count for
529
2.2 and 2.3, on some vegetables, respectively, without imposing negative effects, highlighted its 20
530
promising potential to be used for treating vegetables (Karaca and Velioglu 2014). Ozonation of the
531
white button mushrooms (at 5.3 mg/L for 60 min) reduced the counts of L. monocytogenes by 2.80
532
log and the reduction was lower than E.coli and Salmonella (Akata, Torlak et al. 2015). The effects
533
of shrimp treatment with ozonated water, antimicrobial coating and cryogenic freezing, singly or in
534
combination on the count of natural or inoculated L. innocua were examined by Guo, Jin et al.
535
(2013). The single use of every treatment reduced the natural bacteria and L. innocua by <2 log
536
CFU/g, while the combined use of them showed a synergistic reductions of the natural bacteria and
537
L. innocua (Guo, Jin et al. 2013). The optimal reduction of L. monocytogenes on fresh-cut bell
538
pepper was 3.06 log that was achieved with exposure to 9 ppm ozone for 6 h. The higher exposure
539
time and higher concentration led to a higher reduction of L. monocytogenes (Alwi and Ali 2014).
540
A synergistic effect in the inactivation of L. monocytogenes was found between ozone and
541
heating treatment at 50 °C. While, the simultaneous use of ozone and heat for 1 min reduced the
542
counts of L. monocytogenes by 0.79 and 0.93 log CFU/ml at 25 and 45 °C, respectively, the count
543
reached to below the detection limit (1 log CFU/ml) at 50 and 55 °C (Sung, Song et al. 2014).
544
Therefore, it was concluded that ozone combined with a mild heat treatment can have a higher
545
antimicrobial effect than ozone alone at room temperature (Sung, Song et al. 2014). While, ClO2
546
treatment resulted in the count reductions of 5.5, 2.1, and 7.1 log on carrots, blueberry, and
547
tomatoes, the gaseous O3 resulted in the reductions of only 0.8, 1.8, and 1.1 log, respectively. The
548
results showed that gaseous ClO2 can be a promising disinfectant for these three food products and
549
gaseous O3 was not satisfactory (Bridges, Rane et al. 2018). In fresh brines, 10 min ozonation and
550
10 min UV radiation lead to a 7.44 and 1.95 log CFU/ml reduction, respectively. However, the
551
sequential exposure of 10 min ozonation and UV resulted in >9 log CFU/ml reduction in L.
552
monocytogenes populations in fresh brine, which showed the high efficiency of using these two
553
treatments as hurdles (Kumar, Williams et al. 2016).
21
554
3.7.
555
Non-thermal plasma (NTP) or cold plasma in the food sector is highly recommended for
556
destroying detrimental microorganisms potentially presented in foods including sporulating and
557
spoilage microbes/pathogens. NTP technology refers to the fourth state of matter and consists of
558
partly ionized gas including electrons, charged ions, free radicals, excited molecules, photons and
559
atoms, in the absence of thermodynamic equilibrium. By applying electric discharge to a working
560
gas, inert or ambient air, plasma can be generated. Under atmospheric conditions, NTP is normally
561
consisted of reactive oxygen species (ROS), such as O, O2, O3, reactive nitrogen species (RNS),
562
such as N2, NO., NO2 and if humidity is involved, OH., H2O2, which all are known as potential anti-
563
microbial agents (Kim, Lee et al. 2014, Sant'Ana, Lis et al. 2018, Timmons, Pai et al. 2018). In
564
plasma, electrons have a high temperature while the temperature of active medium remains low.
565
Plasma application is mainly related to the processing of materials at industry level, which for
566
decontamination and processing of food is relatively novel. The typical sources for generation of
567
NTP include radio frequency plasma (RFP), dialectic barrier discharges (DBD), corona discharge
568
and microwave discharges (Phan, Phan et al. 2017). The major advantage of NTP is operating under
569
ambient conditions, which can cause less damages to the quality of foods (Jiang, Sokorai et al.
570
2017, Kim and Min 2018, Sant'Ana, Lis et al. 2018).
571
Cold plasma
The inactivation mechanism of microorganisms by NTP is associated with the existence of
572
reactive species that can attack the cell through oxidation stresses or physical lysis and cause either
573
leakage and release intracellular material (Kim, Lee et al. 2014, Timmons, Pai et al. 2018) or result
574
in genomic DNA damage (Jiang, Sokorai et al. 2017). The anti-microbial efficiency of NTP
575
depends on the applied voltage, frequency, mode of exposure, electrode type, gas mixture, treatment
576
time, and cell membrane characteristics of target microorganism as well as the type of product and
577
the bacterial location (Jiang, Sokorai et al. 2017, Phan, Phan et al. 2017, Kim and Min 2018).
578 579
For inactivation of L. monocytogenes by NTP, just a few studies have been successful in reducing the microbial load to 5-log or more. Table 8 shows a summary of literature studied on the 22
580
antimicrobial effect of NTP against L. monocytogenes from 2015 to 2018. Jiang, Sokorai et al.
581
(2017) and Ragni, Berardinelli et al. (2016) managed to inactivate Listeria spp. by more than 5 log
582
in tomato-smooth surface and in saline solution. Jiang, Sokorai et al. (2017) investigated the
583
inactivation of L. innocua rate in grape, tomato, cantaloupe and baby spinach and studied the
584
quality changes by applying plasma activated hydrogen peroxide under indirect exposure for 45 s
585
treatment and 30 min dwell time. However, for native microorganisms, this treatment was by far
586
less effective than inoculated bacteria. Moreover, decontamination of tomato stem scar was
587
remarkably harder and the population of microorganisms could not be decreased to more than 1.3
588
log. They related it to the formation of biofilms which provides a physical barrier for diffusion of
589
antimicrobial agents. That was completely in accordance to the other studies that showed the
590
effectiveness of NTP treatment depends on the matrix and surface structure of the products (Ragni,
591
Berardinelli et al. 2016, Sant'Ana, Lis et al. 2018).
592 593
[Table 8] The distance from actuator is another major factor for antimicrobial effect of NTP.
594
Timmons, Pai et al. (2018) represented that just at the distance close to the NTP producer, where the
595
concentration of the charged species is higher; the reduction in L. monocytogenes could reach to
596
almost 4.5 log. This can be due to the temporary life of reactive species and the fact that they return
597
to their normal state after a short while. As for the treatment time, while it was believed that longer
598
treatment time always results in higher inactivation rate, but this difference is not always
599
remarkable, and depends on the NTP producer device. Increasing the exposure time from 5 min and
600
10 min to 20 min in the studies conducted by Kim and Min (2018) and Sant'Ana, Lis et al. (2018)
601
slightly improved the inactivation rate from 0.6 to 1.1 log, and from 4.2 to 4.4, respectively. On
602
contrary, Ragni, Berardinelli et al. (2016) showed that changing the treatment time from 40 to 60
603
min can sustainably increase the inactivation rate of L. monocytogenes from 4 log to more than 7
604
log, respectively. In other studies, NTP failed to sufficiently inactivate L. monocytogenes (Choi,
23
605
Puligundla et al. 2016, Kim and Min 2018, Sant'Ana, Lis et al. 2018) and further studies are needed
606
to investigate the affecting factors more thoroughly.
607
There is a considerable disadvantage regarding the NTP treatment, which is the production
608
of nano-particles from electrode materials. Borra, Jidenko et al. (2015) showed that dielectric
609
barrier discharges at atmospheric pressure can generate tailored nanoparticles with the same
610
composition as the metal electrodes. As for the present level of nano-particle in food products,
611
further studies are required.
612
3.8.
Pulsed electric fields (PEF) processing
613
In the food industry, PEF can be used to destroy microorganisms such as molds, yeast, and
614
bacteria to improve the safety of foods. PEF or electroporation technology is defined as the use of
615
short, but high voltage pulses to a target food which is passed through two electrodes
616
(Timmermans, Groot et al. 2014, Zhao, Zhang et al. 2017). PEF technology has been subjected to a
617
wide investigation for its application possibility in food preservation and pasteurization due to its
618
great capacity in inactivation of pathogenic microorganisms and acquiring other merits, compared
619
to conventional thermal processing (Pyatkovskyy, Shynkaryk et al. 2018). PEF is able to disturb the
620
membranes of biological cells. The probable cause for the loss of cell membrane through the PEF
621
may be the creation of hydrophilic pores in the membrane structure and the opening of protein
622
channels (Sharma, Bremer et al. 2014, Pyatkovskyy, Shynkaryk et al. 2018). The type, composition,
623
and all other features of foods may affect the efficiency of PEF in destroying a target
624
microorganism. Two principal mechanisms for the PEF in microbial inactivation are known to be:
625
electroporation and electrical breakdown. Basically, thousands of volts per cm conducted for 20–
626
1000 µs are vital for an efficient inactivation of organisms in food products. The strength of the
627
electric field mainly depends on the objective of its use in food industry. As an example, for
628
increasing the efficiency of drying or enhancing the extraction yields for certain intracellular
629
compounds, lower intensity levels of PEF treatment are promising. However, due to survival of an
24
630
important percentage of cells subjected to PEF at the range of 10–19 kV/cm, only the PEF with
631
electric fields over 25 kV/cm is practically efficient for microbial inhibition. The bacterial spores in food products are resistant to PEF, even at high intensity, as well
632 633
different pathogenic microorganisms show various sensitivity to PEF. Gram positive bacteria are
634
generally less resistant to PEF than Gram negative bacteria. It was claimed that L. monocytogenes is
635
the most resistant microorganism against PEF, and thus it was suggested that the ability of a PEF
636
treatment to kill L. monocytogenes can be an indicator for its effectiveness in adequate inactivation
637
of microorganisms. The lower sensitivity of L. monocytogenes to electric PEF compared to other
638
pathogens might be demonstrated by two reasons (Timmermans, Groot et al. 2014). The size and
639
shape of target microorganisms influences the input needed electric field to destroy the cells.
640
Generally, the smaller cell size leads to a lower membrane to potentially be affected by the
641
treatment. Also, the shape of microorganism can greatly affect the membrane potential: Generally,
642
the electric field required for destroying a rod-shape cell is almost five times stronger than that
643
amount needed for a spherical shaped cell with the same characteristics (Timmermans, Groot et al.
644
2014).
645
Several works have studied the effect of PEF on inactivation of L. monocytogenes in
646
different food products, as summarized in Table 9. The required energy for inducing a 5 log
647
reduction in L. monocytogenes was 113, 257, and 508 kJ/kg for apple, orange, and watermelon
648
juices, respectively which indicated the effect of pH trend (watermelon> orange> apple) on
649
sensitivity of L. monocytogenes to PEF treatment. The comparison of required energy for making a
650
5 log reduction in L. monocytogenes with those levels obtained for other bacteria such as E.coli (67,
651
58, and 197 kJ/kg for apple, orange, and watermelon juices, respectively) and Salmonella (65, 76,
652
and 130 kJ/kg for the same order of juices) well represents the higher resistance of L.
653
monocytogenes to PEF (Timmermans, Groot et al. 2014).
654
[Table 9]
25
655
In several studies, L. innocua was chosen as a L. monocytogenes surrogate, due to the
656
biosafety issues (Schottroff, Gratz et al. 2019). When PEF treatment of water was performed at both
657
10 and 20 V/cm for different time treatments, the increase of electric field input and time treatment,
658
generally led a higher inactivation of L. innocua (Pyatkovskyy, Shynkaryk et al. 2018). The impact
659
of PEF combined with a sanitizer solution treatment on the inactivation of L. innocua inoculated on
660
blueberry fruits was studied (Jin, Yu et al. 2017). L. innocua counts on blueberry subjected to PEF
661
(maximum peak voltage: ±11 kV) for 2 and 4 min was reduced by 2.3 and 2.6 log CFU/g,
662
respectively. However, when blueberries were soaked in a specific sanitizing solution (Tsunami
663
100) and were not treated by PEF, the reduction of less than 1 log CFU/g in L. innocua were
664
observed (Jin, Yu et al. 2017).
665
The use of higher inlet temperature was not effective in increasing the inactivation
666
capability of the PEF against L. innocua in whey proteins which might due to specific conditions of
667
the PEF process, higher temperatures induced a change in membrane fluidity associated with a
668
decrease of the parameter of electric field strength (Schottroff, Gratz et al. 2019). The portion of
669
lethal and sub-lethal injury is an important factor for studying the recovery possibility of injured
670
cells by a target process after treatment and during shelf-life of the product which should be kept at
671
a low acceptable level. The proportion of the sub-lethally injured L. monocytogenes cells in milk
672
were affected by the electric field strength and treatment time and it increased from 18.98% to
673
43.64% with increasing the electric field strength from15 to 30 kV/cm; while it progressively
674
decreased at greater electric field strengths and with longer treatment times (Zhao, Zhang et al.
675
2017). When milk with different initial temperatures were subjected to PEF (Sharma, Bremer et al.
676
2014) by the electric field strengths of 18-28 kV/cm for 17-235 us, the PEF treatment at 4° C did
677
not reduce L. innocua numbers, but its effectiveness increased at higher temperatures. PEF
678
treatments at 22-28 kV/cm (for 17-101 us) reduced L. innocua count to below the detection limit at
679
55° C (Sharma, Bremer et al. 2014).
26
680
Despite the inferred benefits of using PEF technology, some limitations associated with its
681
use have been reported. For example, some spores or ascospores, or vegetative cells have shown
682
resistance to the conventional PEF treatment which can result in to a failure in the process of
683
pasteurization which equals with a potential safety hazard (Arroyo, Cebrián et al. 2012).
684
4. Conclusion
685
Although L. monocytogenes is less common than some other foodborne pathogens in
686
environment and foods, due to having such high mortality rate of about 30% accompanied with its
687
high resistance to sterilization technologies, it was considered the focus of this study. This work
688
was performed to assess the efficiency of non-conventional food processing technologies in
689
destroying L. monocytogenes and potentially most of other pathogenic bacteria in foods. Among all
690
new technologies emerged as an alternative to the conventional heating sterilization, recently high-
691
pressure processing (HPP) was studied extensively, and thanks to the large number of researches,
692
HPP was more developed, resulted in higher number of works with a successful 5-log reduction of
693
L. monocytogenes counts in foods meeting the FDA requirement, followed by ultrasound and
694
microwave technologies. However, based on the literature, there is a serious concern regarding all
695
these methods, which is the sublethal effect and the chance for recovery of L. monocytogenes after
696
treatment. Since the potential recovery of L. monocytogenes during shelf-life can be considered as a
697
serious food safety threat, enough studies should be conducted to address this issue before labeling
698
any treatment as a promising technology in inhibition of L. monocytogenes growth in food products.
699
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40
Product Kiwi puree
Table 1. The effect of conventional heat treatment on the counts of L. monocytogenes in food products Treatment conditions Microbial Initial count, reduction, D- value (min) Others Time, min T, °C log(CFU/ml) log(CFU/ml) 12.5, 7.5, 2.5
50, 55, 60
3, 6, 5
Cold smoked salmon
58, 66
14.1, 0.3
Benlloch-Tinoco, Pina-Perez et al. (2014) Shi, Tang et al. (2014)
Spinach blend PBS
56, 58, 60 56, 58, 60
11.8, 4.5, 1.2 2.7-4.4, 1-1.4, 0.35-0.66
Monu, Valladares et al. (2015) Aryani, den Besten et al. (2015)
BHI
55, 60, 65
9.2-30.2, 0.58-4.1, 0.075-0.57
Ricotta cheese
25, 40
90, 85
Turkey ham
30
90, 80
5
4, 1
Skim Milk
1
65, 70
6.7
Cream
1, 3
70
5.9-6
Smoked tench
2.73
72
TSB
15
55
TSB
1
In shell pistachio
0.5
Almond
0.25
5
End temp.< 60 °C, <50 °C
Spanu, Scarano et al. (2015)
>5, 3.05
Fixed temp.
