Trends in Food Science & Technology 66 (2017) 20e35
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Trends in Food Science & Technology
journal homepage: http://www.journals.elsevier.com/trends-in-food-scienceand-technology
Review
Mild processing applied to the inactivation of the main foodborne
bacterial pathogens: A review
Francisco J. Barba a, d, Mohamed Koubaa b, Leonardo do Prado-Silva c, Vibeke Orlien a,
Anderson de Souza Sant’Ana c, *
a
Department of Food Science, Faculty of Science, University of Copenhagen, Rolighedsvej 26, 1958 Frederiksberg C, Denmark
Sorbonne Universit
es, Universit
e de Technologie de Compi
egne, Laboratoire Transformations Int
egr
ees de La Mati
ere Renouvelable (UTC/ESCOM, EA 4297
TIMR), Centre de Recherche de Royallieu, CS 60319, 60203 Compi
egne Cedex, France
c
~o Paulo, Brazil
Department of Food Science, University of Campinas, Campinas, Sa
d
Nutrition and Food Science Area, Preventive Medicine and Public Health, Food Sciences, Toxicology and Forensic Medicine Department, Faculty of
Pharmacy, Universitat de Val
encia, Avda. Vicent Andr
es Estell
es, s/n, 46100 Burjassot, Val
encia, Spain
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 25 June 2016
Received in revised form
24 April 2017
Accepted 17 May 2017
Available online 19 May 2017
Background: Salmonella, Listeria monocytogenes, Escherichia coli O157:H7 and Campylobacter are the
major bacterial pathogens associated with foodborne diseases and their inactivation is fundamental to
ensure microbiologically safe products. Although efficient in generating safe foods with proper shelflives, pasteurization and commercial sterilization may result in numerous nutritional and sensory
changes in foods. To address these disadvantages, mild processing methods (i.e., processing technologies
for food preservation that apply mild temperature; <40 C) aiming to destroy microbial food contaminants have been developed.
Scope and approach: This review emphasizes the main applications of mild technologies aiming to the
inactivation of the four main pathogenic bacteria of relevance for food safety as well as their mechanisms
of action.
Key findings and conclusions: Mild processing technologies such as high pressure processing, ultrasounds,
pulsed electric fields, UV-light, and atmospheric cold plasma may serve, in some conditions, as useful
alternatives to commercial sterilization and pasteurization aiming to destroy foodborne pathogens. Each
of these mild technologies has a specific mode of microbial inactivation and their knowledge is of
foremost importance in the design and practical application aiming to produce high quality and safe
foods. This is necessary to ensure that mild technologies are highly advantageous in comparison to
conventional technologies not only for preservation of nutritional and sensorial aspects of foods but also
to ensure their safety throughout shelf-life.
© 2017 Elsevier Ltd. All rights reserved.
Keywords:
Food preservation
High pressure processing
Ultrasound
Pulsed electric field
UV-Light
Atmospheric cold plasma
Food safety
Shelf-life
Hurdle technology
1. Introduction
Food preservation has greatly relied on the application of
effective processes able to inactivate foodborne microorganisms.
These processes are of paramount importance and formed the solid
basis for the industrialization and commercialization of foods in
large scale. Pathogenic microorganisms are normally the major
targets of several industrial food processes because of the burden
posed by foodborne diseases. Moreover, these microorganisms may
* Corresponding author. Rua Monteiro Lobato, 80, 13083-862 Campinas, S~
ao
Paulo, Brazil.
E-mail address: and@unicamp.br (A.S. Sant’Ana).
http://dx.doi.org/10.1016/j.tifs.2017.05.011
0924-2244/© 2017 Elsevier Ltd. All rights reserved.
be able to adapt and withstand stressful conditions faced during
food production and storage.
The main traditional methods applied by industries for food
preservation include the application of heat (pasteurization and
sterilization), decrease of temperature (freezing and chilling),
reduction of water activity (addition of salt and sugar, or drying)
and addition of preservatives, among others. These methods may
be very effective, if correctly designed and applied, in inactivating
or ensuring pathogenic microorganisms will not grow and reach
levels that will impair food safety. Nonetheless, these methods
usually result in changes in nutritional, chemical/biochemical and
sensorial properties of foods that reduce their acceptance by consumers. In addition, environmental and wellness concerns served
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
as basis for the development of novel food preservation methods
(mild technologies) such as high pressure-based processes, pulsed
light, among others, have been introduced into food industries
(Georget et al., 2015; Jermann, Koutchma, Margas, Leadley, & Ros
~ a, Alvarez,
n, & Raso,
Polski, 2015; Koutchma, 2009; Saldan
Condo
2014; Serment-Moreno, Barbosa-C
anovas, Torres, & Welti-Chanes,
novas, Torres, &
2014; Serment-Moreno, Fuentes, Barbosa-Ca
Welti-Chanes, 2015). Despite this, it is the ability of a technology to
efficiently destroy a microbial target that will determine its potential practical applications. Given this, the understanding of
mechanisms and factors impacting on microbial inactivation by
mild technologies, specially speaking about the main foodborne
bacterial pathogens, is of foremost relevance for ensuring food
safety. Therefore, in this paper a comprehensive review of literature
on the key aspects of the application of mild technologies aiming to
ensure the production of safe foods is presented.
2. Key microorganisms impacting on food safety
Foodborne illnesses can be defined as any disease originated
from consumption of foodstuffs contaminated with microorganisms or chemicals (Tauxe, Doyle, Kuchenmüller, Schlundt, & Stein,
2010). Foodborne diseases cause the illness of several millions of
people around the world. For instance, in the United States, an
estimated 76 million illnesses occur annually, with more than 5.2
million of the infections that are attributed to foodborne pathogens
(Mead et al., 1999). These infections result in 128,000 hospitalizations and around 3000 deaths annually in the United States (CDC,
2010). Due to their high morbidity and mortality rates, foodborne
illnesses have taken great attention worldwide (Tauxe et al., 2010).
Salmonella spp., Listeria monocytogenes, Campylobacter spp., and
Escherichia coli O157:H7 comprise the most important bacterial
foodborne pathogens associated with foodborne diseases (Alocilja
& Radke, 2003; Chemburu, Wilkins, & Abdel-Hamid, 2005).
The Campylobacter species such as C. jejuni and C. coli have long
been recognized as the most important pathogens in veterinary
field. Moreover, Campylobacter spp. have received special attention
due to their repetitive occurrence in some foods for human consumption. C. jejuni is nowadays considered as the first causative
agent of human foodborne infection in developed countries
(Rantsiou & Cocolin, 2016). For instance, it was reported that both
C. coli and C. jejuni species cause the infection of approximately 2.4
million persons annually in the United States (CDC, 2011). Also,
C. jejuni is the most commonly isolated species from fecal specimens, with almost 90% of the reported cases (Fitzgerald, 2015).
Salmonella is the second most common bacterial pathogen
involved in foodborne diseases after Campylobacter. After
consuming contaminated foods, the symptoms (diarrhea, abdominal cramps, nausea, vomiting, fever, headache, and blood in the
feces (Poppe, 2011) may appear usually after 12e72 h and last for
4e7 days. In most cases, Salmonella infections do not require hospitalization, but high risk groups (children, elderly and those who
have weak immune system) are more prone to become ill and the
illness might be more severe (Grant, Hashem, & Parveen, 2016).
Salmonella infection cases are reported to be approximately 1.4
million in the United States of America annually, which result in
approximately 16,000 hospitalizations and about 600 deaths
(Cummings et al., 2010; Turner, 2010). In poultry industry, Salmonella and Campylobacter are considered as the major concerns
compromising the safety of poultry products. It is widely recognized that chicken represents the major vehicle for these pathogens
(Domingues, Pires, Halasa, & Hald, 2012; Greig & Ravel, 2009; Guo
et al., 2011; Hermans et al., 2012; Newell et al., 2011). However,
many other sources (raw or unpasteurized milk, eggs, meat, etc)
have also been associated to salmonellosis (Gurtler et al., 2015;
21
Poppe, 2011; Wingstrand & Aabo, 2014).
