Trends in Food Science & Technology 107 (2021) 31–37

Contents lists available at ScienceDirect

Trends in Food Science & Technology

journal homepage: www.elsevier.com/locate/tifs

High-pressure processing in inactivation of Salmonella spp. in food products

Rubén Agregán a, Paulo E.S. Munekata a, Wangang Zhang b, *, Jian Zhang b,
Cristina Pérez-Santaescolástica a, José M. Lorenzo a, c, **
a
Centro Tecnológico de la Carne de Galicia, Adva. Galicia n◦ 4, Parque Tecnológico de Galicia, San Cibrao das Viñas, 32900, Ourense, Spain
b
College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China
c
Área de Tecnología de los Alimentos, Facultad de Ciencias de Ourense, Universidad de Vigo, 32004, Ourense, Spain

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Salmonella is a pathogen that can contaminate a wide variety of foods and caused many outbreaks
Salmonella worldwide. Nowadays, the food industry mainly uses thermal processing to improve the safety and shelf life of
Non-thermal technology foods. However, thermal treatment such as pasteurization may affect the fresh-like characteristics of a food
Emerging technology
product. This fact has pushed the food sector to explore a solution that preserves the fresh-like properties of
High hydrostatic pressure
foods.
Food product
Food safety Scope and approach: High hydrostatic pressure (HHP) is an emerging technology that has been studied and is seen
as a real alternative to thermal procedures in food decontamination. This article has reviewed recent findings of
its application in food products to increase the safety against Salmonella spp.
Key findings and conclusions: HHP have potential to preserve food and inactivate Salmonella spp. at the same level
of thermal pasteurization and also preserve fresh-like properties in vegetable and animal products. More intense
HPP conditions are necessary to inactivate these bacteria in solid food than in liquid ones. Moreover, the use of
HHP with other hurdles can improve the reduction of Salmonella spp. counts and prevent their recovery during
storage. Further research might help overcome the low effect in some food products with high fat, protein and
sugar content as well as low water activity that reduce the effectiveness of HPP to inactivate these bacteria.

1. Introduction
Salmonella spp. are bacteria belonging to the family Enterobacteri­
aceae, are facultatively anaerobic gram-negative rod-shaped bacteria
(bacillus) and a pathogen related to many foodborne outbreaks
(Bover-Cid, Belletti, Aymerich, & Garriga, 2017), and its presence in
food has recently been reported in different products that have caused
food poisonings all over the world (Table 1) (Ashton et al., 2015; Inns
et al., 2015). Salmonellosis often causes fever, abdominal discomfort,
diarrhea, and vomiting in hosts. This disease is a serious threat to public
health, especially for young and older as well as in immunosuppressed
groups, who can have more severe symptoms (Mąka & Popowska, 2016).
For this reason, it is essential to offer products with high microbiological
quality on the market. Until the date, two species of Salmonella have
been identified, S. bongori and S. enterica. The latter is in turn divided
into more than 2500 different serovars, and of these, two serovars,
Enteritidis and Typhimurium are associated with more than half of Sal­
monella poisoning cases worldwide (Alghoribi et al., 2019; Saleh et al.,
2019; Wei et al., 2019).
Thermal pasteurization is the quintessential classic food decontam­
ination process and is still widely used today. However, the use of heat
may affect the characteristics of the product, such as color, flavor, or
nutritional value. Regarding the effect in Salmonella spp., thermal pro­
cessing can kill these bacteria in different foods, such as whole liquid egg
(Gurtler, Juneja, Jones, & Purohit, 2019), milk powder (Wei et al.,
2020), and flaxseeds (Malekmohammadi, Shah, Townsend Ramsett, &
Bergholz, 2020).
Conversely, high hydrostatic pressure (HHP) is a non-thermal pres­
ervation technology that has the potential to inactivate pathogenic mi­
croorganisms and preserve the natural characteristics of food. This
technology is also safe, energy-efficient, fast, and waste-free, and can be
applied to both liquid and solid products (Priyadarshini, Rajauria,

* Corresponding author.
** Corresponding author. Centro Tecnológico de la Carne de Galicia, Adva. Galicia n◦ 4, Parque Tecnológico de Galicia, San Cibrao das Viñas, 32900, Ourense,
Spain.
E-mail addresses: wangang.zhang@yahoo.com (W. Zhang), jmlorenzo@ceteca.net (J.M. Lorenzo).