Delgado Suárez, Chairéz Espinosa et al. (2015) Kim and Kang (2015)
2.48, 5
Fixed temp., end temp: 70 °C
5
Smoking oven
5
1
5.2
5
6
>5
4.56
6
>5
2.41
Branciari, Valiani et al. (2016) Ragni, Berardinelli et al. (2016)
+ 0.5 mM Nano d-limonene Superheated steam
Ban and Kang (2016)
0.8
aw=0.565
Rachon, Penaloza et al. (2016)
Seasoning
0.65
aw=0.655
Chicken meat powder
0.61
aw=0.383
Pet food
0.54
aw=0.653
Confectionery
200
pH=3.4
Reference
100
Sausage/ham
14.6/11.8
Sausage/ham
25.4/24.9
Tomato, Lettuce
2.5
Tomato, Lettuce
1.75, 2.5
Water, TSBYE
5, 60
55
Caramel apple
0.08
99
Broth
60
4
60
Wang, Uyttendaele et al. (2016)
4
+3% NaCl
3.5, 3
at 5 °C for 5 days before treatment at 5 °C for 1 day before treatment
Poimenidou, Chatzithoma et al. (2016)
+ 2% Lactic acid
Omori, Miake et al. (2017)
3.5, 1.5
60, 62.5, 65
9
5, 2 <3
Gustafson and Ryser (2017) 1.3, 0.53, 0.24
41
Wang, 2017 Wang, Devlieghere et
Agar
60, 62.5, 65
3.1, 1.2, 0.41
al. (2017)
Salmon roe
57.5, 60, 62.5, 65 57.5, 60, 62.5, 65 52.5
3.42-6.67, 1.34-1.37, 0.3-0.48, 0.1-0.14 12.9-19.68, 5.03-6.77, 1.21-2.4, 0.5-0.79 1.49, 24.76
Li, Huang et al. (2017) 4.5% salt
Apple, Carrot juice
0.016, 0.952
+ 0.5 mM d-limonene
Carrot juice
65.43
juice without fiber and fat
Apple, Carrot juice
Saline solution
15
50, 55, 60
9.1
Mate, Periago et al. (2017)
1.6, 3.4, 4.1
Xuan, Ding et al. (2017)
Tryptic Soy Broth
54
10-17.8
pH=4.5
Tomato puree
54, 58
10.6, 3.42
"
Apple juice
2, 1.75, 0.75, 0.4
55, 60, 65, 70
Chili sauce
4
100
Cantaloupe
4
1, 5.5, 5.5, 5 8
Siguemoto, Gut et al. (2018)
6
10% sugar #
Kim, Park et al. (2018)
85
Steam, #
Neha, Anand et al. (2018)
, after storage, after storage + Acidic acid +H2O2
Trzaskowska, Dai et al. (2018)
aw=0.3, 0.45, 0.6, 0.6, 0.6
Taylor, Tsai et al. (2018)
Ice cream
30
69
Mung Bean
20
60
6
5, 2, 4
Wheat flour
20, 15, 9, 20, 50
80, 80, 80, 75, 70 50, 55, 60
8
3,6, 5, 5, 3.5
Crab meat
Dufort, Sogin et al. (2017)
7.08, 3.13, 1.59, 4.61, 16.85 174.4, 28.2, 1.6
Forney, Fan et al. (2018)
McDermott, Whyte et al. (2018)
#: In this study, Listeria innocua has been used. Temp: Temperature, TSB: Tryptic Soy Broth, PBS: Phosphate-buffered saline, BHI: Brain heart infusion broth. aw: water activity.
42
Table 2. The effect of high hydrostatic pressure treatment on the counts of L. monocytogenes in food products
45, -5
Initial counts, log(CFU/ml) 6-7
Microbial Reduction, log(CFU/ml) 6.2, 5.6
31
5.6-4.9
2.2-3
Merialdi, Ramini et al. (2015)
10
7
Ramos, Chiquirrín et al. (2015)
5 5
25
7
2.5,3.5,4 4
25
7
1.7
8.45
5.13, 5.18
Product
Treatment condition Pressure, Pa Time, min
T, °C
Smoothie
300
5
Pork production
600
6
Milk, whey, buffer
300 400
Green bean
Shelf life Days log (N)
Others
Scolari, Zacconi et al. (2015)
14
3.2
#
, + Chitosan
230, 300
5
45, -5
Dry-cured- ham
800-850
5
15
>5
aw=0.86-0.96
15
>5
aw=0.96
Dry-cured-ham
450
10
12
5.27
15
0.58
Skimmed milk
250, 200
70, 60
7
>7, 1.33
Cured meat Raw milk
700, 600 400, 450
3 5
20 25
5 8
5 >5, >7
Soup
500, 600
5
44
8
6
45
3, 5
3,5
60
28
21
600
1
25
8
6.16, 1.29, 6.16-7.47
Vacuum salad
400
1
18
7
4.2, 1.5
21
Cantaloupe puree
500, 400
5
35, 30
7
>5, <3
10
Ham
500
4
32,15
6
>5
20
8
1
22
>5
22
>3.5
450
Cheese
300
Cold- smoked salmon
600, 450
2
Chicken
300
10
-2
Zacconi, Giosue et al. (2015)
4.23
<5
Bover-Cid, Belletti et al. (2015)
de Alba, Bravo et al. (2015) #
Pinho, Oliveira et al. (2015)
11.7-29 g/l salt, 0.09 mg/l nitrite
Valdramidis, Patterson et al. (2015) Huang, Lung et al. (2015) Ates, Rode et al. (2016)
Chicken
Beef steaks
Donsì, Marchese et al. (2015)
3.6
Smoothie
700-850
Reference
0 salt:0% NaCl, 2.5% NaCl, 0-2.5% CaCl2
Balamurugan, Ahmed et al. (2016)
2.5, >7.5
pH:Low, High
Stratakos, Linton et al. (2016)
ND, 1.5
pH:6.9
Mukhopadhyay, Sokorai et al. (2016) Magalhães, Ferreira et al. (2016)
1-2
15
6
Li and Ganzle (2016) +Thyme extract
Bleoancă, Saje et al. (2016)
6
4, 3
36
<2 ,7.5 at 7°C
+Nisin (10ug/g)
Lebow, DesRocher et al. (2017)
23
6
6
21
ND
Packed with PLA/PEG/CIN4,3
Ahmed, Mulla et al. (2017)
23
6
<3
"
>3
PLA/PEG/CIN1,2
43
Sea bream fillet
300
5
Fruit puree Buffer solution
300
1
Black tiger shrimp
400, 500, 500
pulse, pulse, 12
Milk
400, 400, 500
5, 10,5
400, 500
30
5.3
1.83
10
5.2
5.5
5
"
<1
6
5
#
+0.8 ug/ml Endolysin
30
6
1.2
40
7
3, 4, 4.8
6.86- 6.4
3,>6,>6
, , 15
, ,8.77
5
>5, >6
, 15
, 8.99
+4 mg/ml potassium sorbate
400
"
>6
"
ND
+2 e-Polylysine
Fermented meat sausage
300
5
Cooked sausage
600
10
8/6
2
60
8
10
4, 8/6, 4
2
" 35
ND, 3.5/3, ND 4.5
"
ND
28 "
4.2, 8 ND, 4.7
72
Castro, Silva et al. (2018) + P. acidilactici HA-6111-2 storage at 10 °C
Balamurugan, Inmanee et al. (2018)
aw=0.9, 0.82 , +ready to eat meat microbiota +Nisin, Rosemary
Rubio, Possas et al. (2018) Teixeira, Repkova et al. (2018)
#
Pyatkovskyy, Shynkaryk et al. (2018)
550 500
10 3 "
6 6.5, 7.5 7.2, 6.5
3.7, 2.5 2.5, 3 5.2, 2
Water
400
1
9.5
6.5
Milk
550, 600
3, 12
9
2, >5
550
6/9
9
>5
500
5
6
4, 6
4,6
15
0, 1
600
5
6
4, 6
4
"
<1, 3
Scott A
0, 3
#
+Nisin
Alcantara-Zayala, Serment-Moreno et al. (2018)
CECT 4031
Evert-Arriagada, Trujillo et al. (2018)
600
5
6
4, 6
3.5, >6
Smoked salmon
500
10
25
7
1.5
Smoked salmon Mozzarella cheese
400 500
3 7.4
0.5 5.5
20
2.5
Storage: 10 °C+34 ug/ml Plyp825
Mozzarella cheese Milk
400 500, 400
3 7.4
2 6, 5
27 13
1 8
Storage: 10 °C+3.4 ug/ml Plyp825
5.5, 3.8
4, 3
27
1, 8
Storage: 10 °C+3.4 ug/ml Plyp825
Milk 400 # : in this study, listeria innocua has been used. aw: water activity.
"
Kaur and Rao (2017) Liu, Li et al. (2017)
Chorizo Sausage Ham
Fresh Cheese
van Nassau, Lenz et al. (2017)
#
3 "
Blazquez, Burgos et al. (2017)
Misiou, van Nassau et al. (2018)
44
Table 3. The effect of sonication on the counts of L. monocytogenes in food products Product/medium Amplitude Plastic container Lettuce, Strawberry
Treatment conditions Frequency, Time, kHz min 35 15 37
60, 45
T, °C
Initial count, log(CFU/ml)
Microbial Reduction, log(CFU/ml) 91% 2, >5
Others
Reference
Bath
Torlak and Sert (2013)
#
Birmpa, Sfika et al. (2013)
, Bath
Orange juice
600 W
28-45-100
35
5.5
5
Gabriel (2014)
Stainless steel, TSB and lettuce Lettuce wastewater
1200 W
37
100
6
1
Lee, Kim et al. (2014)
100 µm
24
20
35
5
2
5
<60
6
~5
6
Recycled water from lettuce TSB
20 90 µm
Milk
20
+ native microbes
Anese, Maifreni et al. (2015)
<2
#
, +Peroxyacetic acid
Gómez-López, Gil et al. (2015)
+ sucrose, aw=0.97, pH=6
Franco-Vega, Ramirez-Corona et al. (2015) Gabriel (2015)
3, 8, 10
65, 60, 55
8
5, <3, 2
28-100
50
<60
5.5
5
6
<1
+2%cinnamon oil
Ozcan and Demirel Zorba (2016) Luo and Oh (2016)
Vegetable salad
54 W/L
20
15
Bell pepper
400 W/l
40
5
60, 50, 40
2.5, 1.5, 1.5
Bath
5
60
>4.5
+Acidic water, pH=6.5
0.6
Bath
Salmon fillet
200
45
BHI
60 W
20-100
30
8.5
TSB
120 µm
20
TSB Injection needle
Lettuce leaf
8
22
5
+0.78 ug/ml Melittin
5
+ 40mM ZnO
<1
-
7, 5 7
3.25, <2 >5
700 W
6
2.23
#
6
12 75, 90% "
20 "
14 14
100 W
42
20
20
Endive Water
1.6 100%, 500 W
4
35
Wu and Narsimhan (2017)
4
BHI
9.5
1.6
#: in this study, Listeria innocua has been used. BHI: Brain heart infusion, TSB: Tryptic Soy Broth
45
Mikš-Krajnik, James Feng et al. (2017)
Dolan, Bastarrachea et al. (2018)
Hamann, Tonkiel et al. (2018)
+0.03% peracetic Acid , cleaner tank
Huang, Wrenn et al. (2018)
+ cinnamon leaf oil
Park, Kang et al. (2018)
#
Pyatkovskyy, Shynkaryk et al. (2018)
Table 4. The effect of microwave treatment on the counts of L. monocytogenes in food products Treatment conditions
Initial counts, log(CFU/ml)
Microbial reduction, log(CFU/ml)
Others
Reference
75, 60
6
>5, 2
Household MV
2450
35
7
>6
#
Rodriguez-Marval, Geornaras et al. (2009) Picouet, Landl et al. (2009)
875
80
2
6
>5
Continues
Kiwi puree
1000, 900
2450
82, 75
7
5
Salsa
915
30, 30, 50, 60, 110 340
5.5-6
Kiwi puree
4.8, 3.6, 2.4, 1.8, 1.2 K 1000
7
5, 5, 5, 4.58, 4.73 5.8
Chicken meat Tomato paste
900 1800-3000
2450 915
50
6
6
Peanut butter
2, 4, 6, 6, 6 K
915
300
5-5.6
Chicory Stem
900
2450
90
9, 4.3-5.6
0.24, 1.25, 3.82, 2.8, 1.98 6.5, >5
Apple juice
1000
2450
130
6
5
Chili Sauce
1500
915
50, 50, 70
7.4-7.8
>5
10, 25, 40 % sugar
3000
"
20, 25, 40
>5
10, 25, 40 % sugar
Product
Power, W
Frequency, kHz
Time, s
Frankfurter sausage
1100
2450
Apple puree
652
Catfish fillet
#
2450
T,°C
<50
>70
Sheen, Huang et al. (2012) Benlloch-Tinoco, Pina-Perez et al. (2014) Sung and Kang (2014) Benlloch-Tinoco, Igual et al. (2015) Zeinali, Jamshidi et al. (2015) Kim, Sung et al. (2016)
: in this study,Listeria innocua has been used
46
aw=0.5, 0.5, 0.5, 0.4, 0.3 Under vacuum
Song and Kang (2016) Renna, Gonnella et al. (2017) Siguemoto, Gut et al. (2018) Kim, Park et al. (2018)
Table 5. The effect of irradiation on the counts of L. monocytogenes in food products Treatment conditions
Product Type
Dose, kGy
Crab meat
Gamma
Frozen meat trimming Ready-to-bake cookie dough
Gamma Gamma Electron beam KrCl excilamp
1, 2 1,2 3, 1.5 3 3
Water
Tahini halva
Gamma 521.2 Ci
Coconut water PBS, PW PBS, PW Sliced cheese Ready-to-eat sliced ham
UV UV-A UV-B X X
0.8 1.6 2.4 3.2 4
Time
9,4.5 min 9 min 15, 20 s 15, 20 s 15, 20 s 0.15 min 0.3 min 0.45 min 0.6 min 0.75 min
Initial count, log(CFU/ml)
Microbial reduction, log( CFU/ml)
~6.8 ~7.6 6 5.96 4-5, 5-6 6-7 -
2.3, 5.7 1.5, 4.4 3, 1.5 4.5 5 >3, >3 3.3, >4 1.27, 1.98 0.69, 0.86, 0.62 1.24, 1.66, 1.19 1.97, 2.65, 1.81 2.55, 3.30, 2.29 2.96, 4.30, 3.29 2.7, 4.3, 5.85 0.9, 0.5 5.4, 3.5 3.7, >4.47, >4.47 3.8, >6.2, >6.2
8 5-6 0.4, 0.6, 0.8 0.4, 0.6, 0.8
6.9
*: The results are derived from graphs and the numbers are approximate. PBS: phosphate-buffered saline, PW: peptone water
47
Others
Reference
DMST 1783* DMST 4553*
Suklim et al. (2014) Xavier et al. 2014 Jeong and Kang (2017)
10 MeV 222-nm, 2.03 mJ/cm2, 20W pre-stored for:0, 7, 30d “ “ “ “ 2 10, 20, 25 mJ/cm * 2 356 nm, 94 mJ/cm * 2 307 nm, 21 mJ/cm 160 kV, 10mA
Ha and Kang (2018)
Osaili et al. (2018)
Bhullar et al. (2018) Jeon and Ha (2018) J.-S. Park and Ha (2019) Cho and Ha (2019)
Product Beef muscle Orange juice
Table 6. Effect of Ohmic heating on the counts of L. monocytogenes in food products Ohmic heating conditions Initial Microbial Reduction, count, log Others Frequency, kHz T, °C Time, Rate, V/cm log(CFU/ml) (CFU/ml) min th:3.5, 6,8.5, 13.5 72 3.5 3.83, 5.39, 7.05, 7.05 0.001-10000
95
4
50 50
1
6 6
1 Milk
60
Salsa
2 1
Orange juice
50
12.1
Reference Zell et al, 2010
7.05
th:0
0.9, 0.5, 0.2
pH:2.5, 3.5, 4.5
2.4,0.9,0.7
pH:2.5, 3.5, 4.5
3.3, 3, 2.95, 2.2
Fat %: 0, 3, 7, 10
2, 5
, +1.3mM carvacrol extract
*
Lee, Kim et al. (2015)
* *
Kim and Kang (2015) *
*
2
9.6
1.9,0.73, 0.59, 0.43, 0.11
pH: 2.5, 3, 3.5, 4, 4.5
1
25.6
4.4, 3.4, 1.8, 4.3, >4.5
pH: 2.5, 3, 3.5, 4, 4.5 *
, + carvone, + eugenol, + citral, + thymol (1mM extract) * , + carvone, + eugenol, + citral, + thymol (1mM extract)
Kim and Kang (2017)
Park, Ha et al. (2017)
13.3
5-6
1.2, 1.8, 2.2, 5.8, 5.5
Salsa
11.5
5-6
0.6, 1.9, 2.8, 3.2, 4.3
0.167
30
5-6
0.07, 0.04, 0.43, 0.21, 0.34
Brix:18, 24, 36, 48, 72
0.33
30
0.04, 0.13, 0.42, 0.36, 0.32
"
0.167
60
0.66, 0.50, 1.46, 0.57, 0.31
"
0.33
60
5.94, 5.83, 5.71, 5.71, 0.23
"
Buffered PW Tomato juice *
0.06, 0.2, 0.5, 1
9.43–12.14
6
3.58, 3.62, 3.34, 3.97 2.87, 2.87, 3.41, 3.41
The results are derived from graphs and the numbers are approximate. th: holding time, min. PW: peptone water
48
Kim and Kang (2015)
*
Buffered PW
Apple juice
Kim and Kang (2017)
Kim, Park et al. (2018)
Table 7. The effect of ozone treatment on the counts of L. monocytogenes in food products Ozone treatment conditions Product
Flow rate/ Conc.