L. monocytogenes constitutes another major foodborne pathogen because of its psychrotrophic behavior (ability to grow below
€, & Hirn, 1988; Walker, Archer, & Banks,
7 C) (Junttila, Niemela
€limaa, Tilsala1990), under aerobic and anaerobic conditions (Va
€rvi, & Virtanen, 2015) and in a modified atmosphere packTimisja
aging (Swaminathan & Gerner-Smidt, 2007). In addition, this bacterium is able to grow in a broad pH range (4.0e9.6) (Farber &
Peterkin, 1991), and at low water activity levels such as 0.9
(Nolan, Chamblin, & Troller, 1992; de Daza, Villegas, & Martinez,
1991). These features make L. monocytogenes a great concern in
food industry that requires very effective control measures to be
implemented along the food chain (Lambertz, Ivarsson, LopezValladares, Sidstedt, & Lindqvist, 2013). The disease caused by L.
monocytogenes, i.e., listeriosis, is a severe foodborne disease that is
associated with the consumption of fish, meat, dairy products, as
well as fresh products. In fact, part of these food products have
usually a long shelf-life, and their storage at low temperatures and
in vacuum or modified atmosphere packages does not prevent the
€limaa et al., 2015). Despite this, it
growth of L. monocytogenes (Va
should be highlighted that L. monocytogenes has also been associated to foodborne disease outbreaks linked to the consumption of
wholesome foods that are not necessarialy commercialized at low
temperature conditions, such as fruits. L. monocytogenes can be
isolated not only from raw and processed foods but also from
environmental sources. It is a ubiquitous bacterium of special
concern for specific population groups (e.g. pregnant women, babies, the elderly and people with reduced immunity), for which the
illness can be more severe and even evolute to death.
The fourth main bacterial pathogen associated with foodborne
diseases is E. coli O157:H7, which is mainly transmitted to food
products, directly or indirectly, by the feces of cattle. Once
contamination takes place during processing, foods reach humans
and E. coli O157:H7 may cause the disease (Bari & Inatsu, 2014). This
microorganism produces verocytotoxin or shiga-toxin (verocytotoxin-producing E. coli, or VTEC; Shiga-toxin producing E. coli,
or STEC), which symptoms may include bloody diarrhea, hemolytic
anemia, low platelet count and thrombocytopenia (Karmali,
Gannon, & Sargeant, 2010). This type of pathogenic E. coli was
identified for the first time in the late 1970s (Konowalchuk, Speirs,
& Stavric, 1977) and their toxin structure (described as “Shiga-like”
toxin) was recognized in 1983 to have similar structure and antigenicity as Shiga toxin produced by Shigella dysenteriae type 1
(O'Brien & LaVeck, 1983). VTEC strains involved in human diseases
are especially found in cattle and foods of bovine origin (i.e.
undercooked ground beef patties and unpasteurized milk) (Griffin
& Tauxe, 1991; Rangel, Sparling, Crowe, Griffin, & Swerdlow,
2005). Other important foodstuff involved in VTEC outbreaks
were well reviewed by Rangel et al. (2005) and include fresh
products such as apple cider, spinach, lettuce, radish sprouts, alfalfa
sprouts.
The burden caused by these and other foodborne pathogens
have motivated the food industry to apply strict and robust hygienic protocols to avoid food contamination, as well as to develop
inactivation methods to destroy microorganisms likely present. A
recent and important trend due to consumer's demands is that
inactivation methods must also preserve the sensory and nutritional aspects of foods, while ensuring a proper shelf-life.
3. Key aspects in the design of processes to ensure
microbiologically safe foods during shelf-life
A food preservation method is considered as “ideal” when it
allows improving the shelf-life (inactivation of pathogens and
spoilage microorganisms), preserves the nutritional and
22
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
organoleptic properties, does not leave residual traces in the final
product, and is economically competitive to ensure the profitability
novas, 2003). As
of the food industry (Raso & Barbosa-Ca
mentioned, diverse methods such as decreasing the temperature
(e.g. chilling or freezing), decreasing either water activity or pH
novas, 2003), use of salt, sugar and adding
(Raso & Barbosa-Ca
preservatives are widely used for food preservation. Currently,
thermal treatment is the most extensively applied approach in food
industry to destroy foodborne microorganisms. The concepts and
key aspects of the application of thermal processing to inactivation
of foodborne microorganisms, was recently well reviewed by Smelt
and Brul (2014).
Although efficient, heating causes losses of sensorial (texture,
taste, flavor, and color) and nutritional quality attributes, such as
~ as & Paga
n, 2005a).
reduction of some bioactive compounds (Man
Therefore, there is a growing interest for processes that can reduce
the microbial load without increasing deteriorative reactions in
order to minimize quality losses. Nevertheless, high temperature
and/or long time are required in some foods to inactivate microorganisms (e.g. spores), which affects tremendously the organoleptic and nutritional food properties (Cardello, Schutz, & Lesher,
2007).
In addition to affecting the organoleptic and nutritional attributes of food products, conventional heating treatments require
high-energy consumption, which compromises with the final
product value to guarantee the profitability of the food industry.
Therefore, finding mild processing methods that maintain the
nutritional and organoleptic properties of the food, ensure microbial inactivation in foods to prolong their shelf-life and to safeguarde public health is of paramount importance. In order to
estimate the profitability of any new technology, it is necessary to
calculate the benefit brought to the product, which is highly variable and difficult to estimate. In addition, the economic cost per ton
of product associated with the use of the new technology in comparison with the conventional technology should be assessed. This
cost mainly depends on: i) investment on equipment, ii) energy
cost of the treatment, and iii) general production costs. The latter
ones can be quite variable, as they depend on local conditions (e.g.
rtolas, Alvarez,
cost of water, electricity, labor, ingredients, etc) (Pue
~
Raso, & Maranon, 2013). Althought these are highly relevant parameters, the aspects related to microbial inactivation can be
considered of chief importance. A technology with potential for
food preservation can be decidedly efficient regarding the environmental, sensorial and nutritional aspects. Nonetheless, if that
technology is not able to deliver a lethality of a target microorganism, it will hardly find vast practical applications in the food
industry. Given this, there are some general and specific parameters
that must be taken into account when the mild processing methods
are developed, which are briefly outlined below.
3.1. General parameters of mild technology approaches to
inactivate foodborne microorganisms, with special reference to
pathogenic bacteria
As alternative to thermal inactivation of foodborne pathogens,
numerous methods were described in the literature. Among them,
high pressure processing, pulsed electric fields, ultrasounds, UV
light irradiation, and cold plasma can be considered the most
relevant. Fig. 1 summarizes the technologies described in this review as well as their principles and mechanisms of microbial
inactivation.
In general, most studies performed are focused on the inactivation of Listeria spp., followed by pathogenic and non-pathogenic
E. coli, Salmonella and in low numbers, by Campylobacter (see
Suplementary Fig. 1). This may reflect the great concerns over the
potential presence of L. monocytogenes in minimally processed
foods considering that several foods treated by mild technologies
will further require storage at low temperatures, which will not
€limaa et al., 2015).
prevent the growth of L. monocytogenes (Va
Several studies deal with pathogenic and non-pathogenic E. coli
likely because of their general spread and potential to contaminate
foods through several routes, such as from raw materials, crosscontamination and food handling.
3.1.1. High pressure processing (HPP)
HPP is an efficient preservation treatment applied to packaged
solid or liquid food products with minimal modifications of the
nutritional and sensorial attributes (Barba, Esteve, & Frígola, 2012;
Barba, Terefe, Buckow, Knorr, & Orlien, 2015). HPP is based on the
use of very high pressures (100e1000 MPa) for a temperature range
from 20 to 60 C at short time (few seconds to 20 min) (Oey, Lille,
Van Loey, & Hendrickx, 2008). Fig. 2 represents a schematic diagram of a HPP operating unit and the pressure range of HPP
compared to other known pressure levels. The mechanisms of
microbial inactivation by HPP are based on a combination of
changes in the cell membranes (eg. structural changes in protein
and membrane phospholipids which can alter membrane permeability and the function of membrane-bound proteins), cell walls,
proteins and enzyme-catalyzed cellular functions (Patterson, 2014).
In fact, HPP acts due to molecular volume changes, thus pressure
favors chemical reactions and physical processes accompanied by a
decrease in volume. In addition, the effects of compression of HPP
treatments seem to be highly relevant in terms of microbial inactivation. It is known that compression of foods lead not only to
~ as & Pag
shifts in temperature due to adiabatic heating (Man
an,
2005b) but also in pH (Heremans, 1995). The isostatic principle
ensures that pressure applied and pressure within the food should
be equal. Nonetheless, a special attention should be paid to the fact
that for heterogeneous foods (meats with bones, for instance),
there might be pressure gradients, which will also result in nonuniform temperature distribution (Nair et al., 2016). Considering
that temperature and pressure are key factors for microbial inactivation, variability in microbial inactivation at different locations of
the foods can be observed (Nair et al., 2016). As such, during HPP
several phenomena may occur simultaneously (e.g. disruption of
cell walls and membranes, chemical reactions, enzyme activation
or inactivation, and protein modification such as denaturation and
gel formation) and thereby affecting the overall microbial load. A
more detailed description of HPP processing is provided in the
literature (Patterson, 2014).