https://doi.org/10.1016/j.tifs.2020.11.025
Received 23 July 2020; Received in revised form 10 November 2020; Accepted 29 November 2020
Available online 3 December 2020
0924-2244/© 2020 Elsevier Ltd. All rights reserved.
R. Agregán et al. Trends in Food Science & Technology 107 (2021) 31–37

Table 1 The presence of Salmonella spp. in food is certainly high and it is

Some Salmonella outbreaks worldwide in recent years. scattered in many food products. In the plant environment, it has been
Salmonella spp. Outbreak Location Year Reference observed in crops, including lettuces (Abatcha, Effarizah, & Rusul,
food 2018), bean sprouts, coriander, spinach (Abatcha et al., 2018), and
Salmonella enterica Chicken China 2018 Jiang et al. ground cinnamon, garlic powder, onion powder, red chili pepper pow­
serovar legs (2020) der and green tea (Barrere et al., 2020). Food from animal origin is
Enteritidis undoubtedly one of the main sources of Salmonella. Among these foods,
Salmonella enterica Eggs United 2014 Inns et al. poultry products have a central role due to the many reported cases of
serovar Kingdom (2015)
Enteritidis phage
salmonellosis in humans (Modzelewska-Kapitula & Maj-Sobotka, 2014).
type 14 b Other major sources of this pathogen, which cause a significant number
Salmonella enterica Chicken United 2013–2014 Gieraltowski of outbreaks, include beef, chicken, turkey, pork, milk, and derived
serovar States and et al. (2016) products. Additionally, the aquatic environment is also an important
Heidelberg Puerto
source of foodborne diseases, including salmonellosis. Research has
Rico
Salmonella enterica Mayonnaise States of 2013 Ashton et al. found Salmonella in fresh fish, fish meal, oysters, shrimps, and frog legs,
serovar Jersey (2015) especially in areas contaminated with fecal matter.
Typhimurium In this sense, it is important to highlight that preventing contami­
DT 8 nation is the first step to prevent Salmonella spp. outbreaks by properly
Salmonella enterica Scraped United 2012 Hoffmann
serovar Bareilly tuna States et al. (2016)
treating water prior to use in agriculture (Allende & Monaghan, 2015).
Once food and water innocuity are achieved prior to processing, the
chances of contaminating food with Salmonella reduces and the impor­
O’Donnell, & Tiwari, 2019). tance of proper processing to ensure the inactivation of these bacteria
The study of the ability of HHP to reduce the population of Salmo­ raise as one of the strategies to increase food safety.
nella in food products is of great importance for the food industry since
egg or meat products are susceptible to present this pathogen. In addi­ 3. High hydrostatic pressure (HHP) to inactivate Salmonella in
tion, the application of heat can modify the physicochemical charac­ food products
teristics, nutritional value, and sensory properties of foods. This review
aimed to comment the results of recent research in the field of high 3.1. High hydrostatic pressure (HHP) technology: principles of operation
pressures for the elimination of Salmonella in food products, offering a and germicidal mechanism
perspective of the effectiveness of this technology in preserving different
food products with different physical properties, as well as the limita­ Heat processing has been commonly used to inactivate microor­
tions intrinsic to food that affect treatment. ganisms and enhance food safety. However, thermal processes may
affect the properties of food, such as the loss of nutritional value or
2. Presence of Salmonella in food: A global issue alteration of sensory properties. Moreover, the use of thermal processing
is not a valid option to increase the safety of foods that are commer­
Many Salmonella outbreaks have been reported in the last few years cialized in “raw” form (such as liquid egg products) or for products that
throughout the world (see Fig. 1), associated with the consumption of use other strategies (ripening for dry-cured ham and fermentation for
different foods, such as egg (Moffatt et al., 2016) and meat and vegetable sausages, for instance) due to the drastic reduction in the quality and
products (Jiang et al., 2020). Salmonellosis affected up to 1 million acceptance of food product.
people in the United States annually, and the European Union confirmed At this point, alternative technologies that enhance safety and better
more than 48,000 cases were registered in 2018 (EFSA, 2019). In both preserve food characteristics are interesting options for the food in­
regions of the world, salmonellosis events were mainly attributed to dustry. HHP is a non-thermal technology that offers this advantage, and
Salmonella enterica serovars Enteritidis and Typhimurium. its performance together with its profitability makes it a viable

Fig. 1. Worldwide spread of Salmonella in a wide variety of foods.