Time
Apple juice
1.67, 15, 58.5, 928 mg/min
Raw chicken
33 mg/min
Apple juice
6-9 mg/min
Lettuce/spinach/parsley Fresh-cut bell pepper Mushroom
950 µL/L 9 ppm 2.8 mg/L 5.3 mg/L 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2
5.70, 6.02, 5.49, 4.55 min 9.21, 8.06, 5.49, 4.96 min 3224e4, 2247, 1616, 597 5s 6s 7s 8s 9s 20 s 40 s 40 s 20 min 0.5, 3, 6 24 h 30, 45, 60 min 30, 45, 60 min 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 5 min 10 min
Baby-cut carrots
Lowbush blueberries
Beefsteak tomatoes
Fresh brine (9% NaCl)
Initial count, log(CFU/ml)
4.92, 5.04, 6.30
5–6
6.59 5.1 5.1
Microbial reduction, log(CFU/ml) 5 5 5 1.84, 1.57, 2.82 2.35, 2.27, 3.26 ND, 0, 3.37 ND, ND, 3.62 ND, ND, ND 0.1, 2.5 0.2, 3.5 0.4, 3.7 1.16 2.3, 2.5, 3, 3 0.3, 1.1, 1.9 0.6, 1.6, 2.6 0.3, 0.4 0.8, 0.8 2, 2.5 5, 5.5 0.3, 0.6 1.2, 1.8 0.9, 1.0 2.1, 2.1 0.4, 0.5 0.6, 1.1 5.7, 7.0 6.0, 7.1 5.94, 7.33 >7.83, >9.0
Others
Reference
Brix 18 Brix 36 Brix 72 td:30s, 45s, 60s
Choi, Liu et al. (2012)
at 25, 55 °C
# *
Muthukumar and Muthuchamy (2013)
Sung, Song et al. (2014)
Karaca and Velioglu (2014) Alwi and Ali (2014) Akata, Torlak et al. (2015) Bridges, Rane et al. (2018)
+ 5, 10 min UV + 5, 10 min UV
Kumar et al, 2019
*: the results are received from graphs and the numbers are approximately; #: in this study, Listeria innocua has been used, td: dipping time in deionized water (s) before ozone treatment. Conc.: concentration
49
Table 8. The effect of cold plasma treatment on the counts of L. monocytogenes in food products Treatment conditions Product
Voltage, kV
frequency, kHz
Time, min
Electrode Material
Dist., cm
Saline Solution
13.8
46 kHz
60, 40
Silver/Brass/ Steel/Glass
2.4
Pork
20
58
2
Tomato- Surface Tomato-Stem Scar Spinach Cantaloupe Agar Plate Ham Onion Flakes Peptone water
17 " " " 6.4,6.4 10 9 7
-
45 s* " " " 10, 20 20 5, 5, 20 4
#
10 2 15, 35, 15
Initial count, log(CFU/ml) 9.2
2.5 -
Indirect
Steel mesh
Indirect
Quartz Copper
Floated
1, 3, 7
: in this study, Listeria innocua has been used. * Plus 30 min dwell. Dist.: Distance from actuator
50
Microbial reduction, log(CFU/ml) >7,~4 1
6.2-6.5 " " " 7 3.8 6.2 5- 6
6 1.3 4 3 4.2, 4.4 0.91 <0.6, 0.2, 1.1 <4.5, <2.5, <0.5
Reference Ragni, Berardinelli et al. # (2016) Choi, Puligundla et al. (2016) Jiang, Sokorai et al. (2017)
Sant'Ana, Lis et al. (2018) Kim and Min (2018) Timmons, Pai et al. (2018)
Product
Voltage, kV/cm
Milk
23
Apple juice
20
Orange juice Watermelon juice Blueberry
20 20 2
Milk Water
Table 9. The effect of pulse electric fields (PEF) on the counts of L. monocytogenes in food products PEF treatment conditions Initial Microbial Reduction, counts, Others T, °C Energy, kJ/kg Time log(CFU/ml) log(CFU/ml) *, # 0.101 ms 10 0.6, 2.8, >5 Ti: 4, 50, 55 56 75 2.2 pH 3.5 56
75
56
75 2, 4 min
30 10, 20, 30
0.6 ms 500, 20, 0.64 ms
7 9.5
1 0.2 2.3, 2.6
pH 3.7 pH 5.3
4.9-5.3 1.0, 2.4, 2.1
*, #
10 kV
*, #
100, 80
5.7, 3
Ti: 20, 40, pH: 4
Whey protein 2%
160, 125
1.5,1
Ti: 20,30, pH: 7
Whey protein 10%
160, 120
5.2,2.3
Ti: 20, 30, pH: 4
Whey protein 10%
160,120
1,0.9
Ti: 20,30, pH: 7
: in this study, Listeria innocua has been used. Ti: Inlet temperature, °C.
51
Sharma, Bremer et al. (2014) Timmermans, Groot et al. (2014)
Jin, Yu et al. (2017)
Whey protein 2%
#
Reference
Zhao, Zhang et al. (2017) Pyatkovskyy, Shynkaryk et al. (2018) Schottroff, Gratz et al. (2019)
Technology
HPP
Ultrasound
PEF
Heat
Fundament
High Pressure
Sonoporationt
Transmembrane potential
Energy-t
Mechanism of microbial inactivation
protein denaturation
Cavitation
Electroporation
Physical stress
Principle of microbial inactivation
cell membrane disruption
damaging DNA Cell explosion DNA damage
Membrane permealization
DNA synthesis inhibition
Ribosome
Cell wall disruption
Bacteria Response
Biofilm formation Genetic Diversity Stress resistance
Protein
Principle of microbial inactivation
damaging DNA
Membrane permealization
cell membrane disruption
cell membrane disruption
Mechanism of microbial inactivation
Inactivating cell replicationt
Plasma species on membrane
Pore formation
Free radicals
Fundament
Wave emission
Reactive compounds
Electroporation
Reactive compounds
Technology
Irradiation
Cold plasma
Ohmic
Ozone
Fig. 1. The inactivation mechanism of microorganisms in non-conventional processing technologies. 1
Non treated food characteristics:
Treatment condition:
PrePre-treatment characteristics
Strength(dose) of treatment
Composition and ingredients, importantly:
Type and procedure of treatment Time
Water content Antibacterial compound(s) Status of foods (liquid or solid)
Temperature Being used alone or as a hurdle
Expectations for processed foods:
Target bacterium characteristics:
Type of packaging
General resistance to treatment
ShelfShelf-life
Initial count
Quality and organoleptic characteristics
Interaction with other bacteria
Associated required regulations
Mechanisms for treatment resistance:
Consumer’ Consumer’s demands and attitudes
Genetic diversity
Fig. 2. The parameters which should be considered for optimization of non-conventional processing technologies
2
Highlights:
• • • •
Efficiency of novel food processes to inactivate L. monocytogenes was reviewed. High pressure pasteurization, sonication, and irradiation are efficient to destroy LMONO LMONO is a good indicator for examining the efficiency of sterilization technologies. Food composition, process type, and resistance of LMONO strains are important factors.
S0924-2244(19)30392-9
DOI:
https://doi.org/10.1016/j.tifs.2019.12.009
Reference:
TIFS 2680
To appear in:
Trends in Food Science & Technology
Received Date: 17 May 2019 Revised Date:
23 October 2019
Accepted Date: 9 December 2019
Please cite this article as: Bahrami, A., Baboli, Z.M., Schimmel, K., Williams, L., Jafari, S.M., Efficiency of non-conventional processing technologies for the control of Listeria monocytogenes in food products, Trends in Food Science & Technology (2020), doi: https://doi.org/10.1016/j.tifs.2019.12.009. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.
The most studied novel processing technologies to control Listeria monocytogenes in foods
1
Efficiency of non-conventional processing technologies for the control of Listeria
2
monocytogenes in food products
3
Running title: Control of L. monocytogenes in food products
4
Akbar Bahrami1, Zahra Moaddabdoost Baboli1, Keith Schimmel2, Leonard Williams3*, Seid
5
Mahdi Jafari4*
6
1
Program of Applied Science and Technology, Center for Excellence in Post-Harvest Technologies, North
7
Carolina Agricultural and Technical State University, North Carolina Research Campus, Kannapolis, NC
8
28081, USA
9
2
10 11
1601 East Market Street, Greensboro, NC 27411, USA 3
12 13 14
Program of Applied Science and Technology, North Carolina Agricultural and Technical State University,
Center for Excellence in Post-Harvest Technologies, North Carolina Agricultural and Technical State University, North Carolina Research Campus, Kannapolis, NC 28081, USA
4
Department of Food Materials and Process Design Engineering, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
15
*Corresponding authors: L. Williams, Tel (704) 250-5700, Email: [email protected];
16
S.M. Jafari, Tel./fax: +98 17 32426432, Email: [email protected]
17
Abstract
18
Background: Commercial heat sterilization has been used in the food industry for decades to produce safe
19
foods. However, this technology can have potential detrimental effects on the organoleptic and nutritional
20
quality of foods; so numerous innovative technologies have been developed to destroy pathogens potentially
21
present in foods as well as maintaining the sensory properties. Among pathogenic bacteria, L.
22
monocytogenes is of great importance for optimization of advanced technologies.
23
Scope and approach: It is estimated that L. monocytogenes alone is globally responsible for 23,150
24
sicknesses and 5463 deaths per year and its inactivation is vital for ensuring microbiologically safe food
25
products. In addition, its high resistance to most processes, compared to other pathogenic bacteria has made
26
L. monocytogenes to be one of good indicators for examining the efficiency of food processing technologies.
27
This review focuses on the efficiency of mild food processing technologies and their antimicrobial
28
mechanisms to inactivate L. monocytogenes.
29
Key findings and conclusions: Non-conventional technologies of high hydrostatic pressure, ultrasound, and
30
microwave can be considered as efficient as commercial sterilization methods in destroying L.
31
monocytogenes and potentially other foodborne pathogens. The composition and characteristics of foods,
32
processing conditions, and the resistance of L. monocytogenes (in species level) against the processing are
33
among diverse determining factors affecting the efficiency of these advanced processes. This study provides
34
a comprehensive summary on efficiency of newer technologies to conventional heating which could be
35
helpful for industries as well as researchers to select the best applicable treatment for food product.
36
Keywords: Food processing; Listeria monocytogenes; Pathogenic bacteria; Food safety; New processes. 1
37
1. Introduction
38
L. monocytogenes, the cause of listeriosis, is an important pathogen having a mortality rate of up
39
to 30%, is a Gram positive psychrotrophic bacterium which is the only pathogenic species for
40
human among six species belonging to Listeria spp. (Benlloch-Tinoco, Pina-Perez et al. 2014). The
41
gastroenteritis, meningitis, and septicemia have reported as the main clinical manifestation of L.
42
monocytogenes. Tracking associated outbreaks to L. monocytogenes and its shown capacity to resist
43
harsh processing conditions such as high and cold temperatures, modified atmosphere, and even
44
establishment in food processing environments, indicates potential continuous contamination of
45
foods by L. monocytogenes during processing and post-processing (Magalhães, Ferreira et al. 2016).
46
Conventional thermal processing has been used for a long time to provide stable and safe food
47
products. However, from researcher’s perspective, conventional thermal treatments are not
48
considered as the preferred solution anymore, mainly due to their significant impact on the loss of
49
sensory and nutritious quality of final foods. In this regard, food products that contain chemical
50
preservatives are rejected by consumers as well.
51
This approach has resulted in the introduction of new decontamination processing methods such
52
as high-hydrostatic pressure, sonication, microwave, irradiation, ohmic heating, ozonation, pulsed
53
electric fields, and cold plasma. These technologies not only have presented the capacity to meet the
54
requirements of commercial sterilization techniques to be used in food processing, they may also
55
efficiently bring the merit of keeping the nutritional and sensorial properties of food products better
56
than conventional thermal processing. L. monocytogenes was selected as the focus of this study to
57
assess the efficacy of new food processing technologies due to its high resistance to food processing
58
(compared with other pathogenic bacteria) and its high virulence capacity based on a
59
comprehensive literature review and database research (Pilevar, Hosseini et al. 2019). For example,
60
according to many studies and researches for food outbreaks, related to pathogenic bacteria hazards,
61
and their resistance level against pasteurization in milk products, L. monocytogenes, has been
62
selected and declared as the target pathogen to be controlled in the sterilization process of several 2
63
dairy foods (EuropeanCommission 2016, Ukuku, Onwulata et al. 2017, Schottroff, Gratz et al.
64
2019). Similarly, L. monocytogenes was declared as one of main target microorganisms for the
65
microbiological safety of cooked ready to eat meat products (Teixeira, Repkova et al. 2018).
66
Therefore, due to such considerations, outlooks, and because of the generally higher resistant level
67
of Gram positive bacteria to sterilization processing, inactivation of L. monocytogenes in food
68
products through different advanced technologies was studied. The successful inactivation of L.
69
monocytogenes by employing any new method can indicate its high potential in inactivation of all
70
other pathogenic bacteria. This review provides essential information on comparing the efficiency
71
of non-conventional food processing methods and presents a comprehensive source for food
72
industries to select the best applicable method for their specific product.
73
2. Conventional thermal treatment to reduce L. monocytogenes in foods
74
Thermal processing as a principal and traditional method for inactivation of microorganisms is
75
still the most common treatment for pasteurization and elimination of foodborne pathogens as well
76
as spoilage microorganisms in food products. But heat can adversely affect the quality of food and
77
degrade the nutritional value of the product (Tafti, Peighambardoust et al. 2013, Tafti, Peighardoust
78
et al. 2013). Moreover, mild thermal processing can sub-lethally injure the bacteria, which may
79
allow them to recover and grow during storage. This is the main concern to the safety of thermal
80
processed food (Wang, Uyttendaele et al. 2016). The time needed to reduce the microbial
81
concentration by one log is known as D-value, which shows the thermal resistance of bacteria and it
82
can be derived from bacteria survival curve during treatment. That is because log-linear method has
83
been considered as the easiest method for fitting and predicting the microorganism behavior under
84
thermal treatment (Dufort, Sogin et al. 2017, Wang, Devlieghere et al. 2017, Taylor, Tsai et al.