Moreover, by using HPP for food preservation, numerous benefits are attained including reduced thermal exposure and, thus,
almost no sensory and nutritional changes (Georget et al., 2015)
which gives the consumer an increased sensation of a fresh product
(Ferrari, Maresca, & Ciccarone, 2010; Keenan et al., 2010). For these
reasons, the food industry found interest in replacing conventional
heating processes with high pressure processing. Especially, the
HPP inactivation of the four major pathogen species cited above
(Campylobacter, Salmonella, L. monocytogenes, and E. coli O157:H7)
has drawn attention to numerous food products. In Supplementary
Fig. 2, Box-and-Whisker plots illustrate the number of decimal reductions caused by HPP in Salmonella, Listeria spp. as well as
pathogenic and non-pathogenic E. coli. The range of pressures used
as well as the mean and standard deviation log10 CFU/mL or g
caused by HPP to these microorganisms may vary enormously as
affected by several factors such as food composition, bacterial strain
and environmental conditions (temperature, for instance).
When it comes to the application of HPP for microbial inactivation (Supplementary Fig. 3), it was found that most of the data
available for Campylobacter spp. inactivation by HPP corresponded
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
23
Fig. 1. Chart of the non-conventional, mild technologies described in this review for the inactivation of pathogenic microorganisms in foods. HPP, high pressure processing; US,
ultrasounds; PEF, pulsed electric fields.
to chicken (n ¼ 6 studies), while for Salmonella the top studied food
was ham (n ¼ 16 studies), followed by vegetables (n ¼ 14). For
Listeria spp., most of the studies dealt with juice (n ¼ 14) and milk
(n ¼ 12), while for pathogenic or non-pathogenic E. coli, the top
studied foods were juice (n ¼ 14) and beef (n ¼ 9).
3.1.2. Pulsed electric fields
Pulsed electric fields (PEF) is one of the utmost important mild
technologies for food conservation. PEF technology involves the
application of an electrical treatment during a very short period
(from several ns to several ms) and using a pulse amplitude from
100 to 300 V/cm to 20e80 kV/cm (Koubaa et al., 2015) (Fig. 3). PEF
processing induces the electroporation of the microbial membrane
which results in the alteration of membrane permeability, temporary or permanently (Teissie, Golzio, & Rols, 2005). Generally, this
permeabilization is dependent upon the cell geometry and size
rtolas, Koubaa, & Barba, 2016). Numerous food industries
(Pue
already acquired PEF food processing equipment (Jaeger, Balasa, &
Knorr, 2009; Mohamed & Amer Eissa, 2012), where different
treatment chamber configurations are used to process up to
€ pfl, 2011). Equipment cost constitutes one of
10,000 L/h capacity (To
the major issues limiting the industrialization of PEF technology
(To€pfl, 2006).
Fig. 3a represents a schematic diagram of industrial installation
using PEF for food processing. This technology takes its advantages
from its potential to permeabilize cell structure without damaging
the treated tissue. Studying and understanding the changes
occurring in the cell structure as a result of electric fields represent
the keys to keep and increase the quality and shelf-life of minimally
processed vegetables, respectively, thus maintaining the “fresh-like
characteristics” (Gonzalez & Barrett, 2010).
PEF treatments were studied for microbial inactivation mainly
in milk, eggs, juice and buffer (Ait-Ouazzou et al., 2012, 2011,; Aitn, 2013; Ferna
ndezOuazzou, Espina, Garcia-Gonzalo, & Paga
Molina, Bermúdez-Aguirre, Altunakar, Swanson, & Barbosa~ a,
C
anovas, 2006; Jaeger, Meneses, et al., 2009; Monfort, Saldan
n, Raso, & Alvarez,
rez, Martínez-Lo
pez, &
Condo
2012; Pina-Pe
~ a, Minor-Pe
rez, Raso, & Alvarez,
Rodrigo, 2012; Saldan
2011). PEF
conditions for microbial inactivation of Salmonella spp. (A), Listeria
spp. (B) and pathogenic or non-pathogenic E. coli (C) are shown in
Supplementary Fig. 4. The treatment seems to be promising for
Salmonella spp. inactivation, while it seems to be generally less
efficient for Listeria as well as pathogenic or non-pathogenic E. coli
inactivation (Supplementary Fig. 4).
3.1.2.1. Electric field intensity. One of the most significant factors in
PEF is the electric field. When applying an external electric (Ee) field
across the cellular membrane, a potential difference occurs. The
critical transmembrane potential, known also as critical electric
field (Ec), corresponds to the highest value withstood by the
membrane. When the Ee field exceeds the Ec value, the cellular
membrane breaks down. The effectiveness of PEF is highly
impacted by the type of microorganism as well as the environment
and the differences of the electric field values (Qin, Barbosanovas, Swanson, Pedrow, & Olsen, 1998).
Ca
3.1.2.2. Pulse waveform. Another influencing factor of microbial
inactivation after PEF treatment is pulse waveform. There are two
typical PEF pulse waveforms: exponential decay and square wave
(Fig. 3b).
Numerous works showed that enhanced microbial inactivation
occurs when applying, with the same energy, pulses with square
waves compared to exponential decay waves (Rodrigo, Ruíz,
novas, Martínez, & Rodrigo, 2003; Zhang, MonsalveBarbosa-Ca
lez, Qin, Barbosa-Ca
novas, & Swanson, 1994). Depending on
Gonza
their polarity, pulses could also be classified as monopolar or bipolar (Fig. 3c). When applying bipolar pulses, reversal of the electric
charge occurs by alternating positive and negative pulses. This
treatment causes structural fatigue by changing the movement
direction of charged ions in the cellular membrane, which increases
its susceptibility to electrical breakdown, and accelerate the inactivation of microorganism (Ho, Mittal, Cross, & Griffiths, 1995). On
the other side, when applying monopolar pulses, the inactivation of
microorganism is less effective, as the same polarity is maintained.
Furthermore, as monopolar pulses will separate the charged particles, a deposit will be formed on the electrode, which distorts the
electric field.
3.1.2.3. Pulse width. Pulse width is a crucial parameter to optimize
n, & Sala
for effective microbial inactivation (Raso, Alvarez,
Condo
Trepat, 2000). Therefore, several studies have determined the optimum pulse width, and it was concluded that a pulse width of z2
ms leads to the highest microbial inactivation level, with the less
consumed energy.
Increasing the pulse width over this value is not systematically
accompanied with greater inactivation of microorganisms. However, numerous studies showed that within a field intensity of
25e28 kV/cm, increasing the pulse width leads to increased inactivation of microorganisms (Abram, Smelt, Bos, & Wouters, 2003;
€ nner, 2001; Elez-Martínez,
Aronsson, Lindgren, Johansson, & Ro
-Herna
ndez, Soliva-Fortuny, & Martín-Belloso, 2005).
Escola
24
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
Fig. 2. a. Schematic diagram of HPP operating unit for the inactivation of foodborne microorganisms. The packaged food is placed in a pressure vessel containing a pressuretransmitting liquid (usually water), and the pressure is produced by a hydraulic pump (as shown) or by a piston and is transmitted to the product instantaneously and uniformly. b. Pressure range of HPP among other known mechanisms and associated biological mechanisms with increased pressure.
3.1.3. Temperature
PEF is generally accompanied with increased temperature, due
to ohmic heating. This rise of temperature occurs proportionally to
the treatment intensity (electric field and treatment time), allowing
thus further inactivation of microorganisms through a synergetic
effect (pulses-temperature) at 35e60 C.
The main effects of temperature on microbial inactivation seem
to be associated with an augmented permeability and fluidity of the
microbial membrane and consequently its structural fatigue
(Jayaram, Castle, & Margaritis, 1992). In fact, at low temperature
conditions, phospholipids constituting the membrane of microorganisms are attached, which create a gel-shaped rigid arrangement
ngora-Nieto, San-Martin, & Barbosa-Ca
novas, 2005).
(Sepulveda, Go
Therefore, increasing the temperature will decrease the physical
stability of the membranes, adopting a crystalline liquid appearance, and thus being more susceptible to PEF treatment.
3.1.4. Ultrasounds
Likewise, ultrasound was broadly applied for several food and
non-food applications (e.g. decontamination, extraction of valuable
compounds, etc). The basic mechanism of action of US to inactivate
microorganisms was previously reviewed by several authors
(Piyasena, Mohareb, & McKellar, 2003; Zinoviadou et al., 2015) and
it is mainly based on cavitation phenomena, which promotes the
formation of shock waves when the bubbles that are generated
during the ultrasound processing collapse. These shock waves
promote the generation of high temperatures and pressures, which
are the main factors that result in microbial inactivation. The main
processing parameters that influence ultrasound treatment are: i)
power, ii) frequency (20 kHz-10 MHz), and iii) treatment time.
Several studies have reported the huge potential of ultrasounds
to inactivate microorganism (Zinoviadou et al., 2015). However, in
most of the cases ultrasound does not allow achieving 5-log
reduction of microorganisms when it is used alone, although the
degree of inactivation differs depending on the targeted
microorganism.