32
R. Agregán et al.
alternative to thermal processes. The growth that this technology has
experienced in the last decades had a great impact on the processing of
food. In the early 1990s, this equipment was mainly found in research
centers and universities. However, since the beginning of the 21st cen­
tury, the number of units around the world has been increasing expo­
nentially. Nowadays, HHP is a reality in food production. Some
processing lines of foods, such as fruits, vegetables, seafood, and eggs,
already have this technology, which has been welcomed by the
consumer.
HHP consists of applying high pressures between 100 and 800 MPa
at ambient temperature or applying mild heating with the aim of inac­
tivating pathogenic and spoilage bacteria, yeasts, molds, viruses, and
even spores to offer microbiology stable and safe products (see Fig. 2)
(Balasubramaniam, Martínez-Monteagudo, & Gupta, 2015). Food sub­
jected to this pressure responds according to 3 basic principles, which
determine its behavior.
- Le Chatelier’s principle: pressure enhances any reaction, conforma­
tional change, or phase transition if volume decreases.
- Principle of microscopic ordering: if pressure increases and temper­
ature remains constant, the degree of molecular ordering of the
treated product also increases.
- Isostatic principle: the size and geometry of the products do not in­
fluence compression. Uniform and multidirectional pressure com­
presses the food and once it stops, the food returns to its original
shape.
Industrial high-pressure processing is usually carried out in a batch
mode. This type of equipment generally consists of the following ele­
ments: (a) a vessel where the product is placed to be treated; (b) closures
to seal this vessel; (c) a yoke to protect closures from pressure; (d) a
pumping system to pressurize the vessel; (e) and a fluid that transmits
the corresponding pressure. In laboratories or pilot plants, oil or water
with monopropylene glycol mixture is generally used to prevent corro­
sion and to provide a wider range treatment temperature. However, on
an industrial scale, pure water is always used (Daryaei, Yousef, &
Balasubramaniam, 2016). This technology favors the reduction of the
microbial population in food, increasing the shelf life and enhancing
food safety (see Fig. 3). The main mechanism of action of high pressures
is the irreversible alteration of microbial cellular structure. Both mem­
brane and cell wall are damaged, which increases cell permeability and
Fig. 2. Basic diagram of a high-pressure equipment in batch operation with indirect pressurization.
33
Trends in Food Science & Technology 107 (2021) 31–37
leads to interruption of metabolism. In addition, the loss of the sec­
ondary and/or tertiary or quaternary structure of large molecules and
the modification of complex organized structures, such as the efflux
pump protein, ATPase activity, and ribosome, are favored and leads to
microbial death (Zhang, Wang, Zeng, Han, & Brennan, 2019).
3.2. High hydrostatic pressure (HHP) effect on reducing Salmonella spp.
in vegetable products
Washing fruits and vegetables has been recognized as an ineffective
procedure in removing indigenous microorganisms and pathogens
(Bhilwadikar, Pounraj, Manivannan, Rastogi, & Negi, 2019). This fact
might be related to different Salmonella outbreaks associated with
contaminated vegetables, fruits, and juices, raising consumers’ concerns
(Allison, Daniels, Chowdhury, & Fouladkhah, 2018). Hence, to prevent
these outbreaks and improve food safety, an update of control proced­
ures in the industry and the drive for innovation are necessary. In this
sense, processes, such as peeling, boiling, and blanching of vegetable
materials have been widely studied as decontamination methods.
However, these procedures can affect the quality of the product,
destroying bioactive compounds, such as flavonoids or carotenoids and
micronutrients (Bhilwadikar et al., 2019). HHP can improve safety is­
sues with minimal impact on the physicochemical and nutritional
quality of the product. In this sense, studies were carried out to char­
acterize the effect of HHP in the viability of Salmonella spp. in vegetable
products (Table 2).
An example of the combined treatment was the study carried out by
Shahbaz et al. (2016), in which they used TiO2-UV photocatalysis
together with HHP for the preservation of an apple juice. TiO2-UV
photocatalysis is a non-thermal technique, not yet fully developed,
based on the degradation of pathogens in aqueous conditions by
oxidation using ultraviolet (UV) light. The results showed a synergistic
effect of both treatments. With an energy dose of 8.45 J/cm2 and a
pressure of 400 MPa applied for only 1 min at room temperature (25 ◦ C),
a reduction of 7.2 log CFU/mL in the S. Typhimurium counts was ach­
ieved. Other recent research carried out in fruit juices have also achieved
satisfactory results in the elimination of Salmonella (Petrus, Churey, &
Worobo, 2020). It is well known that the use of high temperatures in the
treatment of juices is deleterious for their nutritional quality (Shahbaz
et al., 2016). One of the main challenges for the industry is to provide
juices with a quality close to that of those freshly squeezed, regardless of
R. Agregán et al. Trends in Food Science & Technology 107 (2021) 31–37