85
2018), although log-linear always is not the best fit (Rachon, Penaloza et al. 2016).
86
Shell and tube or plate heat exchangers, hot water bath, and direct hot steam/air are usually used
87
for thermal processes (Taylor, Tsai et al. 2018). In conventional thermal treating, heat transfers into
88
the product via convection and conduction, therefore, there is a time lag, called come-up time, for 3
89
products to reach the target temperature (Delgado Suárez, Chairéz Espinosa et al. 2015, Rachon,
90
Penaloza et al. 2016). The come-up time depends on the heating rate and heat transfer
91
characteristics of products (Jafari, Jabari et al. 2017, Jafari, Saramnejad et al. 2018). The difference
92
between temperature set-point and actual temperature of the products can be the main reason for
93
failure of microbial inactivation by mild heat treatment (Benlloch-Tinoco, Igual et al. 2015).
94
Table 1 presents a summary of recent studies on applying conventional heat treatment for
95
inactivating Listeria spp. As for modeling the survival curves, Rachon, Penaloza et al. (2016)
96
indicated that at higher temperatures, the microbial curves showed non-linearity especially when
97
come-up time can cause microbial inactivation. In their study, Weibull model was considered as an
98
appropriate fitting. The works conducted on wheat (Taylor, Tsai et al. 2018) and tomato puree
99
(Dufort, Sogin et al. 2017) at lower temperatures, showed that log-linear model can provide a
100
precise fitting. However, Wang, Devlieghere et al. (2017) mentioned that when inactivation curves
101
were obtained from non-selective media, inactivation curve depicted a shoulder, which indicated the
102
nonlinearity of the curve. [Table 1]
103 104
L. monocytogenes has adaptation ability to the environmental stresses which can enhance its
105
resistance to heat treatment (Aryani, den Besten et al. 2015). Decreasing water activity (Taylor, Tsai
106
et al. 2018), increasing salt content (Poimenidou, Chatzithoma et al. 2016, Wang, Uyttendaele et al.
107
2016, Li, Huang et al. 2017), decreasing fat and fiber content (Mate, Periago et al. 2017), higher
108
acidity (Aryani, den Besten et al. 2015, Dufort, Sogin et al. 2017) can enhance the heat resistance of
109
L. monocytogenes due to adaptive response to stress and starvation and result in cross protection
110
(Aryani, den Besten et al. 2015, Poimenidou, Chatzithoma et al. 2016). Increase in heat tolerance of
111
L. monocytogenes was related to upregulation of genes and their recovery levels (Omori, Miake et
112
al. 2017). Omori, Miake et al. (2017) suggested ClpE, ClpB as genes associated with enhanced heat
113
resistance of some L. monocytogenes strains while Pontinen, Aalto-Araneda et al. (2017) mentioned
114
ClpL as a potential predictor for that purpose. 4
115
As for different strains, Aryani, den Besten et al. (2015) determined that among 20 different
116
strains of L. monocytogenes, isolated from different sources, the most thermal resistant strain had a
117
D60 = 4.1 in the range of 55-65 °C and also indicated that for all strains, cells in exponential phase
118
were much less heat resistant compared to stationary phase. Meanwhile, some other studies have
119
shown that the heat tolerance of strains is dependent on the heating temperature (Monu, Valladares
120
et al. 2015, Li, Huang et al. 2017). Monu, Valladares et al. (2015) showed that among five strains of
121
L. monocytogenes studied in their work, L. monocytogenes Scott A presented the lowest D value at
122
lower temperatures, 56°C (D56 = 2.69), and the highest D value, at higher temperature of 60 °C (D60
123
= 0.66) was obtained for this strain. Investigating on the sub-lethal effect of thermal inactivation,
124
Wang, Devlieghere et al. (2017) demonstrated that the portion of sub-lethal injury was increased at
125
higher temperatures and times, and also the cells treated on agar surface were more resistant that
126
those in broth.
127 128
3. New strategies to control the growth of L. monocytogenes in food products To enhance the safety and shelf-life of food products, the use of non-thermal treatments that
129
do not increase the temperature of food products for bacterial inactivation, instead other
130
mechanisms are engaged, is receiving attention. These technologies are applied mainly to reduce
131
the total microbial population, and to destroy pathogenic bacteria such as L. monocytogenes
132
potentially present in food products. The non-thermal strategies can be used before packaging or in
133
post packaging step based on the nature of technology. Although the use of these technologies do
134
not involve heating of foods, they should have the capacity to provide lethality of the target
135
microbes, as well as preserving sensory properties, nutritional, and functional characteristics of food
136
products (Mahdi Jafari, Masoudi et al. 2019, Pilevar, Bahrami et al. 2019). The mechanism of
137
microbial inactivation of newer processing technologies is presented in Fig. 1. For applying
138
optimum conditions of a specific processing technology in terms of safety and quality of foods,
139
diverse parameters should be countered (Fig. 2) which will be covered throughout the manuscript.
140
Such treatments should not have negative impacts on the barrier features of the packaging if they 5
141
are used in post-packaging step. However, the possibility of commercial use of a post-packaging
142
decontamination technology, beside its effectiveness also depends greatly on its installation and
143
maintenances costs. In the following subsections, these non-conventional technologies and their
144
influence on L. monocytogenes will be discussed.
145
Fig. 1
146
Fig. 2
147
3.1.
High Hydrostatic Pressure (HHP) processing
148
The variations in the pressure (a thermodynamic property of physical systems such as
149
biological systems), can be associated with the lower degree of negative effects in use of other
150
property, temperature, which has been commonly used. That was shown that by controlling
151
pressure, we can induce significant impacts on diverse systems. The major and progressively
152
increasing use of HPP in food industries, has been its application as the non-thermal pasteurization
153
of food products, which can enhance the shelf-life of foods, without imposing significant
154
modification in their nutritional, functional and sensory characteristics as it is applied at room
155
temperatures (Zhao, Zhang et al. 2017). HHP processing is performed through applying pressures
156
above 100 MPa to the product through mechanically pressurized liquids, usually water. The
157
behavior of food product changes based on the Le Chatelier’s principle as applying pressure causes
158
a shift in the system equilibrium toward occupying smallest volumes, and in microscopic scale, at
159
constant temperature, it increases the degree of ordering molecules of a given substance. In
160
addition, the pressure is exerted instantly and uniformly throughout the product independent of its
161
size and geometry (Zacconi, Giosue et al. 2015).
162
Effects of HHP on inactivating L. monocytogenes depends on the processing parameters such as
163
applied pressure (Huang, Lung et al. 2015, Zacconi, Giosue et al. 2015, Mukhopadhyay, Sokorai et
164
al. 2016, Kaur and Rao 2017, Liu, Li et al. 2017), temperature (Pinho, Oliveira et al. 2015, Ates,
165
Rode et al. 2016, Mukhopadhyay, Sokorai et al. 2016) and holding time (Mukhopadhyay, Sokorai
166
et al. 2016, Liu, Li et al. 2017, Alcantara-Zayala, Serment-Moreno et al. 2018), composition and 6
167
properties of the matrix such as pH and water activity (Bover-Cid, Belletti et al. 2015, Stratakos,
168
Linton et al. 2016, Rubio, Possas et al. 2018) and the sensitivity of L. monocytogenes strain (Evert-
169
Arriagada, Trujillo et al. 2018). The mechanism of microbial inactivation by HHP consists of
170
unfolding the protein structure, denaturing cell membrane, changing the fluidity in cell membrane,
171
loss of intracellular pH and membrane integrity, and eventually cell disruption. Pressure also causes
172
dissociation of the microorganism ribosomes and limits cell viability (Georget, Sevenich et al. 2015,
173
Lung, Cheng et al. 2015). Depending on the conditions, HHP might not always lead to cell death
174
and may just sub-lethally damage it. Therefore, during storage period, bacteria may repair the
175
injuries and get recovered, especially if the treatment was not severe enough or the storage went
176
under abuse temperature (Li and Ganzle 2016, Lebow, DesRocher et al. 2017, Balamurugan,
177
Inmanee et al. 2018, Misiou, van Nassau et al. 2018).
178
Table 2 provides a summary of studies conducted on inactivation of L. monocytogenes by
179
HHP in different products with or without any additives from 2015 to 2018. In general, HHP is
180
more successful in culture media and liquid foods than solid ones (Bover-Cid, Belletti et al. 2015);
181
under pressures more than 600 MPa and temperatures higher than 40 °C, the rate of sub-lethal
182
damages decreases to more lethal ones (Ates, Rode et al. 2017). The sub-lethal injury has been
183
determined by comparing the difference in viable count of L. monocytogenes population on
184
selective and non-selective media (Ates, Rode et al. 2016, Balamurugan, Inmanee et al. 2018). The
185
cell morphology analysis of L. monocytogenes depicted that HHP caused external changes to
186
cellular structures (Huang, Lung et al. 2015, Liu, Li et al. 2017) and fluorescence micrograph
187
indicated the membrane damage as well as intercellular release especially at pressures higher than
188
400 MPa (Huang, Lung et al. 2015, Scolari, Zacconi et al. 2015). However, HHP might not
189
consistently satisfy in meeting FDA requirement for 5-log reduction of pathogenic bacteria,
190
especially in ready to eat products; so combining other hurdles for microbial growth can assure
191
sufficient reduction and extend the shelf-life. For example, increasing temperature and addition of
192
natural antimicrobials are some of those hurdles (Ahmed, Mulla et al. 2017, Lebow, DesRocher et 7
193
al. 2017, Liu, Li et al. 2017, Castro, Silva et al. 2018, Misiou, van Nassau et al. 2018, Teixeira,
194
Repkova et al. 2018).
195
[Table 2]
196
In products such as smoothie (Scolari, Zacconi et al. 2015, Ates, Rode et al. 2016), fruit
197
puree (Blazquez, Burgos et al. 2017), milk (Huang, Lung et al. 2015, Liu, Li et al. 2017, Misiou,
198
van Nassau et al. 2018), cantaloupe puree (Mukhopadhyay, Sokorai et al. 2016), and soup (Ates,
199
Rode et al. 2016), application of 300-500 MPa for 5 min resulted in a 5-log reduction in population
200
of Listeria spp. in water or buffer solution (Pyatkovskyy, Shynkaryk et al. 2018). However, for
201
chorizo sausage (Rubio, Possas et al. 2018), shrimp (Kaur and Rao 2017), and salmon products
202
(Lebow, DesRocher et al. 2017, Misiou, van Nassau et al. 2018), even pressures higher than 500
203
MPa or longer holding times did not cause sufficient bacterial reduction.
204
In some cases, although the initial reduction in number of L. monocytogenes right after
205
treatment were 5-log or more, during storage a number of surviving cell grew and their count
206
reached to higher than the acceptance limit, in some products such as milk (Liu, Li et al. 2017,
207
Misiou, van Nassau et al. 2018), cheese (Evert-Arriagada, Trujillo et al. 2018), cooked sausage
208
(Balamurugan, Inmanee et al. 2018), and cured meat (Valdramidis, Patterson et al. 2015), which
209
indicated a high number of cells were sub-lethally damaged than being completely inactivated.
210
3.2.
Ultrasound processing
211
Ultrasound technology which is composed of sound waves with frequency beyond the limit
212
of human hearing (20 kHz), due to being relatively cheap, simple and energy saving, is introduced
213
as an emerging technology for processing food products. Ultrasound is being progressively applied
214
in diverse processes such as homogenization, emulsification, extraction, crystallization, cutting,
215
hydrolysis, and microbial inactivation. For example, while, low power ultrasound can be used for
216
physicochemical characterization of food ingredients, high power ultrasound through cavitation can
217
induce diverse physical and chemical/ biochemical changes during food processing. In most cases,
218
the ultrasonic source consists essentially of a plane surface oscillating with simple harmonic motion 8
219
at a single frequency, like a piston in the cylinder of an engine but at a much smaller amplitude and
220
at much higher frequency (Jamalabadi, Saremnezhad et al. , Anese, Maifreni et al. 2015, Gabriel
221
2015). Ultrasound treatments can be classified by their frequency ranges to power ultrasound (16-
222
100 kHz), high-frequency ultrasound (100 kHz -1 MHz), and diagnostic ultrasound (1-10 MHz)
223
(Luo and Oh 2016, Ozcan and Demirel Zorba 2016).
224
The mechanism of ultrasound in inactivation of microorganism is associated with a
225
phenomena called cavitation (Gabriel 2014, Hamann, Tonkiel et al. 2018) , which means formation,
226
growth, and collapse of microbubbles within an aqueous solution (Jamalabadi, Saremnezhad et al.).
227
Over a number of acoustic cycles, the bubbles grow until they reach a critical size, where the
228
ultrasonic energy fails to retain the increasing vapor phase in the bubble; so bubbles become
229
unstable and collapse violently results in creating shock waves with a huge amount of energy
230
(Gabriel 2014). Cavitation can cause severe damage to the cell walls, pit on their surface, erode
231
them and result in microbial inactivation. Under the localized extreme temperature conditions
232
generated by cavitation, the water molecules dissociate to free radicals including hydroxyl and
233
hydrogen. The free radicals may cause DNA damage, disrupt enzymatic activity and damage
234
liposomes and cell membrane by disrupting the structural and functional components up to cell lysis
235
(Gabriel 2014). The radicals formed in this reaction are also highly reactive and responsible for a
236
chemical reaction by ultrasonic irradiation (Anese, Maifreni et al. 2015). During the high-frequency
237
sonication, the number of cavitation events is more, compared to low-frequency, but with smaller
238
bubbles, so the micro-stream has not enough energy for the physical force but the total energy
239
release is sufficient to break the chemical bonds of water molecules (Lee, Kim et al. 2014, Franco-
240
Vega, Ramirez-Corona et al. 2015).
241
The lethal effect of ultrasound depends on the applied power per volume, frequency,
242
treatment time, temperature and geometry of reactor. Table 3 represents a summary of applying
243
ultrasound for inactivating L. monocytogenes in different food products. In general, based on
244
several studies, ultrasound was not successful to inactivate L. monocytogenes sufficiently unless 9
245
under mild temperatures (> 60 °C) (Anese, Maifreni et al. 2015, Franco-Vega, Ramirez-Corona et
246
al. 2015, Gabriel 2015) or by adding additives (Wu and Narsimhan 2017, Dolan, Bastarrachea et al.
247
2018). The efficiency of ultrasound on inactivation of L. monocytogenes is engaged with the
248
cavitation rate, so it is more effective in liquid media, such as juices (Gabriel 2014), broth (Franco-
249
Vega, Ramirez-Corona et al. 2015, Dolan, Bastarrachea et al. 2018), or milk (Gabriel 2015) , but it
250
has a limitation for pre-packaged foods. Moreover, since cavitation happens at a high-pressure zone,
251
the geometry and volume of reactor play important roles.
252
[Table 3]
253
As Table 3 shows, recently researchers are focusing on potential of ultrasound for
254
decontamination of fresh or ready-to-eat products. In the studies on disinfecting lettuce or the water
255
for removing Listeria spp. through use of bath ultrasound reactor, sonication could not inactivate
256
the microbial content more than 2.5 logs (Lee, Kim et al. 2014), even in the present of additives
257
such as peroxyacetic acid (Gómez-López, Gil et al. 2015) or Tween-20 and sodium dodecyl sulfate
258
(SDS) (Huang, Wrenn et al. 2018). Only Anese, Maifreni et al. (2015) showed that under
259
uncontrolled continuous sonication, L. monocytogenes count in wastewater of fresh-cut lettuce
260
reduced by 5-log for samples treated for 5 min. In this study, the temperature increased
261
continuously and reached to 60° after 5 min.