However, interestingly, this technology presents a great versatility and can be combined with other techniques such as temperature (thermosonication), pressure (manosonication), pressure and
temperature (manothermosonication), thus having a synergistic
effect with all of them when they are used together. Therefore, this
technology has the potential to be used to decrease the temperature used in heat treatments, pressure in high pressure processing,
etc., thus allowing mild processing treatments, which can avoid the
degradation of nutritional and quality parameters (Zinoviadou
et al., 2015).
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
25
Fig. 3. a. Schematic diagram of industrial installation using PEF technology for the inactivation of microorganisms in food products. b. Exponential and square waves used in PEF
treatments. c. Bipolar square wave.
Research was done on L. monocytogenes, a number of strains of
Salmonella spp., E. coli, S. aureus, B. subtilis and some other microorganisms. However, most data available in the literature is focused
on the study of Listeria inactivation in milk (n ¼ 24). Less than two
studies were conducted for each of Campylobacter spp., Salmonella
spp. and E. coli, highlighting the potential use of this method for
ensuring the safety of milk and dairy products (Allen et al., 2008;
novas, 2008; Boysen &
Bermúdez-Aguirre & Barbosa-Ca
Rosenquist, 2009; Haughton, Lyng, Morgan, et al., 2012; Huang,
Mittal, & Griffiths, 2006; Lee, Kim, Cadwallader, Feng, & Martin,
~ as, Paga
n, Raso, Sala, & Condo
n, 2000; Musavian,
2013; Man
~ as, Raso, &
Krebs, Nonboe, Corry, & Purnell, 2014; Pag
an, Man
n, 1999).
Condo
3.1.5. UV-light
Ultraviolet (UV) light corresponds to the portion of the electromagnetic spectrum having wavelengths ranging between 100
and 400 nm. The formation of lesions in the genomic DNA of the
organisms, by UV-B and UV-C radiation, represents the main cause
of microorganisms' inactivation (Friedberg, Walker, & Siede, 1995;
Harm, 1980). The presence of these lesions inhibits the DNA replication and therefore results in inactivating the microorganisms
(Fig. 4) (Oguma et al., 2001).
The first application of UV-light treatment at large scale was
carried out in Marseille (France) in 1906, for the decontamination of
drinking water (Masschelein & Rice, 2002). Nowadays, wide range
of applications in food safety and food quality have been reported,
including the treatment of apple cider (Koutchma, Keller, Chirtel, &
n, Serrano, Monfort, Alvarez,
Parisi, 2004), orange juice (Gaya
&
n, 2012; Tran & Farid, 2004), liquid egg products (Unluturk,
Condo
Atılgan, Handan Baysal, & Tarı, 2008), milk (Krishnamurthy,
Demirci, & Irudayaraj, 2007), and honey (Fit et al., 2014). UV-light
was described as an efficient method for the inactivation of a
wide range of microorganisms including viruses (Eischeid, Meyer,
& Linden, 2009), vegetative cells and bacterial spores, fungi
mez-Lo
pez, Devlieghere, Bonduelle, & Debevere, 2005), and
(Go
parasites (Hijnen, Beerendonk, & Medema, 2006).
Due to this wide range of applications, UV-light could be used
similarly for the disinfection of food-contacting surfaces, foods, and
mez-Lo
pez, Koutchma, & Linden, 2012). It was
liquids in general (Go
also demonstrated that the application of UV light improves the
toxicological safety of foods by reducing the levels of mycotoxins
(i.e. patulin) in apple cider (Dong et al., 2010), and by reducing the
allergenicity of foodstuffs such as liquid peanut butter (Chung,
Yang, & Krishnamurthy, 2008).
UV-light has been extensively applied for the inactivation of
E. coli (pathogenic or non-pathogenic) in juice (n ¼ 27 data) and
milk (n ¼ 8 data). Less than two studies focused on the use of UVlight for the inactivation of Campylobacter spp., Salmonella spp. and
Listeria spp. (Chun et al., 2009, Chun, Kim, Lee, Yu, & Song, 2010;
26
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
Chun, Kim, Chung, Won, & Song, 2009; Crook, Rossitto, Parko,
Koutchma, & Cullor, 2015; Haughton et al., 2011; Haughton, Lyng,
Cronin, et al., 2012; Orlowska, Koutchma, Kostrzynska, & Tang,
2015; Yin, Zhu, Koutchma, & Gong, 2015).
3.1.6. Atmospheric cold plasma
Plasma represents a neutral ionized gas constituted of particles
that include free radicals, free electrons, positive and negative ions,
quanta of electromagnetic radiation, as well as excited and nonexcited particles (Misra, Tiwari, Raghavarao, & Cullen, 2011).
When plasma is generated at room pressure and temperature, it is
termed atmospheric cold plasma (ACP). ACP technology is a novel
approach dealing with the inactivation of microorganisms to
improve the food safety, along with the preservation of the
organoleptic properties (Ziuzina, Han, Cullen, & Bourke, 2015). The
technology takes its advantages from its use of reduced water
quantity, low processing temperatures, and low cost.
The plasma agents mentioned above are responsible of the lethal action of microorganisms through the interaction with the
biological material. The mechanism of action of ACP was shown to
be due to the degradation of proteins, lipids, and cellular DNA
(Mogul et al., 2003). Reactive species in plasma cause direct
oxidative effects on the outer surface of microbial cells. It was
shown that ACP is efficient to inactivate a wide range of microorganisms including bacteria (Nelson & Berger, 1989), spores
(Feichtinger, Schulz, Walker, & Schumacher, 2003; KellyWintenberg et al., 1999; Lee, Paek, Ju, & Lee, 2006), and viruses
(Terrier et al., 2009). The mechanisms of action were well reviewed
in the literature (Misra et al., 2011). Plasma was mainly used to
inactivate pathogenic or non-pathogenic E. coli in vegetable
matrices (Baier et al., 2014, 2015).
Table 1 presents some applications of mild technologies for the
inactivation of the main bacterial pathogens in foods.
4. Combining mild technology processes for destruction of
foodborne pathogens
Even though some of mild technologies can be applied alone to
achieve a determined destruction of a foodborne pathogen (for
instance, 5 log10 CFU/g or mL reductions), given the necessity to
reduce physical, biochemical, sensorial and nutritional changes in
foods, a combination of processes is frequently applied. This combination allows the optimization of microbial inactivation while
decreasing unwanted chemical and biochemical changes in the
foods. Below, a detailed assessment is presented on the application
of mild technologies (combined or not with other methods) aiming
to destroy the main foodborne pathogens. This section will provide
an overview of work done and will also serve as basis for identification of aspects demanding further investigations.
4.1. Campylobacter spp.
4.1.1. High pressure processing (HPP) alone or combined with other
techniques
The inactivation of C. jejuni (strains 35919 and 35921) by high
pressure was studied by Solomon and Hoover (2004). It was found
that the pressure resistance of the C. jejuni strains was affected by
the substrate, i.e., a protective effect was observed when the HPP
was applied in foods (ultra-high temperature (UHT) whole milk,
e). This resulted in a
UHT skim milk, soya milk and chicken pure
need to increase the pressure in 50e75 MPa to achieve the similar
log reductions. C. jejuni strains were found to present similar
sensitivity to HPP as other Gram-negative foodborne pathogens
(Jackowska-Tracz & Tracz, 2015), for which treatments of
<10 min at 300-40 MPa at ambient temperature can reach >5 log
reductions. The pressure inactivation of C. jejuni and C. coli seems to
follow first-order kinetic order which allow the application of HPP
at short times (1 min and 30 s) at ambient pressure and 70 C or at
450 MPa and 15 C and to achieve > 6 log reductions, respectively
(Lori, Buckow, Knorr, Heinz, & Lehmacher, 2007).
In another study, a reduction of 6 log10 cycles in the counts of
C. jejuni inoculated in smoked salmon was obtained through
treatments 200 MPa during 64.26 min, 300 MPa during 17.10 min,
ski, Pe,conek,
or 400 MPa for less than 5 min (Jackowska, Szczawin
& Fonberg-Broczek, 2008). While Campylobacter are known to be
sensitive to HPP and treatments combining pressure (600 MPa) and
temperature (40 C) can result in >6 log reductions, the presence of
pressure-resistant bacteria such as E. coli AW1.7 might hinder the
effectiveness of the process. E. coli AW1.7 is one of the most
pressure-resistant bacterial vegetative cells and for a process to
Fig. 4. Mechanism of action of UV-light for microbial inactivation.
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
27
achieve 4.5 log CFU/g reductions in minced poultry meat, pressure
€nzle, 2012). These
of 600 MPa and 40 C are required (Liu, Betti, & Ga
results indicate that a global assessment of the microbiota present
in the foods and also the substrate per se should be considered for
proper decisions to be made. Therefore, when dealing with mild
processing technologies, it should be taken into account that the
use of pre-established temperature/pressure binomials or combined treatments (Gunther, Sites, & Sommers, 2015) should be
avoided and these should be established case by case to avoid food
safety or spoilage issues.
considered. However, the combination of treatments must be
carefuly investigated as a synergistic effect between UV-light irradiation and other methods will not always be observed. For
example, the combination of UV-light irradiation (0.048 J/cm2) and
crust freezing (air temperature of 5 to 27 C and freezing times
varying from 6 to 70 min) resulted in no synergistic in Campylobacter inactivation on raw chicken (Haughton, Lyng, Cronin, et al.,
2012).