Fig. 3. Salmonella flow through the food chain and pasteurization treatment using high hydrostatic pressure (HHP).

Table 2
Treatments with high hydrostatic pressure (HHP) on plant products reported in literature and the corresponding logarithmic reductions found in Salmonella
population.
Salmonella sp. Plant product Pressure Time Temperature Log Culture media Reference
(MPa) (min) (◦ C) reduction

Salmonella enterica serovar Enteritidis, serovar Orange juice 35 10 25 0.75 log Analysis by using Allison et al. (2018)
Montevideo, serovar Newport, serovar Anatum, 103 cfu/ml Proc Power of SAS9.2
and serovarTyphimurium 241 2 25 0.53 log software
cfu/ml
4 0.69 log
cfu/ml
8 1.44 log
cfu/ml
10 1.88 log
cfu/ml
380 2 25 2.76 log
cfu/ml
4 5.56 log
cfu/ml
8 25 >7 log cfu/
10 ml
Salmonella enterica serovar Poona RM 2350, serovar Cantaloupe 300 5 8 (i) 2.7 log cfu/ TSA and XLT4 Mukhopadhyay
Newport H1275, and serovar Stanley H0558 puree g et al. (2016)
15 (i) 3.1 log cfu/
g
400 5 8 (i) 4.8 log cfu/
g
15 (i) 5.8 log cfu/
g
500 5 8 (i) ≥7 log cfu/
15 (i) g

TSA: Tryptic Soy Agar; XLT4: Xylose Lactose Tergitol.

(i): initial treatment temperature.

the subsequent processing. HHP offers in this case a clear advantage over
thermal treatments, presenting itself as a technology with good pros­
pects for the future. In fact, HHP is already being used successfully in
commercial juice processing (Petrus et al., 2020).
HHP has also shown effectiveness against Salmonella in other fruit-
based products. Hurtado et al. (2015) treated fruit smoothies for
retailing lines using different pressures and times, and they found that
applying 350 MPa for 5 min (initial temperature of 9–10 ◦ C and
maximum temperature below 25 ◦ C) improved the microbial stability 30
days during refrigerated storage, with the total absence of Salmonella.
On the other hand, Mukhopadhyay et al. (2016) used HHP to preserve a
cantaloupe puree. They assessed the effect of applying different pres­
sures (300, 400, and 500 MPa) for 5 min at the initial temperatures of 8
and 15 ◦ C. They observed that at 500 MPa Salmonella was completely
inactivated, independently of the treatment temperature (maximum
process temperature was 35 ◦ C), achieving a reduction higher than 6.7
log CFU/g.
Peanut butter is a widely consumed food product in the United
States, which in recent years has been in the spotlight due to several
salmonellosis outbreaks associated with its consumption. Since 2006, at