262
Although the effect of additives such as cinnamon oil (Ozcan and Demirel Zorba 2016,
263
Park, Kang et al. 2018), SDS, peroxyacetic acid, or benzalkonium chloride did not improve the
264
lethal effect of ultrasound on L. monocytogenes, peracetic acid (Hamann, Tonkiel et al. 2018),
265
antimicrobial peptide (Wu and Narsimhan 2017), or zinc oxide (Dolan, Bastarrachea et al. 2018)
266
had sufficient synergic effects with ultrasound depending on the concentration used.
267
Although ultrasound has shown capacity to bring beneficial modifications in different
268
aspects including pasteurization, the physicochemical impacts of ultrasound processing might also
269
cause food quality problems by making off-flavors, variations in physical parameters and
270
decomposition of compounds. For example, cavitation can produce radicals in liquid mediums that 10
271
can be cause of initiating the degradation of products as well trigger the radical chain reactions and
272
make significant quality defects in food products (Pingret, Fabiano-Tixier et al. 2013).
273
3.3.
Microwave heating
274
Microwave heating has shown a widespread application in the food sector such as cooking,
275
drying, pasteurization and preservation of food compounds. Microwave affects the dipolar and ionic
276
components of foods by exposing to oscillating electric field at frequencies of 915 or 2450 MHz
277
(Sung and Kang 2014, Benlloch-Tinoco, Igual et al. 2015). Microwave is providing several
278
advantages such as rapid heating rate (Siguemoto, Gut et al. 2018), faster heat penetration, energy
279
savings (due to volumetric heating) and reduced processing cost and time. Microwave sterilization
280
can effectively reduce the potential pathogens counts in foods, as well can inactivate the enzyme,
281
thus, preserves the nutritional properties of foods (Chen, Li et al. 2017). There are some studies
282
emphasizing on non-thermal effects of microwave radiation as well (Kim, Park et al. 2018). Despite
283
those advantages, there is a major problem with microwave heating which is related to the non-
284
uniform heat distribution as it affects microbiological safety (Kim, Sung et al. 2016). Hamoud-
285
Agha, Curet et al. (2014) conducted numerical investigation on 915 MHz microwave heating by
286
applying finite element methods and showed the surface layers of products loss heat due to
287
convection to the surrounding environment. Therefore, microwave heating leaves cold spots and hot
288
spots on the products. Kim, Sung et al. (2016) showed that the side temperature of tomato paste can
289
be 37-43°C, while the center has the temperature of 80 °C. In addition, microwave heating like
290
conventional heating can result in moisture loss. However, the solid-state power sources as a viable
291
alternative to magnetrons have shown a capacity for decreasing the problem of cold spots (Atuonwu
292
and Tassou 2018).
293
In general, the microbial inactivation efficiency of microwave heating depends on the
294
applied power, frequency of electric field, treatment time, as well as geometry and dielectric
295
properties of the product. Unfortunately, the number of studies on this subject is limited. Table 4
296
provides a summary of studies on microwave heating for inactivation of L. monocytogenes. By 11
297
using domestic microwave ovens with frequency of 2450 MHz, a 5-log microbial reduction was
298
met at high powers, 900-1100 W, after 75 s for Frankfurter sausage, 82 s for kiwi puree, 50 s for
299
chicken meat (Zeinali, Jamshidi et al. 2015), 120 s for chicory stem (Renna, Gonnella et al. 2017),
300
and 130 s for apple juice (Siguemoto, Gut et al. 2018). Microwave devices with a lower frequency,
301
915 KHz, are mainly used for industrial equipment (Sung and Kang 2014) and need power more
302
than 1500 W for sufficient microbial inactivation (Sung and Kang 2014, Kim, Park et al. 2018).
303
[Table 4]
304
Salt, sugar and moisture content affect the dielectric properties of the product and in turn,
305
affect the microwave heating efficiency. Song and Kang (2016) showed that water activity had a
306
direct influence on the reduction of L. monocytogenes and Kim, Park et al. (2018) demonstrated that
307
that lower sugar content of chili sauce can reduce the treatment time.
308
The geometry of product is also important since microwave heating concentrates more around the
309
geometric center of products, so it might leave focused effects on products (especially for round
310
shape foods) and make damages on the texture or quality of foods (Song and Kang 2016). That is
311
why there is a controversial dispute over the favorable effects of microwave on quality properties of
312
foods. Therefore, optimization of treatment conditions is of great importance for using microwave
313
technology. That might be the reason “smart” oven was suggested to be a solution, which still
314
requires more study.
315 316
3.4.
Irradiation
Food irradiation has received much attention as an established technology in the food sector for
317
enhancing the safety and quality of food products. While the use of irradiation in food sector is very
318
diverse, inhibition of sprouting, insect and parasite disinfestation, shelf-life extension, and
319
destroying non-spore forming pathogens are the most commonly applications of irradiation in the
320
food industry (Farkas and Mohácsi-Farkas 2011). Irradiation, a non-thermal technology, is defined
321
as the application of ionizing radiation in small doses and can be used as a decontaminant
322
technology, to enhance the safety and shelf-life of foods (Birmpa, Sfika et al. 2013, Mikš-Krajnik, 12
323
James Feng et al. 2017). For example, it can be used for fresh meat to inactivate parasites, decrease
324
the pathogenic microorganisms in several foods, or impose insect disinfestation capacity in grains
325
and fruits (Birmpa, Sfika et al. 2013, Donsì, Marchese et al. 2015). UV light, γ, X, and α rays, and
326
electron beams are the most used irradiation techniques in industry. The term of ‘irradiation’ is most
327
often inferring to the γ-irradiation. It has been shown that the UV light as a disinfection choice in
328
food facilities, has a greater germicidal potential compared to the most known chemical compounds
329
such as chlorine and hydrogen peroxide with the optimal efficiency at 254 nm wavelength (Mikš-
330
Krajnik, James Feng et al. 2017).
331
The cobalt-60 (Co-60) is the main source of irradiation and the dose used in diverse treatments
332
varies based on the type of target food (Suklim, Flick et al. 2014) . The impact of ionizing radiation
333
on microorganisms in general, depends on several parameters such as the dose of treatment, the
334
dose and rate of absorption, and the environmental conditions (importantly temperature and gas
335
atmosphere). The mechanism of irradiation in inactivation of bacteria is mainly through damaging
336
their DNA that leads to the prevention of proliferation.
337
The results of use of irradiation in controlling L. monocytogenes in several foods is
338
presented in Table 5. A high reduction (greater than 6.65 and 7.56 logs) in L. monocytogenes counts
339
in blue swimming crab lump meat for the irradiation treatments of 4 and 6 kGy, respectively.
340
Irradiation at 1 and 2 kGy doses provided 2.10 and 5.35 logs reduction, respectively for L.
341
monocytogenes DMST 1783, and 1.56 and 4.19 logs for L. monocytogenes DMST 4553. In
342
addition, during 28 days storage of the product after irradiation, the recovery of injured L.
343
monocytogenes was observed (Suklim, Flick et al. 2014).
344
[Table 5]
345
The reductions of 2.0, 3.50, and 45.0 log CFU/g in L. monocytogenes population in the
346
dough subjected to the electron beam treatment at 1, 2, and 3 kGy, and 1.0 and 2.2 CFU/g for the
347
samples subjected to the gamma treatment at 1.5 and 2.5 kGy, respectively. The use of doses greater
348
than 3.0 kGy for both electron beam and gamma irradiation reduced L. monocytogenes counts to 13
349
below the detection limit (Jeong and Kang 2017). Treatment of sliced cheese at a dose of 0.2 and
350
0.4 kGy of X-ray irradiation resulted in 2.28 and 3.70 log reductions in L. monocytogenes and that
351
was reduced to the less than the detectable limit (< 0.7 CFU/g) for the samples subjected by 0.6 and
352
0.8 kGy treatments.
353
Ha & Kang (2018) used krypton-chlorine excilamp irradiator for inactivation of L. monocytogenes
354
in water (Ha and Kang 2018). Generally, at higher treatment times and initial population
355
inoculated, more reduction and less reduction, in L. monocytogenes count was found, respectively
356
(Table 5). In treatment of Tahini halva through gamma radiation, by increasing irradiation dose,
357
higher reductions of L. monocytogenes was found (Osaili, Al-Nabulsi et al. 2018).
358
In coconut water subjected to a continuous-flow UV irradiator, a linear trend was found for
359
inactivation of L. monocytogenes with increase in the UV dose (Bhullar, Patras et al. 2018).
360
Antimicrobial impacts of three different UV irradiations (A, B, and C) in two different buffer
361
solutions on L. monocytogenes were studied by Jeon and Ha (2018). The wavelength of UV light
362
that is commonly used in food industry ranges from 100 to 400 nm and the wavelength range of the
363
UV-C was 200–280 nm that had the highest efficiency in inactivation of bacteria and viruses,
364
compared to UV-A or UV-B. Therefore, although irradiation doses used in this study of Jeon and
365
Ha (2018) was UV-A> UV-B > UV-C, the efficiency in destroying L. monocytogenes was not in
366
this trend (Table 5) which could be due to the great differences in mechanism of three types of UV
367
(A, B, and C) against live microorganisms. The impact of irradiation and storage on the L.
368
monocytogenes and L.innocua counts in carrot and cut tomato has also been investigated and the
369
populations of both organisms decreased by at least 2 log10 at 1 kGy dose and no re-growth during
370
storage was observed (Mohácsi-Farkas, Nyirő-Fekete et al. 2014).
371
However, there is a controversial issue over radiation use -whether or not it may lead to the
372
formation of radioactivity in foods, resulting in the harmful impacts on the body - which has made a
373
significant limitation for irritation use, in spite of its advantages (Birmpa, Sfika et al. 2013, Xuan,
374
Ding et al. 2017). In this regard, the Codex Alimentarius Commission declared that the maximum 14
375
dose of irritation use is 10 kGy (Roberts 2014). In order to use irradiation for foods, the
376
transportation of final products to an irradiation unit sounds necessary which is another limiting
377
factor for using irradiation as a post-packaging technology (Parlato, Giacomarra et al. 2014). One of
378
other main drawbacks of irradiation to control pathogenic bacteria is its low penetrating power,
379
which provides a limited efficiency, especially on foods with irregular surfaces. Therefore, it has
380
been greatly proposed that irradiation combined with other technologies and methods can be a
381
practical choice to be used against pathogenic bacteria in foods.
382
Research studies are indicating that people are showing more tendency to accept irradiated
383
foods after receiving appropriate information regarding its safety and quality which has been a
384
challenge associated with the use of this technology in food sector.
385
3.5.
Ohmic heating
386
Ohmic heating is an innovative thermal technology which provides a fast and uniform
387
heating through employing electric current flowing into the target foods during diverse processes
388
such as drying, cooking, and sterilization. This technique due to showing capacities in terms of
389
reducing heat damage and nutrient loss compared to conventional thermal treatments has gained
390
much attention. The conversion of electrical energy into thermal energy is the main principle of
391
Ohmic technology. A critical aspect in using Ohmic technology is the direct contact of foods with
392
the electrodes. The migration of metal ions into foods with a toxic potential due to electrode
393
corrosion has been one of important obstacles of extensive use of Ohmic heating in the food
394
industry for many years (Kim and Kang 2015). However, nowadays the problem has been solved in
395
some degree by introducing the inert electrodes and pulse waveforms. It has been reported that the
396
pulsed Ohmic heating, has provided the possibility of inactivating foodborne pathogens without
397
making electrode corrosion in some foods (Kim, Choi et al. 2017). The major mechanism of Ohmic
398
heating for inactivation of microorganisms is through heating effects. However, some other
399
mechanisms such as pore formation (electroporation) in the cell membrane of microorganisms have
400
been reported (Park, Ha et al. 2017, Kim, Park et al. 2018). The electroporation can lead in cell 15
401
permeability and cause membrane disruption and finally lead to the cell death (Kim and Kang 2015,
402
Kim and Kang 2017), however, it seems that the whole mechanism of antimicrobial inactivation of
403
Ohmic is not still fully understood.
404
The advantages of Ohmic technology which is providing a uniform and rapid heating
405
throughout product volume, depends on the conductivity of target product, the configuration and
406
properties of treatment chamber, and the composition and flow characteristics of food. Another
407
important point in using this technology is the use of electrodes as heating source instead of
408
contacting foods with hot surfaces (such as some conventional thermal technologies) which
409
possibly plays an important preventive role in production of biological, organic or inorganic
410
unwanted layers during Ohmic heating (Kim and Kang 2015, Lee, Kim et al. 2015). In Ohmic
411
technology, the heating process can be significantly shortened which can result in a higher quality
412
of final food products, while maintaining the required sterilization impact. For research-based
413
fields, batch-type is commonly used and for industry sections, the continuous-type is more
414
promising.
415
The efficiency of Ohmic heating for inactivation of L. monocytogenes in diverse foods has
416
been studied extensively, as shown in Table 6. The results of several works have revealed that L.
417
monocytogenes is more resistant to Ohmic heating than other pathogenic bacteria. For example, the
418
population of mesophilic aerobic bacteria, mold-yeast, and Staphylococcus aureus was reduced
419
significantly and even Salmonella spp. was completely eliminated from meatballs samples, while
420
Ohmic heating was not able to inactivate all L. monocytogenes cells (Sengun, Yildiz Turp et al.
421
2014). Although, for most cases, the reduction of L. monocytogenes was similar for Ohmic and
422
conventional heating (for specific times and temperatures), since Ohmic processing was able to
423
increase the temperature more rapidly (than conventional), L. monocytogenes was inactivated more
424
effectively by Ohmic heating in the fixed treatment time intervals (Kim and Kang 2015).
425
[Table 6]
16
426
The higher temperature and time of treatment led to a higher reduction of L. monocytogenes
427
at any pH value for juice samples, without making negative effects (Lee, Kim et al. 2015). The
428
efficiency of continuous-type pulsed Ohmic in reducing the inoculated L. monocytogenes on
429
buffered peptone water (BPW) and tomato juice showed that Ohmic treatment parameters such as
430
flow rate, voltage, and initial temperature are determining factors affecting efficiency of
431
continuous-type Ohmic heating in inactivation of pathogens (Kim, Park et al. 2018). In addition,
432
using preheating could help inactivation of pathogens. A 5 log reductions of L. monocytogenes was
433
observed in treating tomato juice by Ohmic heating of 12.14Vrms/cm at 0.2 L/min flow rate of
434
preheated sample to 50 °C (Kim, Park et al. 2018).
435
Several studies have addressed the effect of food composition on the efficiency of Ohmic
436
heating in reducing pathogenic bacteria such as L. monocytogenes. For example, it was shown that
437
the milk fat and lactose have inhibitory impacts on the inactivation of L. monocytogenes by Ohmic
438
heating (Kim and Kang 2015, Lee, Kim et al. 2015, Kim, Jo et al. 2017). The higher heating rate in
439
milk samples with a lower fat content may be attributed to the higher electrical conductivity of these
440
products which indicates the possibility of non-uniform heating (Lee, Kim et al. 2015). Therefore,
441
for dairy foods, in specific the milk fat content and in general the food product composition should
442
be considered as a determining factor for assessing the efficiency of Ohmic heating for
443
pasteurization process. The sugar concentration (°Brix) of apple juice is an important factor for
444
optimization of Ohmic heating for pasteurization (Park, Ha et al. 2017). When, the voltage ranged
445
from 30 to 60 V/cm and 5 different °Brix (18 to 72) was used, the 72 °Brix juice showed the lowest
446
heating rate and considering the results of all experiments, the highest performance coefficients
447
were reported for two combinations of 30 V/cm in 36 °Brix and 60 V/cm in 48 °Brix. However, a 5-
448
log reduction of L. monocytogenes was observed for 60 s treatment (30 V/cm) of juice with 36
449
°Brix, but for the juice with 48 °Brix, the Ohmic heating for 20 s at 60 V/cm achieved this level of
450
reduction (Park, Ha et al. 2017). Therefore, for juices with different concentration of sugar, to reach
451
to the best choice of Ohmic heating condition, experiments and modeling efforts is needed. 17
452
While the conventional heating rate was not significantly affected by pH level and L.