4.1.2. Ultrasound processing alone or combined with other
techniques
The application of ultrasounds aiming to destroy Campylobacter
has been mainly focused enhancing the safety of poultry meats.
Ultrasounds are more effective in inactivating this pathogen when
combined with mild heat conditions. Campylobacter has been
found to be sensitive to ultrasound processing, and particularly
C. jejuni presents higher susceptibility to thermosonication
compared to thermal or sonication treatments. A combined system
of steam and US (SonoSteam) built in the evisceration area in a
Danish broiler plant that works at conventional slaughter speeds of
8500 birds per hour was able to reduce the initial concentration of
Campylobacter in about 1 log₁₀ CFU per broiler carcass (Musavian
et al., 2014). Other authors evaluated the effects of steamultrasound to inactivate Campylobacter from broiler meat,
observing a significant reduction of 2.5 log10 CFU per carcass
(Boysen & Rosenquist, 2009).
Thermosonication, thermal or sonication treatments result in up
to 4.7, 1.4 and 3.2 log10 CFU reductions of C. jejuni in liquid media,
respectively (Haughton, Lyng, Morgan, et al., 2012). The inactivation of Campylobacter seems to be generally more affected by
thermosonication treatment in liquid matrices than the inoculated
poultry products. In addition, the efficiency of the inactivation
process is also affected by the intensity of the unit. Treatments done
in high-intensity units (HI) (20,000 W/L) are more efficient in
destroying Campylobacter than low-intensity unit (LI) (20 W/L)
(Haughton, Lyng, Morgan, et al., 2012).
Ultrasound can also be combined with other methods aiming to
reduce the counts of Campylobacter in the plastic craters used for
transportation of live poultry to abattoir. Ultrasound treatment
(4 kW, 3e6 min) combined with temperature (65 C) and mechanical scrubbing may lead to at least 4 log10 reduction of C. jejuni
(Allen et al., 2008). This treatment can be an alternative to the
application of soaking (55 C), followed by scrubbing the craters for
90 s and further washing at 60 C for 15 s (Allen et al., 2008),
showing that ultrasound and combined treatments with ultrasounds can also comprise alternatives for disinfection of processing
premises or utensils.
4.2.1. High pressure processing (HPP) alone or combined with other
techniques
The use of HPP aiming to destroy Salmonella in foods of animal
origin as well as in fresh and processed produce has been investigated. The impact of single- and multiple-cycle HPP treatments on
the inactivation of S. Enteritidis in chicken breast fillets was
~ ez
investigated by Morales, Calzada, Rodríguez, De Paz, and Nun
(2009). The findings indicated that an increase in the number of
cycles, resulted in an increased inactivation of S. Enteritidis in
chicken breast fillets (treatment at 300 MPa and 12 C): 0.6
log10 CFU/g to 3.3 log10 CFU/g for a 0 min cycle to a 20 min cycle,
respectively. In addition, an increase in the number of cycles
resulted in an augment in the number of injured cells of S. Enteritidis. Furthermore, the increase of pressure from 300 to 400 MPa
resulted in up to 5 log10 CFU/g reductions in the counts of S.
Enteritidis (Morales et al., 2009). The use of low temperature
(4e6 C) during HPP treatment (450 MPa during 10 min) of ground
chicken (95% lean) caused 5 log10 CFU/g of Salmonella spp. cocktail.
The combination of lower pressures and one cycle of 15 min (250 or
350 MPa) reduced Salmonella counts in 0.5 log10 or 1.7 log10 CFU/g,
respectively. On the other hand, the use of several cycles (3 cycles;
5 min per cycle) at 250 and 350 MPa resulted in 1.3 and 3.3
log10 CFU/g reduction of Salmonella counts, respectively (Sheen,
Cassidy, Scullen, Uknalis, et al., 2015). Another factor that seems
to affect the inactivation efficiency of HPP is the temperature of
treatment. For instance, HPP treaments applied to raw chicken
breast fillets at temperatures of 35 to 30 C and pressure of 300 and
400 MPa, resulted in 2e4 log10 CFU/g of Salmonella Typhimurium
(DMST 28913), respectively (Tananuwong, Chitsakun, & Tattiyakul,
2012).
In addition to chicken meat, Salmonella is also a major problem
in beef meat. In this way, the potential application of high pressure
treatments on the inactivation of S. Enteritidis was investigated (de
Alba, Bravo, & Medina, 2012). The counts of S. Enteritidis were
reduced by 3.7 and 5.9 log10 CFU/g after a processing at 450 MPa
during 5 and 10 min, respectively.
The study of HPP inactivation in specific food matrixes is relevant because food composition is known to exert a protective effect
bol, Aymerich, Monfort, &
on the microorganisms (Garriga, Gre
Hugas, 2004). In processed meat products such as dry-cured ham,
Salmonella inactivation by HPP was optimized through a response
surface approach (Bover-Cid, Belletti, Garriga, & Aymerich, 2012). A
model that allows the determination of optimum processing conditions as influenced by pressure (347e852 MPa), holding time
(2.3e15.75 min), and temperature (7.6e24.4 C) was proposed. In
addition to pressure and time, the interaction of temperature with
pressure and time is also relevant for Salmonella inactivation by
HPP. Through the model, processors can select pressure, time and
temperature conditions and further verify whether legal lethality
standards are achieved. HPP has also been studied as postprocessing treatment for the inactivation of foodborne pathogens
such as Salmonella in meat products. According to Garriga et al.
(2004), a HPP treatment at 600 MPa for 6 min at 31 C is capable
to reduce the risks associated with the presence of Salmonella in
4.1.3. UV-light alone or combined with other techniques
As for ultrasound, studies dealing with UV-light irradiation are
mainly focused on inactivation of Campylobacter in chicken meat
and chicken processed products. Studies included the use of UVlight irradiation in raw chicken (Chun et al., 2010) and in final
products (Chun et al., 2009). There were also studies aiming to
assess the inactivation efficiency of Campylobacter by the application of UV-light irradiation alone or combined with other methods.
For instance, in chicken breasts and in ready-to-eat sliced ham, UVlight irradiation processes at dosis of 8 kJ/m2 and 5 kJ/m2, respectively, led no more than 1.7 log10 CFU/g reductions of C. jejuni (Chun
et al., 2009, 2010). Therefore, given the limited inactivation effectiveness of the UV-light irradiation, if the application demands
more than 1.5e2.0 log10 CFU/g of Campylobacter, the combination of
UV-light irradiation treatment with other methods should be
4.2. Salmonella spp.
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
28
Table 1
Some examples of application of mild technologies for the inactivation of the main bacterial pathogens in foods.
Technology Parameters
HPP
PEF
UV-light
Campylobacter spp.
Salmonella spp.
Listeria spp.