34
R. Agregán et al.
least three cases have been reported in this country (Li, Huang, & Chen,
2014). One of them corresponded to S. enterica serovar Tennessee that
does not usually cause outbreaks. In an attempt to reduce the incidence
of Salmonella, D’Souza, Karwe, and Schaffner (2014) reported that HHP
was not a suitable technology to pasteurize peanut butter as it cannot
effectively eliminate Salmonella, even after 18 min of treatment at 600
MPa (initial temperature of 24 ◦ C and maximum temperature of 43 ◦ C)
with the addition of an antimicrobial such as nisin. In this sense,
high-pressure processing is not efficient to ensure microbial safety in
peanut butter.
In the case of refrigerated juices and purees, HHP has an important
impact in the viability of Salmonella spp. and achieve reduction levels
superior to 5 log CFU/mL, alone or in combination with other technol­
ogies using up to 500 MPa for up to 20 min at mild (25–35 ◦ C) or room
temperature. Moreover, the effect of HHP in the inactivation prevents
the further recovery of these bacteria during refrigerated storage of
vegetable products. It is also relevant to mention that HHP induces a
pasteurization effect and an additional hurdle must be used in combi­
nation with HHP processing to prevent microbial spoilage during stor­
age (refrigeration or freezing, for instance).
3.3. High hydrostatic pressure (HHP) effect on reducing Salmonella spp.
in animal products
The gastrointestinal tract of animals is an important reservoir of
Salmonella, with a wide variety of hosts, including birds (e.g., chicken
and turkey) and mammals (e.g., pig and cattle). Foods commercialized
in fresh form these animals may be contaminated with this pathogen
throughout the production chain, as well as in processing, distribution,
and sale operations. The germicidal effect of high pressures depends not
only on the microorganism itself but also on the physicochemical
characteristics of the food matrix. For instance, it is known that high-fat
content and/or low water activity (aw), as well as the presence of pro­
teins and sugars in meat products, protects microorganisms somehow
against high-pressure treatment. Conversely, a low pH has the opposite
effect (Bover-Cid et al., 2017).
The elimination of Salmonella in dry-cured ham by using high pres­
sures has been the subject of different investigations carried out in
recent years (Table 3). For instance, when the dry-cured ham was
manufactured without the addition of NaCl, the presence of viable cells
was detected during the 28 days after treatment with high pressures,
indicating the importance, already known, of common salt for food
safety in this type of meat products. The authors themselves pointed out
Table 3
Treatments with high hydrostatic pressure (HHP) on animal products reported in literature and the corresponding logarithmic reductions found in Salmonella
population.
Salmonella sp. Animal product
Salmonella enterica serovar Enteritidis CECT 4155, Dry-cured ham
CECT 4300, and CECT 4396
Salmonella enterica serovar Typhimurium ATCC Italian salami
14020 and 118,174/1 and serovar Derby 106,463/ - Low fat
1 (enterprise A)
- Milano
(enterprise B)
- Finocchiona
(enterprise B)
- Pepperoni
(enterprise C)
- Strolghino
(enterprise C)
- Napoli (enterprise
H)
- Varzi (enterprise
I)
RVB: Rappaport–Vassiliadis Broth; SSA: Salmonella Shigella Agar; XLD: Xylose Lysine Desoxycholate agar.
(i): initial treatment temperature; (m): maximum treatment temperature.
Trends in Food Science & Technology 107 (2021) 31–37
the antimicrobial power of common salt, highlighting its preservative
effect in food. It is important to mention that a recent study indicated
that HHP treatment induced an excessive proteolysis in dry-cured ham
and led to reduced sensory quality (López-Pedrouso et al., 2019).
As previously mentioned, aw and fat content are key factors that
determine the degree of lethality of high pressures in microorganisms.
Bover-Cid et al. (2017) evaluated the effect of these two variables on a
dry-cured ham subjected to HHP. The product was previously inoculated
with 6–7 log CFU/g of S. enterica serovar London. The results showed
that aw effectively influenced the lethality of high pressures. At low aw
(0.88), a pressure increase had a limited effect on the bacteria: 450 and
750 MPa for 15 at the initial temperature of 15 ◦ C caused a reduction of
2.3 and 3.2 log CFU/g, respectively. In contrast, the different fat content
assayed had no clear protective effect on Salmonella.
According to the results reported in the literature, the bactericidal
effect of high-pressure on Salmonella in a product such as dry-cured ham
supports the use of this technology. These positive results seem to be the