453
monocytogenes was inactivated more effectively at lower pH (Kim and Kang 2015), different result
454
was reported for Ohmic heating (Table 6). Possibly due to the higher electrical conductivity at
455
higher pH, the rapid inactivation of L. monocytogenes was observed at pH= 4.5. Thus, the change of
456
pH level should be considered in optimizing pasteurization of orange juice through Ohmic heating
457
(Kim and Kang 2015). In another work, the low frequency (0.06- 1 kHz) pulsed Ohmic heating was
458
used to inactivate L. monocytogenes in BPW and tomato juice (Kim, Choi et al. 2017). The larger
459
reductions of L. monocytogenes in BPW than tomato juice was observed, which may be due to the
460
strong acid resistance of L. monocytogenes so that this has enabled it to survive under the conditions
461
of low pH of orange juice and the protection effect of food ingredients on L. monocytogenes against
462
treatment. Based on the lower numbers of propidium iodide uptake, indicating lower cell membrane
463
damage obtained for higher frequencies, the low frequency Ohmic treatment was recommended due
464
to the reduced resuscitation level than higher frequency treatments (Kim, Choi et al. 2017). The
465
effect of voltage gradients (30-60V/cm) of Ohmic heating and °Brix of apple juice (18-72) on L.
466
monocytogenes inactivation was investigated (Park, Ha et al. 2017). At all voltage levels, the 72
467
°Brix apple juice, showed the lowest heating rate. A 5-log reduction of L. monocytogenes was
468
achieved in 20 s treatment at 60 V/cm, for all °Brix samples, except 72 °Brix. Generally, it was
469
reported that the time duration required for 5-log reduction at 30 V/cm in 36 °Brix was about three
470
times longer than for 60 V/cm for all °Brix samples, except for 72 °Brix (Park, Ha et al. 2017).
471
The synergetic combination effect of Ohmic heating with various essential oils (carvone,
472
eugenol, thymol, and citral) for destroying L. monocytogenes in BPW and salsa has been studied as
473
well (Kim and Kang 2017). The combination of Ohmic heating with citral in BPW and with thymol
474
in salsa showed the most synergistic anti-Listerial effect (5.8 and 4.3 log CFU/ml reduction in L.
475
monocytogenes, respectively). Therefore, the combination of Ohmic heating and thymol treatment
476
was suggested for effective pasteurization of salsa (Kim and Kang 2017). The combination effect of
477
carvacrol and Ohmic heating for inactivation of L. monocytogenes in salsa showed a synergetic 18
478
effect after 30 and 40s treatment. While, the enumeration on resuscitation media after treatment
479
showed the inactivation of about 0.3 and 2 log for treatment by 1.3 mMol carvacrol and 12.1
480
Vms/cm Ohmic heating after 50s, respectively; the combination of them brought over 5 log
481
reduction in L. monocytogenes counts (Kim and Kang 2017).
482
3.6.
Ozonation
483
The use of ozone technology for decreasing the load of bacteria at surfaces in contact with
484
foods has attracted much attention recently. This technology involves the use of ozone or triatomic
485
oxygen (O3) which is an unstable allotrope of oxygen either in gaseous or dissolved form, to
486
decrease the load of target microorganisms in the food industry. The FDA approval of ozone as a
487
direct additive in food in 2001 triggered an increasing interest in ozone applications. Ozone has
488
shown a promising capacity to be considered as an alternative sanitizer for chlorine substances;
489
since during using ozone when it is liberating the principal product of oxygen, it will be
490
decomposed to several free radicals and leaves no residual components on foods which is an
491
important advantageous property than chlorine compounds (Akata, Torlak et al. 2015). For
492
example, in the work of treating apple juice with ozone, the concentration of residual ozone was
493
below the acceptable levels (0.4 mg/L) for all treated samples (Sung, Song et al. 2014). The use of
494
ozone requires relatively a short contact time and the treatment can take place during the process of
495
foods or on the final products (Ronholm, Lau et al. 2016).
496
Ozone has been effective against both Gram positive and Gram negative bacteria as well as
497
fungi, and even it has shown a capacity to be a virucidal agent. Among the parameters that affect
498
ozone antimicrobial properties, its solubility in water as well as the stability of its reactions with
499
organic and inorganic compounds are important. However, relative humidity (Timmermans, Groot
500
et al.), pH, temperature, food additives, and the amount of organic compounds present in food
501
formulation which can surround the cells and protect them are among important properties of foods
502
affecting the antimicrobial efficiency of ozone (Bridges, Rane et al. 2018). As well, the sensitivity
503
of target microorganisms (in strain level) to ozone, food matrix, the method of ozone treatment, the 19
504
devices and procedures for measurements of ozone are important parameters in optimization of
505
ozone treatment for specific foods (Khadre, Yousef et al. 2001, Aponte, Anastasio et al. 2018). In
506
fact, the oxidant potential of ozone can induce the reactions leading to the destruction of cell walls
507
and cytoplasmic membranes of bacteria. Ozone may attack principal components of cells such as
508
glycoproteins, glycolipids, and other amino acids and disrupt or inhibit the enzymatic reactions of
509
the cell (Sheng, Hanrahan et al. 2018). These changes can increase membrane permeability that is
510
the most important parameter of cell viability, resulting in the functional cessation of cell system
511
(Khadre, Yousef et al. 2001, Aponte, Anastasio et al. 2018).
512
The successful use of ozone in processing different food products has been reported (Crowe,
513
Skonberg et al. 2012, Muthukumar and Muthuchamy 2013, Aponte, Anastasio et al. 2018) and
514
summarized in Table 7. The use of aqueous ozone in salmon fillets (concentrations up to 1.5 mg/L)
515
efficiently reduced the initial number of aerobic bacterial populations and showed a significant
516
reduction of the L. innocua counts without making negative effects (Crowe, Skonberg et al. 2012).
517
When fresh chicken samples were dipped in deionized water, containing L. monocytogenes (for 30,
518
45 and 60 s) and were subjected to the gaseous ozone for 1 to 9 min (33 mg/min), ozone treatment
519
(at 33 mg/min for 9 min) efficiently inactivated 5-6 log CFU/g of L. monocytogenes on chicken to
520
below detection limit (Muthukumar and Muthuchamy 2013).
521 522
[Table 7] While the rate of ozone generation did not affect the efficiency of process, the time required
523
to obtain a 5 log reduction (t5d) increased at higher Brix in apple juice (Choi, Liu et al. 2012).
524
Sheng, Hanrahan et al. (2018) showed that gaseous ozone decreased L. innocua count on apple fruit
525
surfaces to ~1.0 Log10 CFU/apple after 30-week cold storage and suggested the use of ozone gas in
526
combination with the commercial cold storage to control Listeria spp. in apple fruit during storage
527
(Sheng, Hanrahan et al. 2018). (Karaca and Velioglu 2014). The efficiency of ozone was very close
528
to that of distilling and chlorinating (100 mg/L), resulted in the reduction of L. innocua count for
529
2.2 and 2.3, on some vegetables, respectively, without imposing negative effects, highlighted its 20
530
promising potential to be used for treating vegetables (Karaca and Velioglu 2014). Ozonation of the
531
white button mushrooms (at 5.3 mg/L for 60 min) reduced the counts of L. monocytogenes by 2.80
532
log and the reduction was lower than E.coli and Salmonella (Akata, Torlak et al. 2015). The effects
533
of shrimp treatment with ozonated water, antimicrobial coating and cryogenic freezing, singly or in
534
combination on the count of natural or inoculated L. innocua were examined by Guo, Jin et al.
535
(2013). The single use of every treatment reduced the natural bacteria and L. innocua by <2 log
536
CFU/g, while the combined use of them showed a synergistic reductions of the natural bacteria and
537
L. innocua (Guo, Jin et al. 2013). The optimal reduction of L. monocytogenes on fresh-cut bell
538
pepper was 3.06 log that was achieved with exposure to 9 ppm ozone for 6 h. The higher exposure
539
time and higher concentration led to a higher reduction of L. monocytogenes (Alwi and Ali 2014).
540
A synergistic effect in the inactivation of L. monocytogenes was found between ozone and
541
heating treatment at 50 °C. While, the simultaneous use of ozone and heat for 1 min reduced the
542
counts of L. monocytogenes by 0.79 and 0.93 log CFU/ml at 25 and 45 °C, respectively, the count
543
reached to below the detection limit (1 log CFU/ml) at 50 and 55 °C (Sung, Song et al. 2014).
544
Therefore, it was concluded that ozone combined with a mild heat treatment can have a higher
545
antimicrobial effect than ozone alone at room temperature (Sung, Song et al. 2014). While, ClO2
546
treatment resulted in the count reductions of 5.5, 2.1, and 7.1 log on carrots, blueberry, and
547
tomatoes, the gaseous O3 resulted in the reductions of only 0.8, 1.8, and 1.1 log, respectively. The
548
results showed that gaseous ClO2 can be a promising disinfectant for these three food products and
549
gaseous O3 was not satisfactory (Bridges, Rane et al. 2018). In fresh brines, 10 min ozonation and
550
10 min UV radiation lead to a 7.44 and 1.95 log CFU/ml reduction, respectively. However, the
551
sequential exposure of 10 min ozonation and UV resulted in >9 log CFU/ml reduction in L.
552
monocytogenes populations in fresh brine, which showed the high efficiency of using these two
553
treatments as hurdles (Kumar, Williams et al. 2016).
21
554
3.7.
555
Non-thermal plasma (NTP) or cold plasma in the food sector is highly recommended for
556
destroying detrimental microorganisms potentially presented in foods including sporulating and
557
spoilage microbes/pathogens. NTP technology refers to the fourth state of matter and consists of
558
partly ionized gas including electrons, charged ions, free radicals, excited molecules, photons and
559
atoms, in the absence of thermodynamic equilibrium. By applying electric discharge to a working
560
gas, inert or ambient air, plasma can be generated. Under atmospheric conditions, NTP is normally
561
consisted of reactive oxygen species (ROS), such as O, O2, O3, reactive nitrogen species (RNS),
562
such as N2, NO., NO2 and if humidity is involved, OH., H2O2, which all are known as potential anti-
563
microbial agents (Kim, Lee et al. 2014, Sant'Ana, Lis et al. 2018, Timmons, Pai et al. 2018). In
564
plasma, electrons have a high temperature while the temperature of active medium remains low.
565
Plasma application is mainly related to the processing of materials at industry level, which for
566
decontamination and processing of food is relatively novel. The typical sources for generation of
567
NTP include radio frequency plasma (RFP), dialectic barrier discharges (DBD), corona discharge
568
and microwave discharges (Phan, Phan et al. 2017). The major advantage of NTP is operating under
569
ambient conditions, which can cause less damages to the quality of foods (Jiang, Sokorai et al.
570
2017, Kim and Min 2018, Sant'Ana, Lis et al. 2018).
571
Cold plasma
The inactivation mechanism of microorganisms by NTP is associated with the existence of
572
reactive species that can attack the cell through oxidation stresses or physical lysis and cause either
573
leakage and release intracellular material (Kim, Lee et al. 2014, Timmons, Pai et al. 2018) or result
574
in genomic DNA damage (Jiang, Sokorai et al. 2017). The anti-microbial efficiency of NTP
575
depends on the applied voltage, frequency, mode of exposure, electrode type, gas mixture, treatment
576
time, and cell membrane characteristics of target microorganism as well as the type of product and
577
the bacterial location (Jiang, Sokorai et al. 2017, Phan, Phan et al. 2017, Kim and Min 2018).
578 579
For inactivation of L. monocytogenes by NTP, just a few studies have been successful in reducing the microbial load to 5-log or more. Table 8 shows a summary of literature studied on the 22
580
antimicrobial effect of NTP against L. monocytogenes from 2015 to 2018. Jiang, Sokorai et al.
581
(2017) and Ragni, Berardinelli et al. (2016) managed to inactivate Listeria spp. by more than 5 log
582
in tomato-smooth surface and in saline solution. Jiang, Sokorai et al. (2017) investigated the
583
inactivation of L. innocua rate in grape, tomato, cantaloupe and baby spinach and studied the
584
quality changes by applying plasma activated hydrogen peroxide under indirect exposure for 45 s
585
treatment and 30 min dwell time. However, for native microorganisms, this treatment was by far
586
less effective than inoculated bacteria. Moreover, decontamination of tomato stem scar was
587
remarkably harder and the population of microorganisms could not be decreased to more than 1.3
588
log. They related it to the formation of biofilms which provides a physical barrier for diffusion of
589
antimicrobial agents. That was completely in accordance to the other studies that showed the
590
effectiveness of NTP treatment depends on the matrix and surface structure of the products (Ragni,
591
Berardinelli et al. 2016, Sant'Ana, Lis et al. 2018).
592 593
[Table 8] The distance from actuator is another major factor for antimicrobial effect of NTP.
594
Timmons, Pai et al. (2018) represented that just at the distance close to the NTP producer, where the
595
concentration of the charged species is higher; the reduction in L. monocytogenes could reach to
596
almost 4.5 log. This can be due to the temporary life of reactive species and the fact that they return
597
to their normal state after a short while. As for the treatment time, while it was believed that longer
598
treatment time always results in higher inactivation rate, but this difference is not always
599
remarkable, and depends on the NTP producer device. Increasing the exposure time from 5 min and
600
10 min to 20 min in the studies conducted by Kim and Min (2018) and Sant'Ana, Lis et al. (2018)
601
slightly improved the inactivation rate from 0.6 to 1.1 log, and from 4.2 to 4.4, respectively. On
602
contrary, Ragni, Berardinelli et al. (2016) showed that changing the treatment time from 40 to 60
603
min can sustainably increase the inactivation rate of L. monocytogenes from 4 log to more than 7
604
log, respectively. In other studies, NTP failed to sufficiently inactivate L. monocytogenes (Choi,
23
605
Puligundla et al. 2016, Kim and Min 2018, Sant'Ana, Lis et al. 2018) and further studies are needed
606
to investigate the affecting factors more thoroughly.
607
There is a considerable disadvantage regarding the NTP treatment, which is the production
608
of nano-particles from electrode materials. Borra, Jidenko et al. (2015) showed that dielectric
609
barrier discharges at atmospheric pressure can generate tailored nanoparticles with the same
610
composition as the metal electrodes. As for the present level of nano-particle in food products,
611
further studies are required.
612
3.8.
Pulsed electric fields (PEF) processing
613
In the food industry, PEF can be used to destroy microorganisms such as molds, yeast, and
614
bacteria to improve the safety of foods. PEF or electroporation technology is defined as the use of
615
short, but high voltage pulses to a target food which is passed through two electrodes
616
(Timmermans, Groot et al. 2014, Zhao, Zhang et al. 2017). PEF technology has been subjected to a
617
wide investigation for its application possibility in food preservation and pasteurization due to its
618
great capacity in inactivation of pathogenic microorganisms and acquiring other merits, compared
619
to conventional thermal processing (Pyatkovskyy, Shynkaryk et al. 2018). PEF is able to disturb the
620
membranes of biological cells. The probable cause for the loss of cell membrane through the PEF
621
may be the creation of hydrophilic pores in the membrane structure and the opening of protein
622
channels (Sharma, Bremer et al. 2014, Pyatkovskyy, Shynkaryk et al. 2018). The type, composition,
623
and all other features of foods may affect the efficiency of PEF in destroying a target
624
microorganism. Two principal mechanisms for the PEF in microbial inactivation are known to be:
625
electroporation and electrical breakdown. Basically, thousands of volts per cm conducted for 20–
626
1000 µs are vital for an efficient inactivation of organisms in food products. The strength of the
627
electric field mainly depends on the objective of its use in food industry. As an example, for
628
increasing the efficiency of drying or enhancing the extraction yields for certain intracellular
629
compounds, lower intensity levels of PEF treatment are promising. However, due to survival of an
24
630
important percentage of cells subjected to PEF at the range of 10–19 kV/cm, only the PEF with
631
electric fields over 25 kV/cm is practically efficient for microbial inhibition. The bacterial spores in food products are resistant to PEF, even at high intensity, as well
632 633
different pathogenic microorganisms show various sensitivity to PEF. Gram positive bacteria are
634
generally less resistant to PEF than Gram negative bacteria. It was claimed that L. monocytogenes is
635
the most resistant microorganism against PEF, and thus it was suggested that the ability of a PEF
636
treatment to kill L. monocytogenes can be an indicator for its effectiveness in adequate inactivation
637
of microorganisms. The lower sensitivity of L. monocytogenes to electric PEF compared to other
638
pathogens might be demonstrated by two reasons (Timmermans, Groot et al. 2014). The size and
639
shape of target microorganisms influences the input needed electric field to destroy the cells.