E. coli
Time (min)
Dose (MPa)
Food
0.50e64.26
200e450
UHT whole milk
Poultry meat
Smoked salmon
1.00e15.75
250e852
Meat products
Tomato
Pepper
Strawberry puree
1.00e40.00
103e600
Beef; Ground beef; Beef jerky
RTE meats
LWE
Alfafa seeds
Fruit juice
Source
Solomon & Hoover, 2004
Lori et al., 2007
Jackowska et al., 2008
Liu et al., 2012
Garriga et al., 2004
Morales et al., 2009
Maitland et al., 2011
Tananuwong et al., 2012
Sheen et al., 2015a,b
de Alba et al., 2012
Neetoo & Chen, 2012
Toledo et al., 2012
Bover-Cid et al., 2012
Huang et al., 2013
1.00e30.00
100e600
Buffer
Orange juice
Pear nectar
Yogurt
RTE salads
Liquid whole eggs (LWE)
Dry-cured-ham
Beef carpaccio
Hayman et al., 2008
Guerrero-Beltr
an et al., 2011a
novas, & WeltiGuerrero-Beltr
an, Barbosa-Ca
Chanes, 2011b
Evrendilek & Balasubramaniam, 2011
Stratakos et al., 2016
de Alba et al., 2015
Luscher et al., 2004
Lee et al., 2003
Other
information
e
With US and thermal
treatment
e
Time (min)
e
Dose (kV per m) e
Food
e
11.6 106
25.00e30.00
Skim milk
LWE
Source
e
rez et al., 2012
Pina-Pe
Monfort et al., 2012a,b,c
Other
information
e
e
9.90 105-5.00 106
25.00e38.90
Buffer
Skim milk
LWE
ndez-Molina et al., 2006
Ferna
~ a et al., 2011
Saldan
Espina et al., 2014
Nisin (100e200 mg/mL)
Lemon EO (200 mg/L)
2.10 107
30.00e37.60
Buffer
Raw milk
Fruit juice
Jaeger et al., 2009a,b
Ait-Ouazzou et al., 2011, 2012,
2013
e
Time (min)
Dose
0.13e0.53
0.192 J/cm2
0.048 J/m2
0.002e5.00 kJ/m2
Sliced ham
Chicken breast; Raw
Chicken
Skim milk
Haughton et al., 2011
Haughton, et al., 2012a,b
Chun et al., 2009
Chun et al., 2010
e
e
1600-1950 J/L
0.55e13.70
200-5000 J/L
4.00e23.80
5-290 mJ/cm2
Whole milk
UHT milk
Apple Juice
Milk
Crook et al., 2015
Crook et al., 2015
Orlowska et al., 2015
Yin et al., 2015
e
e
e
e
e
5.00e30.00
24 kHz
e
e
e
Skim milk
Milk þ 1% fat
Whole milk
novas, 2008
Bermúdez-Aguirre & Barbosa-Ca
e
e
With thermal treatment
e
0.50e2.00
5 Argon [L/min] þ 0,1% O2
Corn salad
Corn salad leaves
Cucumber
Apple
Tomato
Baier et al., 2014, 2015
e
Food
Source
Other
information
US
Time (min)
Dose
Food
Source
Other
information
Plasma
Microorganisms
3.00e6.00
4 kW
30.00e40.00 kHz
Poultry meat
Broiler carcasses
Allen et al., 2008
e
Musavian et al., 2014
With thermal treatment
Time (min)
e
Dose (kV per m) e
Food
e
e
e
e
e
e
e
Source
Other
information
e
e
e
e
e
e
Morales et al., 2008
Gill and Ramaswamy (2008)
Black et al., 2010
Neetoo et al., 2009
Lowder et al., 2014
Sheen et al., 2015a,b
Monfort et al., 2012a,b,c
Espina et al., 2013
Cherrat et al., 2014
Scheinberg et al., 2014
Guerrero-Beltr
an et al., 2011a
Guerrero-Beltr
an et al., 2011b
e
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
meat products. In this study, Salmonella was not detected in meat
products submitted to HPP treatment (600 MPa for 6 min at 31 C)
after storage at refrigerated conditions (4 C) after 120 days
(Garriga et al., 2004).
Several studies have also been done on the application of HPP to
destroy Salmonella in fresh and processed produce. According to
Maitland, Boyer, Eifert, and Williams (2011), HPP can be applied as a
post-harvest approach to reduce low loads of Salmonella in diced
and whole tomatoes. These authors reported that pressures of 350,
450, and 550 MPa during 2 min resulted in 0.5, 2.2 and 3.7
log10 CFU/g of Salmonella, respectively. The practices applied after
harvest may also be important in impacting Salmonella inactivation.
~o
Neetoo and Chen (2012) showed that wetting and soaking Jalapen
and Serrano peppers affected Salmonella inactivation by HPP. The
increase in pressure from 300 to 500 MPa and the use of soaking
~ o and Serrano
and wetting increased Salmonella inactivation Jalapen
peppers as compared to unwetted produce (Neetoo & Chen, 2012).
The application of wetting and soaking seems to enhance the
inactivation efficiency of HPP due to increase in water activity of
produce tissues (Neetoo & Chen, 2012).
HPP has also been applied aiming to inactivate Salmonella in
processed fruits and vegetables. The combination of HPP and
freezing on the inactivation of Salmonella spp. inoculated in
strawberry puree was evaluated by Huang, Ye, and Chen (2013).
Freezing at 18 C during 12 weeks followed by a HPP process
(450 MPa during 2 min at 21 C) resulted in >5.5 log CFU/g in the
counts of Salmonella spp. in strawberry puree. Treatments of
600 MPa for 5 or 8 min led to 5.9 and 6.5 log10 cycles of Salmonella
rez
spp. in Spanish potato omelet (tortilla de patatas) (Toledo, Pe
lvez, 2012).
Pulido, Abriouel, Grande, & Ga
4.2.2. Pulsed electric fields treatment alone or combined with other
techniques
Studies dealing with the application of pulsed electric field
technology for Salmonella inactivation commonly consider the
combination with other methods. Despite this, the number of
decimal reductions caused by this technology seem to be limited.
For instance, the effect of the combination between PEF (10, 20, and
30 kV/cm at treatment times ranging between 60 and 3000 ms) and
cinnamon (1, 2.5 and 5% (w/v)) on the fate of S. Typhimurium in
rez et al., 2012). Even though
skim milk (SM) was studied (Pina-Pe
the results indicated the synergistic effect of PEF and cinnamon, the
number of decinal reductions was not superior to ~2 log10 cycles
using a PEF treatment of 30 kV/700 ms in SM supplemented with 5%
cinnamon. Another example of PEF combined with other methods
~ a, et al.
for inactivation of Salmonella is the study by Monfort, Saldan
(2012). PEF was combined with heat (52e60 C for up to 3.5 s) and
additives (EDTA or triethyl citrate (TC)) aiming to enhance the
inactivation of Salmonella in liquid whole egg (LWE). The combined
treatments resulted not only in the decrease of heat resistance of
Salmonella serovars tested, but also in the reduction of the heat
treatment time in up to 92 times depending on the condition. In
this study, a variability in terms of inactivation efficiency of Salmonella serovars was reported. Amongst the seven Salmonella serotypes tested, Salmonella Senftenberg and Salmonella Enteritidis
4396 were shown to be less affected by the combined treatment
~ a, et al., 2012) highlighting the importance
applied (Monfort, Saldan
to consider the strain variability in the design of processes based on
mild technologies. A PEF (25 kV/cm; 200 kJ/kg) treatment followed
by pasteurization (60 C/3.5 min), in presence of 1% TC or 10 mM
EDTA, represents a promising alternative to industrial ultrapasteurization which may reaches up to 70e71 C/1.5 min
(Monfort, Sagarzazu, et al., 2012).
29
4.2.3. Ultrasound processing alone or combined with other
techniques
As for PEF, the inactivation efficiency of ultrasound is enhanced
through the combination with other methods. For instance, Salmonella Enteritidis inactivation in liquid whole egg (LWE) as
affected by ultrasound, PEF, heat and hydraulic high pressure was
studied. The treaments applied resulted in additive effects rather
than synergism. The best combination was hydraulic high pressure
followed by ultrasound treatment, which led to ~3 log10 CFU/mL
reduction of Salmonella in LWE (Huang et al., 2006). Similarly,
resistance to manosonication and monothermosonication in LWE
of three Salmonella serovars (S. Enteritidis, S. Typhimurium, and S.
~ as et al., 2000; Pag
Senftenberg) was studied (Man
an et al., 1999;
n, & Sala, 1998). Results demonstrated that S.
Raso, Pag
an, Condo
Senftenberg showed the highest resistance among the three studied
serovars.
Nonetheless,
treating
LWE
with
manothermosonication at 60 C was effective to reduce S. Senftenberg
775 W by 3 log10 CFU/mL, compared to only 0.5 log10 CFU/mL when
n et al.,
using conventional heating at the same temperature (Paga
1999).
4.2.4. UV-light alone or combined with other techniques
The combination of UV-light with mild temperatures was
applied to destroy S. enterica serovars (Gay
an, Serrano, Raso,
n, 2012). Results showed that the required doses
Alvarez,
& Condo
to cause reduction of 99.99% of the initial load ranged from 18.03 to
12.75 J/mL for S. enterica serovar Typhimurium STCC 878, and
S. enterica serovar Enteritidis ATCC 13076, respectively. It was also
shown that UV-tolerance was unaffected by the pH and water activity of the treated medium, whereas an exponential decrease was
noticed by increasing the absorption coefficient. UV-light and
heating presented an inactivating synergistic effect when simultaneously applied. However, these effects were mainly observed
when UV-light is applied after the heat treatment (UV-H). The
proposed combination of UV-light and heat treatments was found
to be a promising alternative in food industry for the pasteurization
of liquid foods with high UV absorptivity, such as fruit juices.
In meat products such as ready-to-eat (RTE) sliced ham a dose
needed to reduce the initial microbial load of S. enterica serovar
Typhimurium by 90% through UV-light irradiation (1000e8000 J/
m2) was 2.39 J/m2 (Chun et al., 2009). The highest dose used
(8000 J/m2) was efficient to reduce the counts of S. Typhimurium by
2.0 log10 CFU/g, respectively. In chicken breast, an UV-light treatment with doses varying from 0 to 5 kJ/m2 resulted in no more than
1.3 log10 CFU/g of S. enterica serovar Typhimurium (Chun et al.,
2010). UV-light treatment (0.192 J/cm2) caused upt to 1.3 and 4.2
log10 CFU/cm2 of S. enterica serovar Enteritidis on raw chicken fillet
and packaging and surface materials (Haughton et al., 2011).