consequence of the combination of factors (such as the treatment time,
operation temperature, and pressure level) that affect the lethality of
this emerging technology. On the other hand, the use of antimicrobials
for food preservation in combination with HHP has been assayed in
different products. These combined treatments tend to produce a syn­
ergistic effect. A relevant example is the study carried out by De Alba,
Bravo, and Medina (2015) who used the bovine lactoperoxidase system
(LPS) (a natural enzyme) and Bovine lactoferrin (LF) (glycoprotein),
both with antimicrobial activity, in combination with high-pressure
treatment to decontaminate a dry-cured ham. They found that both
LPS and LF applied individually had no germicidal effect on S. Enter­
itidis. Conversely, the HHP-LPS and HHP-LF treatments showed a syn­
ergistic effect. A pressure of 450 MPa for 10 min at approximately 12 ◦ C
with LPS caused a reduction of 4.32 log CFU/g on S. Enteritidis counts. In
the case of LF, a reduction of 3.75 log CFU/g was obtained in combi­
nation with high-pressure processing. On the other hand, the application
of pressure without the addition of any of the antimicrobials caused a
reduction of 2.22 log CFU/g. Therefore, the combined treatments pro­
duced additional reductions of 2.1 log CFU/g and 1.53 log CFU/g in the
population of Salmonella for HHP treatment combined with LPS and LF,
respectively. In percentage terms, it meant that the combined treatments
of HHP-LPS and HHP-LF were almost 50% and slightly more than 30%
more lethal against S. Enteritidis, respectively. Montiel, Martín-Cabre­
jas, and Medina (2015) carried out a similar study on cooked ham. The
antimicrobial compounds reuterin, LPS, and FL were used in combina­
tion with HHP for the preservation of this meat product. However,
Pressure Time Temperature Log Culture medium Reference
(MPa) (min) (◦ C) reduction
450 10 12 2.22 log RVB (if necessary) De Alba et al.
cfu/g and SSA (2015)
600 5 14 (i) XLD Bonilauri et al.
4.72 log (2019)
cfu/g
5.84 log
cfu/g
4.73 log
cfu/g
3.03 log
cfu/g
4.33 log
cfu/g
3.16 log
cfu/g
4.32 log
cfu/g
35
R. Agregán et al.
unlike the previous study, the combination of treatments did not have a
synergistic effect in S. Enteritidis inactivation.
Fermented meat products are traditionally considered microbiolog­
ically safe. However, several Salmonella outbreaks associated with the
consumption of these products in the European Union and the United
States have questioned such safety. Salmonella Compliance Guidelines
for small and very small meat and poultry establishments that produce
ready-to-eat (RTE) products (USDA-FSIS, 2017) recommended at least 5
log reductions in the population of Salmonella spp. This reduction is
carried out by processes such as fermentation. However, there is scien­
tific evidence that fermenting a meat product does not ensure 5 log re­
ductions. For this reason, further treatment with HHP can improve food
safety with minimal impact on the product’s characteristics (Bonilauri
et al., 2019). These authors carried out a study to model the reduction of
a combination of three Salmonella spp. (S. Typhimurium ATCC 14020, S.
Typhimurium 118,174/1, and S. Derby strain 106,463/1) during the
elaboration of Italian salami. The effects of time, temperature, pH, aw,
and Salmonella spp. counts were studied in a total of 20 salamis pro­
duced by 10 enterprises. The results showed that none of the proposed
processing conditions achieved 5 log CFU/g reduction at the end of the
ripening period. However, the authors observed that a high-pressure
treatment (600 MPa for 5 min at the initial temperature of 4 ◦ C) once
the product was finished caused a reduction in all samples of between
2.41 and 5.84 log CFU/g. The sum of reductions resulting from the
manufacturing process and high-pressure treatment led to a total
reduction greater than 5 log CFU/g in the salami, thus complying with
the recommendations for this type of product.
The processing of fermented sausages is characterized by a combi­
nation of factors that act as a barrier against the growth of spoilage and
pathogenic microorganisms. Factors, such as pH, aw, and the matrix
characteristics, in addition to the high-pressure treatment parameters,
can affect Salmonella survival. The combination of these hurdles in­
activates or prevents the growth of these bacteria. More specifically, the
acidity, pH, and aw are the most relevant factors that prevent spoilage in
fermented meat products. Other relevant factors are the use of curing
salts, low redox potential, and the competition of microbiota for avail­
able resources. Despite all these barriers, it is not possible to ensure food
safety. According to the results, a non-thermal technology such as HHP