640
Generally, the smaller cell size leads to a lower membrane to potentially be affected by the
641
treatment. Also, the shape of microorganism can greatly affect the membrane potential: Generally,
642
the electric field required for destroying a rod-shape cell is almost five times stronger than that
643
amount needed for a spherical shaped cell with the same characteristics (Timmermans, Groot et al.
644
2014).
645
Several works have studied the effect of PEF on inactivation of L. monocytogenes in
646
different food products, as summarized in Table 9. The required energy for inducing a 5 log
647
reduction in L. monocytogenes was 113, 257, and 508 kJ/kg for apple, orange, and watermelon
648
juices, respectively which indicated the effect of pH trend (watermelon> orange> apple) on
649
sensitivity of L. monocytogenes to PEF treatment. The comparison of required energy for making a
650
5 log reduction in L. monocytogenes with those levels obtained for other bacteria such as E.coli (67,
651
58, and 197 kJ/kg for apple, orange, and watermelon juices, respectively) and Salmonella (65, 76,
652
and 130 kJ/kg for the same order of juices) well represents the higher resistance of L.
653
monocytogenes to PEF (Timmermans, Groot et al. 2014).
654
[Table 9]
25
655
In several studies, L. innocua was chosen as a L. monocytogenes surrogate, due to the
656
biosafety issues (Schottroff, Gratz et al. 2019). When PEF treatment of water was performed at both
657
10 and 20 V/cm for different time treatments, the increase of electric field input and time treatment,
658
generally led a higher inactivation of L. innocua (Pyatkovskyy, Shynkaryk et al. 2018). The impact
659
of PEF combined with a sanitizer solution treatment on the inactivation of L. innocua inoculated on
660
blueberry fruits was studied (Jin, Yu et al. 2017). L. innocua counts on blueberry subjected to PEF
661
(maximum peak voltage: ±11 kV) for 2 and 4 min was reduced by 2.3 and 2.6 log CFU/g,
662
respectively. However, when blueberries were soaked in a specific sanitizing solution (Tsunami
663
100) and were not treated by PEF, the reduction of less than 1 log CFU/g in L. innocua were
664
observed (Jin, Yu et al. 2017).
665
The use of higher inlet temperature was not effective in increasing the inactivation
666
capability of the PEF against L. innocua in whey proteins which might due to specific conditions of
667
the PEF process, higher temperatures induced a change in membrane fluidity associated with a
668
decrease of the parameter of electric field strength (Schottroff, Gratz et al. 2019). The portion of
669
lethal and sub-lethal injury is an important factor for studying the recovery possibility of injured
670
cells by a target process after treatment and during shelf-life of the product which should be kept at
671
a low acceptable level. The proportion of the sub-lethally injured L. monocytogenes cells in milk
672
were affected by the electric field strength and treatment time and it increased from 18.98% to
673
43.64% with increasing the electric field strength from15 to 30 kV/cm; while it progressively
674
decreased at greater electric field strengths and with longer treatment times (Zhao, Zhang et al.
675
2017). When milk with different initial temperatures were subjected to PEF (Sharma, Bremer et al.
676
2014) by the electric field strengths of 18-28 kV/cm for 17-235 us, the PEF treatment at 4° C did
677
not reduce L. innocua numbers, but its effectiveness increased at higher temperatures. PEF
678
treatments at 22-28 kV/cm (for 17-101 us) reduced L. innocua count to below the detection limit at
679
55° C (Sharma, Bremer et al. 2014).
26
680
Despite the inferred benefits of using PEF technology, some limitations associated with its
681
use have been reported. For example, some spores or ascospores, or vegetative cells have shown
682
resistance to the conventional PEF treatment which can result in to a failure in the process of
683
pasteurization which equals with a potential safety hazard (Arroyo, Cebrián et al. 2012).
684
4. Conclusion
685
Although L. monocytogenes is less common than some other foodborne pathogens in
686
environment and foods, due to having such high mortality rate of about 30% accompanied with its
687
high resistance to sterilization technologies, it was considered the focus of this study. This work
688
was performed to assess the efficiency of non-conventional food processing technologies in
689
destroying L. monocytogenes and potentially most of other pathogenic bacteria in foods. Among all
690
new technologies emerged as an alternative to the conventional heating sterilization, recently high-
691
pressure processing (HPP) was studied extensively, and thanks to the large number of researches,
692
HPP was more developed, resulted in higher number of works with a successful 5-log reduction of
693
L. monocytogenes counts in foods meeting the FDA requirement, followed by ultrasound and
694
microwave technologies. However, based on the literature, there is a serious concern regarding all
695
these methods, which is the sublethal effect and the chance for recovery of L. monocytogenes after
696
treatment. Since the potential recovery of L. monocytogenes during shelf-life can be considered as a
697
serious food safety threat, enough studies should be conducted to address this issue before labeling
698
any treatment as a promising technology in inhibition of L. monocytogenes growth in food products.
699
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40
Product Kiwi puree
Table 1. The effect of conventional heat treatment on the counts of L. monocytogenes in food products Treatment conditions Microbial Initial count, reduction, D- value (min) Others Time, min T, °C log(CFU/ml) log(CFU/ml) 12.5, 7.5, 2.5
50, 55, 60
3, 6, 5
Cold smoked salmon
58, 66
14.1, 0.3
Benlloch-Tinoco, Pina-Perez et al. (2014) Shi, Tang et al. (2014)
Spinach blend PBS
56, 58, 60 56, 58, 60
11.8, 4.5, 1.2 2.7-4.4, 1-1.4, 0.35-0.66
Monu, Valladares et al. (2015) Aryani, den Besten et al. (2015)
BHI
55, 60, 65
9.2-30.2, 0.58-4.1, 0.075-0.57
Ricotta cheese
25, 40
90, 85
Turkey ham
30
90, 80
5
4, 1
Skim Milk
1
65, 70
6.7
Cream
1, 3
70
5.9-6
Smoked tench
2.73
72
TSB
15
55
TSB
1
In shell pistachio
0.5
Almond
0.25
5
End temp.< 60 °C, <50 °C
Spanu, Scarano et al. (2015)
>5, 3.05
Fixed temp.
Delgado Suárez, Chairéz Espinosa et al. (2015) Kim and Kang (2015)
2.48, 5
Fixed temp., end temp: 70 °C
5
Smoking oven
5
1
5.2
5
6
>5
4.56
6
>5
2.41
Branciari, Valiani et al. (2016) Ragni, Berardinelli et al. (2016)
+ 0.5 mM Nano d-limonene Superheated steam
Ban and Kang (2016)
0.8
aw=0.565
Rachon, Penaloza et al. (2016)
Seasoning
0.65
aw=0.655
Chicken meat powder
0.61
aw=0.383
Pet food
0.54
aw=0.653
Confectionery
200
pH=3.4
Reference
100
Sausage/ham
14.6/11.8
Sausage/ham
25.4/24.9
Tomato, Lettuce
2.5
Tomato, Lettuce
1.75, 2.5
Water, TSBYE
5, 60
55
Caramel apple
0.08
99
Broth
60
4
60
Wang, Uyttendaele et al. (2016)
4
+3% NaCl
3.5, 3
at 5 °C for 5 days before treatment at 5 °C for 1 day before treatment
Poimenidou, Chatzithoma et al. (2016)
+ 2% Lactic acid
Omori, Miake et al. (2017)
3.5, 1.5
60, 62.5, 65
9
5, 2 <3
Gustafson and Ryser (2017) 1.3, 0.53, 0.24
41
Wang, 2017 Wang, Devlieghere et
Agar
60, 62.5, 65
3.1, 1.2, 0.41
al. (2017)
Salmon roe
57.5, 60, 62.5, 65 57.5, 60, 62.5, 65 52.5
3.42-6.67, 1.34-1.37, 0.3-0.48, 0.1-0.14 12.9-19.68, 5.03-6.77, 1.21-2.4, 0.5-0.79 1.49, 24.76
Li, Huang et al. (2017) 4.5% salt
Apple, Carrot juice
0.016, 0.952
+ 0.5 mM d-limonene
Carrot juice
65.43
juice without fiber and fat
Apple, Carrot juice
Saline solution
15
50, 55, 60
9.1
Mate, Periago et al. (2017)
1.6, 3.4, 4.1
Xuan, Ding et al. (2017)
Tryptic Soy Broth
54
10-17.8
pH=4.5
Tomato puree
54, 58
10.6, 3.42
"
Apple juice
2, 1.75, 0.75, 0.4
55, 60, 65, 70
Chili sauce
4
100
Cantaloupe
4
1, 5.5, 5.5, 5 8
Siguemoto, Gut et al. (2018)
6
10% sugar #
Kim, Park et al. (2018)
85
Steam, #
Neha, Anand et al. (2018)
, after storage, after storage + Acidic acid +H2O2
Trzaskowska, Dai et al. (2018)
aw=0.3, 0.45, 0.6, 0.6, 0.6
Taylor, Tsai et al. (2018)
Ice cream
30
69
Mung Bean
20
60
6
5, 2, 4
Wheat flour
20, 15, 9, 20, 50
80, 80, 80, 75, 70 50, 55, 60
8
3,6, 5, 5, 3.5
Crab meat
Dufort, Sogin et al. (2017)
7.08, 3.13, 1.59, 4.61, 16.85 174.4, 28.2, 1.6
Forney, Fan et al. (2018)
McDermott, Whyte et al. (2018)
#: In this study, Listeria innocua has been used. Temp: Temperature, TSB: Tryptic Soy Broth, PBS: Phosphate-buffered saline, BHI: Brain heart infusion broth. aw: water activity.
42
Table 2. The effect of high hydrostatic pressure treatment on the counts of L. monocytogenes in food products
45, -5
Initial counts, log(CFU/ml) 6-7
Microbial Reduction, log(CFU/ml) 6.2, 5.6
31
5.6-4.9
2.2-3
Merialdi, Ramini et al. (2015)
10
7
Ramos, Chiquirrín et al. (2015)
5 5
25
7
2.5,3.5,4 4
25
7
1.7
8.45
5.13, 5.18
Product
Treatment condition Pressure, Pa Time, min
T, °C
Smoothie
300
5
Pork production
600
6
Milk, whey, buffer
300 400
Green bean
Shelf life Days log (N)
Others
Scolari, Zacconi et al. (2015)
14
3.2
#
, + Chitosan
230, 300
5
45, -5
Dry-cured- ham
800-850
5
15
>5
aw=0.86-0.96
15
>5
aw=0.96
Dry-cured-ham
450
10
12
5.27
15
0.58
Skimmed milk
250, 200
70, 60
7
>7, 1.33
Cured meat Raw milk
700, 600 400, 450
3 5
20 25
5 8
5 >5, >7
Soup
500, 600
5
44
8
6
45
3, 5
3,5
60
28
21
600
1
25
8
6.16, 1.29, 6.16-7.47
Vacuum salad
400
1
18
7
4.2, 1.5
21
Cantaloupe puree
500, 400
5
35, 30
7
>5, <3
10
Ham
500
4
32,15
6
>5
20
8
1
22
>5
22
>3.5
450
Cheese
300
Cold- smoked salmon
600, 450
2
Chicken
300
10
-2
Zacconi, Giosue et al. (2015)
4.23
<5
Bover-Cid, Belletti et al. (2015)
de Alba, Bravo et al. (2015) #
Pinho, Oliveira et al. (2015)
11.7-29 g/l salt, 0.09 mg/l nitrite
Valdramidis, Patterson et al. (2015) Huang, Lung et al. (2015) Ates, Rode et al. (2016)
Chicken
Beef steaks
Donsì, Marchese et al. (2015)
3.6
Smoothie
700-850
Reference
0 salt:0% NaCl, 2.5% NaCl, 0-2.5% CaCl2
Balamurugan, Ahmed et al. (2016)
2.5, >7.5
pH:Low, High
Stratakos, Linton et al. (2016)
ND, 1.5
pH:6.9
Mukhopadhyay, Sokorai et al. (2016) Magalhães, Ferreira et al. (2016)
1-2
15
6
Li and Ganzle (2016) +Thyme extract
Bleoancă, Saje et al. (2016)
6
4, 3
36
<2 ,7.5 at 7°C
+Nisin (10ug/g)
Lebow, DesRocher et al. (2017)
23
6
6
21
ND
Packed with PLA/PEG/CIN4,3
Ahmed, Mulla et al. (2017)
23
6
<3
"
>3
PLA/PEG/CIN1,2
43
Sea bream fillet
300
5
Fruit puree Buffer solution
300
1
Black tiger shrimp
400, 500, 500
pulse, pulse, 12
Milk
400, 400, 500
5, 10,5
400, 500
30
5.3
1.83
10
5.2
5.5
5
"
<1
6
5
#
+0.8 ug/ml Endolysin
30
6
1.2
40
7
3, 4, 4.8
6.86- 6.4
3,>6,>6
, , 15
, ,8.77
5
>5, >6
, 15
, 8.99
+4 mg/ml potassium sorbate
400
"
>6
"
ND
+2 e-Polylysine
Fermented meat sausage
300
5
Cooked sausage
600
10
8/6
2
60
8
10
4, 8/6, 4
2
" 35
ND, 3.5/3, ND 4.5
"
ND
28 "
4.2, 8 ND, 4.7
72
Castro, Silva et al. (2018) + P. acidilactici HA-6111-2 storage at 10 °C
Balamurugan, Inmanee et al. (2018)
aw=0.9, 0.82 , +ready to eat meat microbiota +Nisin, Rosemary
Rubio, Possas et al. (2018) Teixeira, Repkova et al. (2018)
#
Pyatkovskyy, Shynkaryk et al. (2018)
550 500
10 3 "
6 6.5, 7.5 7.2, 6.5
3.7, 2.5 2.5, 3 5.2, 2
Water
400
1
9.5
6.5
Milk
550, 600
3, 12
9
2, >5
550
6/9
9
>5
500
5
6
4, 6
4,6
15
0, 1
600
5
6
4, 6
4
"
<1, 3
Scott A
0, 3
#
+Nisin
Alcantara-Zayala, Serment-Moreno et al. (2018)
CECT 4031
Evert-Arriagada, Trujillo et al. (2018)
600
5
6
4, 6
3.5, >6
Smoked salmon
500
10
25
7
1.5
Smoked salmon Mozzarella cheese
400 500
3 7.4
0.5 5.5
20
2.5
Storage: 10 °C+34 ug/ml Plyp825
Mozzarella cheese Milk
400 500, 400
3 7.4
2 6, 5
27 13
1 8
Storage: 10 °C+3.4 ug/ml Plyp825
5.5, 3.8
4, 3
27
1, 8
Storage: 10 °C+3.4 ug/ml Plyp825
Milk 400 # : in this study, listeria innocua has been used. aw: water activity.