4.3. Listeria spp.
4.3.1. High pressure processing (HPP) alone or combined with other
techniques
HPP has been used alone or combined with different methods
aiming to destroy L. moncoytogenes. HPP process combined with
mint essential oil was investigated for the inactivation of
L. monocytogenes and L. innocua in a yogurt drink (ayran)
(Evrendilek & Balasubramaniam, 2011). A HPP treatment (600 MPa,
300 s) caused > 5 log10 CFU/g in the initial load of L. monocytogenes
and L. innocua, while the addition of mint essential oil boosted the
inactivation of L. monocytogenes and L. innocua by more than 6
log10 CFU/mL. In addition, when the combined process was used
HPP pressure values of 100e300 MPa were enough to obtain
similar inactivation of L. monocytogenes and L. innocua. When
coriander essential oil was added to active packaging and combined
30
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
with HPP (500 MPa for 1 min), resulted in a synergistic effect and
led to reduction in the counts of Listeria below the limit of quantification during 60 days of storage at 4 C. On the other hand, the
growth of Listeria was slowed down but not completely inhibited
when the RTE chicken breast was stored at 8 C. This study showed
that active packaging combined with in-package HPP treatment
could be used as an approach to reduce the risk of L. monocytogenes
in RTE chicken without changing the organoleptic and sensory
properties. The addition of Stevia rebaudiana Bertoni extracts that
contain high amounts of natural antimicrobials (0e2.5% w/v) to a
fruit extract matrix led to increase in the inactivation of
L. monocytogenes by HPP treatment (300e500 MPa, 5e15 min). Up
to 5 log10 CFU/g log reductions of L. monocytogenes were obtained
when combining HPP (453 MPa, 5 min) with 2.5% (w/v) of Stevia
(Barba, Criado, Belda-Galbis, Esteve, & Rodrigo, 2014).
HPP treatments (200e600 MPa/5e20 min/20e40 C) caused
more than 4 log10 CFU/g reduction of L. monocytogenes inoculated
in Queso Fresco (Tomasula et al., 2014). Nonetheless, as
L. monocytogenes is psychrotrophic microorganism, the use of other
preservation method is needed to avoid its growth during chilled
storage of Queso Fresco (Tomasula et al., 2014). In this way, an
approach to inhibit L. monocytogenes in RTE foods comprises the
combination of HPP and protective cultures. This approach may be
very useful to overcome failures in the cold chain that could allow
the growth of L. monocytogenes. This strategy has been studied in
salads with pH values of 4.3 and 5.6, added of a protective culture
(Weissella viridescens), treated through HPP (400 MPa during
1 min), following storage at 4 and 12 C. While HPP caused 4.0 and
1.5 log10 CFU/g reductions of L. monocytogenes in RTE salad with pH
4.3 and 5.6, respectively (Stratakos et al., 2016), W. viridescens was
able to inactivate/inhibit L. monocytogenes during storage of RTE
salads depending on the pH and storage temperature. A HHP
treatment with a post-processing barrier to inhibit further growth
of pathogens was studied by de Alba, Bravo, and Medina (2015). The
combination of HPP (450 MPa, 10 min) with lactoperoxidase (LP)
system or lactoferrin (LF) failed to enhance the inactivation and
inhibition of L. monocytogenes growth in sliced dry-cured-ham
during storage for 60 days at 8 C (de Alba et al., 2015). In
another study, Bravo, de Alba, and Medina (2014) reported that a
HHP (450 MPa, 5 min) combined with lactoperoxidase system
(LPOS) or activated lactoferrin (ALF) applied in cured beef carpaccio
was effective only against S. Enteritidis and E. coli O157:H7 (Bravo
et al., 2014).
4.3.2. Pulsed electric fields treatment alone or combined with other
techniques
PEF was also effective to inactivate different Listeria strains in
food products when applied either alone or in combination with
other techniques. The energy required by PEF to inactivate
L. innocua inoculated in 0.2% skim milk (SM) was lower than that
consumed by thermal pasteurization. It was demonstrated that the
energy densities required to reduce the microbial load by 3
log10 CFU/g reductions were of 120, 212, and 270 kJ/L, which
correspond to input voltages of 30, 35, and 40 kV, respectively
ndez-Molina et al., 2006).
(Ferna
Even though PEF can be combined with other methods, it seems
temperature will hold the main influence on the inactivation of
~a
microorganisms. Through a response surface approach, Saldan
et al. (2011) found that the increase in temperature from 4 to
50 C during PEF treatment resulted in an increase of the inactivation of L. monocytogenes by 3 log10 CFU/g cycles. Further, the
combination of PEF, with low pH (3.5), nisin (200 mg/mL) and mild
temperature (50 C) caused up to 5.5 log10 CFU/g reductions in the
populations of L. monocytogenes.
The combination of PEF (25 kV/cm and 100 kJ/kg) followed by
heat (60 C, 3.5 min) applied to LWE supplemented with 200 mL/L of
lemon EO resulted in inactivation of 4 log10 cycles of
L. monocytogenes. On the other hand, individually processes resulted in inactivation of <1.5 log10 cycles of this bacterium. A synergism was reported, which could comprise an alternative to
industrial ultrapasteurization at lower temperature to provide
microbiologically safe LWE products (Espina, Monfort, Alvarez,
n, 2014). This study also reported that the
García-Gonzalo, & Paga
inactivation efficiency of a combined process with PEF and mild
heat will be dependent upon the EO applied (Espina et al., 2014). It
is known that food componentes influence the antimicrobial activity of natural compounds.
4.3.3. Ultrasound processing and UV-light alone or combined with
other techniques
The inactivation efficiency of ultrasound treatment combined
with heat treatment seems also to be affected by food composition.
Bermúdez-Aguirre and Barbosa-C
anovas (2008) found that
increasing the fat content in milk decreased L. innocua inactivation.
While 2.5 log reductions of L. innocua was observed in whole milk
(3.47% of fat), in fat free milk up to 4.9 log reductions were observed
after 30 min of treatment. The results obtained can be related to the
influence of food composition on the efficiency of ultrasound
treatment. Fat is known to reduce the penetration of ultrasound
and also to impact on energy distribution. In addition, as cavitation
is very important for the inactivation through ultrasound, different
solid contents in milk will result in different boiling point of the
product, which affects cavitation and microbial inactivation
(Earnshaw et al., 1995). The importance of cavitation for microbial
inactivation has been corroborated by Bermúdez-Aguirre, Mawson,
and Barbosa-C
anovas (2011). These authors reported that while
thinning in cell walls was observed in heat-treated samples, in the
samples submitted to thermo-sonication, the formation of pores
through the cell membranes was observed. After 10 and 30 min of
sonication breakage lines and broken cells were observed, respectively (Bermúdez-Aguirre et al., 2011).
The effect of UV-light in a thin-film turbulent flow combined
with heat on the inactivation of milkborne microorganisms was
investigated and this treatment was also reported to be feasible for
milk processing (Crook et al., 2015). L. monocytogenes was found to
be the most UV resistant microorganism amongst seven tested
(L. monocytogenes, Serratia marcescens, S. Senftenberg,
Y. enterocolitica, A. hydrophila, E. coli, and S. aureus), as exposure to
UV-light at 2000 J/L was needed to cause 5 log10 reduction of this
bacterium inoculated in whole milk.
4.4. Escherichia coli
4.4.1. High pressure processing (HPP) alone or combined with other
techniques
The application of single-cycle high-pressure treatment of
400 MPa (12 C) for 1 min and 20 min for the inactivation of E. coli
O157:H7 in ground beef resulted in 0.82e4.38 log10 CFU/g reductions, respectively. On the other hand, applying multiple-cycle
treatments resulted 4.38 and 4.96 log10 CFU/g reductions at
400 MPa (12 C) for four 1-min and three 5-min cycles, respectively
~ ez, 2008). A HPP treatment at
(Morales, Calzada, Avila, & Nun
600 MPa with a holding time of 3 min applied in RTE meats
(Hungarian salami and All Beef salami) was able to reduce E. coli
O157:H7 load by more than 4 log10 CFU/g (Gill & Ramaswamy,
2008). The combination of a HPP treatment of ground beef at
400 MPa for 10 min followed by freezing enhanced the inactivation
of E. coli O157:H7 (Black, Hirneisen, Hoover, & Kniel, 2010). Another
study showed that previous freezing (35 C) followed by a HPP
treatment at 551 MPa pressure for 4 min resulted in 1.7 log10 CFU/g
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
reduction of E. coli O157:H7 inoculated in beef semitendinosus
(Lowder, Waite-Cusic, & Mireles DeWitt, 2014).
HPP treatments have also been studied aiming to inactivate
E. coli O157:H7 in fermented/dried meat products such as Genoa
salami. HPP treatments at 600 MPa or at 483 MPa for 1e12 min
caused additional inactivation of E. coli O157:H7 inoculated in
Genoa salami that reached 5.8 log10 CFU/g reduction (Porto-Fett
et al., 2010). The combination of HPP and boiling water seems to
be an alternative for E. coli O157:H7 inactivation during beef jerky
processing as a treatment at 550 MPa and during 60 s result in up to
4.4 log10 CFU reductions per strip of this bacterium. E. coli O157:H7
was found to be more sensitive to the treatment than S. aureus and
L. monocytogenes (Scheinberg, Svoboda, & Cutter, 2014).
Heterogeneity in HPP resistance of STEC has been shown by
Sheen, Cassidy, Scullen, & Sommers (2015). These authors found
D10 values (HPP conditions necessary to cause 1 cyle reduction in a
target microorganism count) for 39 STEC strains varying from 0.89
to 25.7 min when subjected to HPP (350 MPa, 4 C, up to 40 min) in
ground beef (80% lean). This reinforces the need of proper assessment of microbial target strains used in the design of mild
technologies-based processes for microbial inactivation. An error in
selecting an appropriate strain may severely impact on the lethality
of the process and further on public health.
HPP has also been used to destroy E. coli O157:H7 in vegetables,
such as alfafa seeds. A treatment at 600 MPa at 40 C caused 5
log10 CFU reductions of E. coli O157:H7 inoculated in alfafa seed
samples. Other treatments with reduced pressure values or
increased time resulted in similar lethal effects on E. coli O157:H7,
i.e., 550 MPa for 2 min and 40 C, 300 MPa for 2 min and 50 C, and
400 MPa for 5 min and 45 C. Nonetheless, considering the effects
for seeds's germination, the first treatment (550 MPa for 2 min and
40 C) was considered the most appropriate for practical applications (Neetoo, Pizzolato, & Chen, 2009).
4.4.2. Pulsed electric fields, ultrasound processing and UV-light
alone or combined with other techniques
Fewer studies on the use of pulsed electric fields, ultrasound and
UV-light for E. coli inactivation, including pathogenic types, have
been found in comparison to HPP, for instance. This can be related
to characteristics of food matrixes in which pathogenic E. coli has an
importance or due to the fact that other technologies (HPP, for
instance), are more efficient from both microbial inactivation and
economical points of view. Despite this, as for other technologies,
the combination of PEF and EO has been evaluated for inactivation
of E. coli O157:H7 with increase in the treatment efficiency
depending on combination of hurdles and also on the type EO.
Generaly, up to 5 log10 CFU/mL reductions can be obtained as
influenced by several factors (Ait-Ouazzou et al., 2011, 2012, 2013;
~ a, Monfort, Condo
n, Raso, & Alvarez,
Saldan
2012).
A manothermosonication treatment (400 kPa/59 ºC) of 1.4 min
caused 5 log10 reductions of E. coli in apple cider while 3.7 min and
15.9 min were needed to achieve the same reduction through
thermosonication and sonication alone, respectively (Lee et al.,
2013; Ugarte-Romero, Feng, Martin, Cadwallader, & Robinson,
2006).
UV-light combined or not with dimethyl dicarbonate (DMDC)
(25, 50, and 75 mg/L), and heat (55 C) were used for inactivation of
n, Raso, Condo
n, &
E. coli in commercial apple (Gouma, Gaya
Alvarez,
2015). A synergistic effect between the techniques was
observed and it was found that the addition of 75 mg/mL of DMDC
followed by UV-light and heat at 55 C caused 5 log10 CFU/mL reductions of E. coli in commercial apple after only 1.8 min (Gouma
et al., 2015).
The type of monochromatic UV-light wavelengths (222, 254,
and 282 nm) was found to influence on the inactivation of E. coli
31
O157:H7 in bovine milk. Yin et al. (2015) reported higher inactivation of this bacterium when treatment was done using UV-light
at the wavelength of 254 nm, when compared inactivation obtained at 222 and 282 nm (Yin et al., 2015).
4.4.3. Atmospheric cold plasma
Cold plasma, known also as non-thermal atmospheric-pressure
plasma, was efficiently applied to inactivate different microorganisms. For instance, this technique was used for the treatment of
fresh fruits and vegetables (Baier et al., 2014). In some produce
items, non-thermal atmospheric-pressure plasma treatment can
result in up to 4.7 log10 CFU reductions of E. coli. The inactivation
efficiency seems to vary depending on the produce item (Baier
et al., 2015). Non-thermal atmospheric-pressure plasma seems to
be a promising and very cost-effective technology for microbial
inactivation.
5. Conclusions
As can be seen in Suplementary Fig. S5, HPP is the most studied
mild processing technology applied for microbial inactivation followed by UV-light. The superior HPP data may based on three facts;
the pressure-induced killing of bacteria was discovered already in
the 19th century, HPP can be applied to a diverse range of foods,
and HPP seems to be more efficient to destroy foodborne microorganisms. Contrary, the few numbers of data dealing with plasma
inactivation of foodborne microorganisms seems to be due to a
more recent application of this technology for food processing. As
such, several developments and barriers have to be overcome so
this technology can be widely applied.
The mild processing technologies HPP, PEF, US, UV-light, and
ACP constitute efficient alternatives to conventional heat inactivation methods (sterilization and pasteurization). Nonetheless, the
choice of a mild technology for food processing demands careful
analysis weighting the installation cost, the energy consumption,
environmental issues, impact on and of food formulation, the
complementarity with existing equipment and the effectiveness of
the technology, combined or not, to deliver a specified destruction
of the microbial target which will affect product's safety and shelflife. Through this review it was possible to notice that a few limited
number of studies deal with the determination of inactivation kinetics of target microorganisms subjected to a specific mild technology. Despite this, the determination of inactivation of kinetics is
of major relevance for the design of a preservation method aiming
to ensure a specified destruction of a microbial target. Once the
changes in the environmental conditions over the inactivation kinetic parameters are estimated, a preservation process can be safely
designed and further validated. However, most studies dealing
with microbial inactivation by mild technologies have focused on
the determination of the number of decimal reductions rather than
inactivation kinetics associated with a specific formulation and
processing conditions. Conversely, this seems not adequate as it
does not allow readily comparisons regarding foodborne pathogens' resistance to a specified condition. In addition, the determination of the number of decimal reductions do not permit to
intuitively assess the impact of environmental conditions in the
rate of inactivation kinetics, which is very important as most large
scale processes work under dynamic (variable) conditions.
Furthermore, for foods subjected to mild processing, not only microbial inactivation is relevant, but also the presence of injured cells
due to sublethal inactivation. Because of this, special attention
should be taken for the development of more robust food formulations throught he concept of hurdle technology. These formulations should be able to inhibit the growth of any injured cells
possibly present in the product after mild processing and prone to
32
F.J. Barba et al. / Trends in Food Science & Technology 66 (2017) 20e35
reach levels that may result in public health issues. These facts also
shed light on the significance of assessing the robustness of food
formulations through challenge tests for proper decision-making
regarding the best formulation for a specific mild technology of
food preservation.
Another key point regarding microbial inactivation through
mild technologies is the ability to accurately determine the inactivation kinetic parameters. This is even more relevant to minimal
processing because a lack of precision may greatly impact on survival of a target microorganism that will further cause severe public
health issues. In this way, variability in microbial inactivation is a
phenomena that really matters for the safety of mild processed
foods (Aryani, den Besten, Hazeleger, & Zwietering, 2015;
Koutsoumanis,
Lianou,
&
Gougouli,
2016;
Lianou
&
Koutsoumanis, 2013a, 2013b). Therefore, the variability in microbial inactivation (Koutsoumanis et al., 2016) and the recovery of
injured microorganisms deserve great attention. Finally, in an era of
consumer's demands for mild processed foods, an advanced
knowledge of microbial ecology (of raw materials, food formulations, environment of food processing), storage and commercialization conditions along with data on microbial behavior in foods
(inactivation and growth) seem to be even more important for the
production of shelf-stable and safe foods.
Acknowledgements
F.J. Barba was supported from the Union by a postdoctoral Marie
Curie Intra-European Fellowship (Marie Curie IEF) within the 7th
European Community Framework Programme (http://cordis.
europa.eu/fp7/mariecurieactions/ief_en.html) (project number
626524 dHPBIOACTIVE d Mechanistic modeling of the formation
of bioactive compounds in high pressure processed seedlings of
Brussels sprouts for effective solution to preserve healthy compounds in vegetables). L.P.-Silva and A.S. Sant’Ana are grateful to
CNPq (Conselho Nacional de Desenvolvimento Científico e Tec~o de
gico) (Grant #302763/2014-7) and CAPES (Coordenaça
nolo
Aperfeiçoamento de Pessoal de Nível Superior) (PROEX/CAPES
#3300301702P1) for the financial support for the projects undertaken at the Laboratory of Quantitative Food Microbiology, University of Campinas, Brazil.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.tifs.2017.05.011.
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