"
Kaur and Rao (2017) Liu, Li et al. (2017)
Chorizo Sausage Ham
Fresh Cheese
van Nassau, Lenz et al. (2017)
#
3 "
Blazquez, Burgos et al. (2017)
Misiou, van Nassau et al. (2018)
44
Table 3. The effect of sonication on the counts of L. monocytogenes in food products Product/medium Amplitude Plastic container Lettuce, Strawberry
Treatment conditions Frequency, Time, kHz min 35 15 37
60, 45
T, °C
Initial count, log(CFU/ml)
Microbial Reduction, log(CFU/ml) 91% 2, >5
Others
Reference
Bath
Torlak and Sert (2013)
#
Birmpa, Sfika et al. (2013)
, Bath
Orange juice
600 W
28-45-100
35
5.5
5
Gabriel (2014)
Stainless steel, TSB and lettuce Lettuce wastewater
1200 W
37
100
6
1
Lee, Kim et al. (2014)
100 µm
24
20
35
5
2
5
<60
6
~5
6
Recycled water from lettuce TSB
20 90 µm
Milk
20
+ native microbes
Anese, Maifreni et al. (2015)
<2
#
, +Peroxyacetic acid
Gómez-López, Gil et al. (2015)
+ sucrose, aw=0.97, pH=6
Franco-Vega, Ramirez-Corona et al. (2015) Gabriel (2015)
3, 8, 10
65, 60, 55
8
5, <3, 2
28-100
50
<60
5.5
5
6
<1
+2%cinnamon oil
Ozcan and Demirel Zorba (2016) Luo and Oh (2016)
Vegetable salad
54 W/L
20
15
Bell pepper
400 W/l
40
5
60, 50, 40
2.5, 1.5, 1.5
Bath
5
60
>4.5
+Acidic water, pH=6.5
0.6
Bath
Salmon fillet
200
45
BHI
60 W
20-100
30
8.5
TSB
120 µm
20
TSB Injection needle
Lettuce leaf
8
22
5
+0.78 ug/ml Melittin
5
+ 40mM ZnO
<1
-
7, 5 7
3.25, <2 >5
700 W
6
2.23
#
6
12 75, 90% "
20 "
14 14
100 W
42
20
20
Endive Water
1.6 100%, 500 W
4
35
Wu and Narsimhan (2017)
4
BHI
9.5
1.6
#: in this study, Listeria innocua has been used. BHI: Brain heart infusion, TSB: Tryptic Soy Broth
45
Mikš-Krajnik, James Feng et al. (2017)
Dolan, Bastarrachea et al. (2018)
Hamann, Tonkiel et al. (2018)
+0.03% peracetic Acid , cleaner tank
Huang, Wrenn et al. (2018)
+ cinnamon leaf oil
Park, Kang et al. (2018)
#
Pyatkovskyy, Shynkaryk et al. (2018)
Table 4. The effect of microwave treatment on the counts of L. monocytogenes in food products Treatment conditions
Initial counts, log(CFU/ml)
Microbial reduction, log(CFU/ml)
Others
Reference
75, 60
6
>5, 2
Household MV
2450
35
7
>6
#
Rodriguez-Marval, Geornaras et al. (2009) Picouet, Landl et al. (2009)
875
80
2
6
>5
Continues
Kiwi puree
1000, 900
2450
82, 75
7
5
Salsa
915
30, 30, 50, 60, 110 340
5.5-6
Kiwi puree
4.8, 3.6, 2.4, 1.8, 1.2 K 1000
7
5, 5, 5, 4.58, 4.73 5.8
Chicken meat Tomato paste
900 1800-3000
2450 915
50
6
6
Peanut butter
2, 4, 6, 6, 6 K
915
300
5-5.6
Chicory Stem
900
2450
90
9, 4.3-5.6
0.24, 1.25, 3.82, 2.8, 1.98 6.5, >5
Apple juice
1000
2450
130
6
5
Chili Sauce
1500
915
50, 50, 70
7.4-7.8
>5
10, 25, 40 % sugar
3000
"
20, 25, 40
>5
10, 25, 40 % sugar
Product
Power, W
Frequency, kHz
Time, s
Frankfurter sausage
1100
2450
Apple puree
652
Catfish fillet
#
2450
T,°C
<50
>70
Sheen, Huang et al. (2012) Benlloch-Tinoco, Pina-Perez et al. (2014) Sung and Kang (2014) Benlloch-Tinoco, Igual et al. (2015) Zeinali, Jamshidi et al. (2015) Kim, Sung et al. (2016)
: in this study,Listeria innocua has been used
46
aw=0.5, 0.5, 0.5, 0.4, 0.3 Under vacuum
Song and Kang (2016) Renna, Gonnella et al. (2017) Siguemoto, Gut et al. (2018) Kim, Park et al. (2018)
Table 5. The effect of irradiation on the counts of L. monocytogenes in food products Treatment conditions
Product Type
Dose, kGy
Crab meat
Gamma
Frozen meat trimming Ready-to-bake cookie dough
Gamma Gamma Electron beam KrCl excilamp
1, 2 1,2 3, 1.5 3 3
Water
Tahini halva
Gamma 521.2 Ci
Coconut water PBS, PW PBS, PW Sliced cheese Ready-to-eat sliced ham
UV UV-A UV-B X X
0.8 1.6 2.4 3.2 4
Time
9,4.5 min 9 min 15, 20 s 15, 20 s 15, 20 s 0.15 min 0.3 min 0.45 min 0.6 min 0.75 min
Initial count, log(CFU/ml)
Microbial reduction, log( CFU/ml)
~6.8 ~7.6 6 5.96 4-5, 5-6 6-7 -
2.3, 5.7 1.5, 4.4 3, 1.5 4.5 5 >3, >3 3.3, >4 1.27, 1.98 0.69, 0.86, 0.62 1.24, 1.66, 1.19 1.97, 2.65, 1.81 2.55, 3.30, 2.29 2.96, 4.30, 3.29 2.7, 4.3, 5.85 0.9, 0.5 5.4, 3.5 3.7, >4.47, >4.47 3.8, >6.2, >6.2
8 5-6 0.4, 0.6, 0.8 0.4, 0.6, 0.8
6.9
*: The results are derived from graphs and the numbers are approximate. PBS: phosphate-buffered saline, PW: peptone water
47
Others
Reference
DMST 1783* DMST 4553*
Suklim et al. (2014) Xavier et al. 2014 Jeong and Kang (2017)
10 MeV 222-nm, 2.03 mJ/cm2, 20W pre-stored for:0, 7, 30d “ “ “ “ 2 10, 20, 25 mJ/cm * 2 356 nm, 94 mJ/cm * 2 307 nm, 21 mJ/cm 160 kV, 10mA
Ha and Kang (2018)
Osaili et al. (2018)
Bhullar et al. (2018) Jeon and Ha (2018) J.-S. Park and Ha (2019) Cho and Ha (2019)
Product Beef muscle Orange juice
Table 6. Effect of Ohmic heating on the counts of L. monocytogenes in food products Ohmic heating conditions Initial Microbial Reduction, count, log Others Frequency, kHz T, °C Time, Rate, V/cm log(CFU/ml) (CFU/ml) min th:3.5, 6,8.5, 13.5 72 3.5 3.83, 5.39, 7.05, 7.05 0.001-10000
95
4
50 50
1
6 6
1 Milk
60
Salsa
2 1
Orange juice
50
12.1
Reference Zell et al, 2010
7.05
th:0
0.9, 0.5, 0.2
pH:2.5, 3.5, 4.5
2.4,0.9,0.7
pH:2.5, 3.5, 4.5
3.3, 3, 2.95, 2.2
Fat %: 0, 3, 7, 10
2, 5
, +1.3mM carvacrol extract
*
Lee, Kim et al. (2015)
* *
Kim and Kang (2015) *
*
2
9.6
1.9,0.73, 0.59, 0.43, 0.11
pH: 2.5, 3, 3.5, 4, 4.5
1
25.6
4.4, 3.4, 1.8, 4.3, >4.5
pH: 2.5, 3, 3.5, 4, 4.5 *
, + carvone, + eugenol, + citral, + thymol (1mM extract) * , + carvone, + eugenol, + citral, + thymol (1mM extract)
Kim and Kang (2017)
Park, Ha et al. (2017)
13.3
5-6
1.2, 1.8, 2.2, 5.8, 5.5
Salsa
11.5
5-6
0.6, 1.9, 2.8, 3.2, 4.3
0.167
30
5-6
0.07, 0.04, 0.43, 0.21, 0.34
Brix:18, 24, 36, 48, 72
0.33
30
0.04, 0.13, 0.42, 0.36, 0.32
"
0.167
60
0.66, 0.50, 1.46, 0.57, 0.31
"
0.33
60
5.94, 5.83, 5.71, 5.71, 0.23
"
Buffered PW Tomato juice *
0.06, 0.2, 0.5, 1
9.43–12.14
6
3.58, 3.62, 3.34, 3.97 2.87, 2.87, 3.41, 3.41
The results are derived from graphs and the numbers are approximate. th: holding time, min. PW: peptone water
48
Kim and Kang (2015)
*
Buffered PW
Apple juice
Kim and Kang (2017)
Kim, Park et al. (2018)
Table 7. The effect of ozone treatment on the counts of L. monocytogenes in food products Ozone treatment conditions Product
Flow rate/ Conc.
Time
Apple juice
1.67, 15, 58.5, 928 mg/min
Raw chicken
33 mg/min
Apple juice
6-9 mg/min
Lettuce/spinach/parsley Fresh-cut bell pepper Mushroom
950 µL/L 9 ppm 2.8 mg/L 5.3 mg/L 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2 0.86 mg/g O3 1.71 mg/g O3 0.06, 0.07 mg/ g ClO2 0.12, 0.15 mg/ g ClO2
5.70, 6.02, 5.49, 4.55 min 9.21, 8.06, 5.49, 4.96 min 3224e4, 2247, 1616, 597 5s 6s 7s 8s 9s 20 s 40 s 40 s 20 min 0.5, 3, 6 24 h 30, 45, 60 min 30, 45, 60 min 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 2.5, 5.0 h 5 min 10 min
Baby-cut carrots
Lowbush blueberries
Beefsteak tomatoes
Fresh brine (9% NaCl)
Initial count, log(CFU/ml)
4.92, 5.04, 6.30
5–6
6.59 5.1 5.1
Microbial reduction, log(CFU/ml) 5 5 5 1.84, 1.57, 2.82 2.35, 2.27, 3.26 ND, 0, 3.37 ND, ND, 3.62 ND, ND, ND 0.1, 2.5 0.2, 3.5 0.4, 3.7 1.16 2.3, 2.5, 3, 3 0.3, 1.1, 1.9 0.6, 1.6, 2.6 0.3, 0.4 0.8, 0.8 2, 2.5 5, 5.5 0.3, 0.6 1.2, 1.8 0.9, 1.0 2.1, 2.1 0.4, 0.5 0.6, 1.1 5.7, 7.0 6.0, 7.1 5.94, 7.33 >7.83, >9.0
Others
Reference
Brix 18 Brix 36 Brix 72 td:30s, 45s, 60s
Choi, Liu et al. (2012)
at 25, 55 °C
# *
Muthukumar and Muthuchamy (2013)
Sung, Song et al. (2014)
Karaca and Velioglu (2014) Alwi and Ali (2014) Akata, Torlak et al. (2015) Bridges, Rane et al. (2018)
+ 5, 10 min UV + 5, 10 min UV
Kumar et al, 2019
*: the results are received from graphs and the numbers are approximately; #: in this study, Listeria innocua has been used, td: dipping time in deionized water (s) before ozone treatment. Conc.: concentration
49
Table 8. The effect of cold plasma treatment on the counts of L. monocytogenes in food products Treatment conditions Product
Voltage, kV
frequency, kHz
Time, min
Electrode Material
Dist., cm
Saline Solution
13.8
46 kHz
60, 40
Silver/Brass/ Steel/Glass
2.4
Pork
20
58
2
Tomato- Surface Tomato-Stem Scar Spinach Cantaloupe Agar Plate Ham Onion Flakes Peptone water
17 " " " 6.4,6.4 10 9 7
-
45 s* " " " 10, 20 20 5, 5, 20 4
#
10 2 15, 35, 15
Initial count, log(CFU/ml) 9.2
2.5 -
Indirect
Steel mesh
Indirect
Quartz Copper
Floated
1, 3, 7
: in this study, Listeria innocua has been used. * Plus 30 min dwell. Dist.: Distance from actuator
50
Microbial reduction, log(CFU/ml) >7,~4 1
6.2-6.5 " " " 7 3.8 6.2 5- 6
6 1.3 4 3 4.2, 4.4 0.91 <0.6, 0.2, 1.1 <4.5, <2.5, <0.5
Reference Ragni, Berardinelli et al. # (2016) Choi, Puligundla et al. (2016) Jiang, Sokorai et al. (2017)
Sant'Ana, Lis et al. (2018) Kim and Min (2018) Timmons, Pai et al. (2018)
Product
Voltage, kV/cm
Milk
23
Apple juice
20
Orange juice Watermelon juice Blueberry
20 20 2
Milk Water
Table 9. The effect of pulse electric fields (PEF) on the counts of L. monocytogenes in food products PEF treatment conditions Initial Microbial Reduction, counts, Others T, °C Energy, kJ/kg Time log(CFU/ml) log(CFU/ml) *, # 0.101 ms 10 0.6, 2.8, >5 Ti: 4, 50, 55 56 75 2.2 pH 3.5 56
75
56
75 2, 4 min
30 10, 20, 30
0.6 ms 500, 20, 0.64 ms
7 9.5
1 0.2 2.3, 2.6
pH 3.7 pH 5.3
4.9-5.3 1.0, 2.4, 2.1
*, #
10 kV
*, #
100, 80
5.7, 3
Ti: 20, 40, pH: 4
Whey protein 2%
160, 125
1.5,1
Ti: 20,30, pH: 7
Whey protein 10%
160, 120
5.2,2.3
Ti: 20, 30, pH: 4
Whey protein 10%
160,120
1,0.9
Ti: 20,30, pH: 7
: in this study, Listeria innocua has been used. Ti: Inlet temperature, °C.
51
Sharma, Bremer et al. (2014) Timmermans, Groot et al. (2014)
Jin, Yu et al. (2017)
Whey protein 2%
#
Reference
Zhao, Zhang et al. (2017) Pyatkovskyy, Shynkaryk et al. (2018) Schottroff, Gratz et al. (2019)
Technology
HPP
Ultrasound
PEF
Heat
Fundament
High Pressure
Sonoporationt
Transmembrane potential
Energy-t
Mechanism of microbial inactivation
protein denaturation
Cavitation
Electroporation
Physical stress
Principle of microbial inactivation
cell membrane disruption
damaging DNA Cell explosion DNA damage
Membrane permealization
DNA synthesis inhibition
Ribosome
Cell wall disruption
Bacteria Response
Biofilm formation Genetic Diversity Stress resistance
Protein
Principle of microbial inactivation
damaging DNA
Membrane permealization
cell membrane disruption
cell membrane disruption
Mechanism of microbial inactivation
Inactivating cell replicationt
Plasma species on membrane
Pore formation
Free radicals
Fundament
Wave emission
Reactive compounds
Electroporation
Reactive compounds
Technology
Irradiation
Cold plasma
Ohmic
Ozone
Fig. 1. The inactivation mechanism of microorganisms in non-conventional processing technologies. 1
Non treated food characteristics:
Treatment condition:
PrePre-treatment characteristics
Strength(dose) of treatment
Composition and ingredients, importantly:
Type and procedure of treatment Time
Water content Antibacterial compound(s) Status of foods (liquid or solid)
Temperature Being used alone or as a hurdle
Expectations for processed foods:
Target bacterium characteristics:
Type of packaging
General resistance to treatment
ShelfShelf-life
Initial count
Quality and organoleptic characteristics
Interaction with other bacteria
Associated required regulations
Mechanisms for treatment resistance:
Consumer’ Consumer’s demands and attitudes
Genetic diversity
Fig. 2. The parameters which should be considered for optimization of non-conventional processing technologies
2
Highlights:
• • • •
Efficiency of novel food processes to inactivate L. monocytogenes was reviewed. High pressure pasteurization, sonication, and irradiation are efficient to destroy LMONO LMONO is a good indicator for examining the efficiency of sterilization technologies. Food composition, process type, and resistance of LMONO strains are important factors.