could improve the safety and stability of fermented meat products.
Eggs are the food par excellence that is most frequently related to
Salmonella. In fact, eggs were the cause of 53% of all salmonellosis cases
reported to the Centre for Disease Control and Prevention (CDC) in the
United States between 1985 and 2002 (Whiley & Ross, 2015). Fresh
liquid eggs products are used in the manufacture of many food products,
such as homemade ice cream, mayonnaise, and cold desserts, so that
those that have not undergone a decontamination process may represent
a risk to public health (Keerthirathne, Ross, Fallowfield, & Whiley,
2017). Therefore, in order to produce safe products, the industry sub­
mits fresh egg products (intended for the manufacture of foods) to
pasteurization. However, high temperatures negatively influence the
functional properties of eggs, as well as its nutritional value, taste, and
texture (Souza, de Melo, Santos, Lima, & Vieira, 2019).
The use of HHP in foods of animal origin can increase the safety
against Salmonella spp., especially in combination with other hurdles
(such as activity water, salt, and antimicrobial systems). The intensity of
treatment varies among the products considered in this review: for dry-
cured ham and sausages, pressures above 400 MPa are necessary to
achieve 5 log CFU/g reduction. Conversely in liquid egg products,
pressures in the range between 100 and 300 MPa can be applied to
achieve the same reduction level in Salmonella counts. Similar to dis­
cussed for vegetable foods, it is necessary to combine the HPP with
another hurdle technology (such as refrigeration) to preserve the safety
achieved by this non-thermal technology.
36
Trends in Food Science & Technology 107 (2021) 31–37
4. Conclusion
HHP has shown to inactivate Salmonella in a wide variety of food
products, from both vegetable and animal origin. Recent research pre­
sents encouraging results that place it as an alternative to thermal
treatments to improve the safety against Salmonella spp. growth. In fact,
it has been used for some time in the food industry for the preservation
of products such as juices. Still, there are certain limitations when using
this technology. The food composition and state affect significantly the
efficiency of high pressures. Fat content, aw, and pH limiting factors in
the use of this technology for the elimination of Salmonella spp. in foods.
Moreover, food products in solid state must be treated with more intense
conditions to achieve pasteurization level than liquid ones. Further
research into the use of HHP and/or modifications in the manufacturing
of these products, especially in combinations with other hurdle tech­
nologies are suggested to be carried out to improve the safety against
these bacteria.
Acknowledgements
Thanks to GAIN (Axencia Galega de Innovación) for supporting this
review (grant number IN607A2019/01). Jose M. Lorenzo is member of
the HealthyMeat network, funded by CYTED (ref. 119RT0568). Ac­
knowledgements to INIA for granting Cristina Pérez Santaescolástica
with a predoctoral scholarship (grant number CPD2015-0212). Paulo E.
S. Munekata acknowledges postdoctoral fellowship support from Min­
istry of Economy and Competitiveness (MINECO, Spain) “Juan de la
Cierva” program (FJCI-2016-29486).
References
Abatcha, M. G., Effarizah, M. E., & Rusul, G. (2018). Prevalence, antimicrobial resistance,
resistance genes and class 1 integrons of Salmonella serovars in leafy vegetables,
chicken carcasses and related processing environments in Malaysian fresh food
markets. Food Control, 91, 170–180. https://doi.org/10.1016/j.
foodcont.2018.02.039
Alghoribi, M. F., Doumith, M., Alrodayyan, M., Zayer, M. Al, Köster, W. L., Muhanna, A.,
et al. (2019). S. Enteritidis and S. Typhimurium harboring SPI-1 and SpI-2 are the
predominant serotypes associated with human salmonellosis in Saudi Arabia.
Frontiers in Cellular and Infection Microbiology, 9(MAY), 187. https://doi.org/
10.3389/fcimb.2019.00187
Allende, A., & Monaghan, J. (2015). Irrigation water quality for leafy crops: A
perspective of risks and potential solutions. International Journal of Environmental
Research and Public Health, 12(7), 7457–7477. https://doi.org/10.3390/
ijerph120707457
Allison, A., Daniels, E., Chowdhury, S., & Fouladkhah, A. (2018). Effects of elevated
hydrostatic pressure against mesophilic background microflora and habituated
Salmonella serovars in orange juice. Microorganisms. https://doi.org/10.3390/
microorganisms6010023
Ashton, P. M., Peters, T., Ameh, L., McAleer, R., Petrie, S., Nair, S., et al. (2015). Whole
genome sequencing for the retrospective investigation of an outbreak of Salmonella
Typhimurium DT 8. PLoS Currents, 7. https://doi.org/10.1371/currents.
outbreaks.2c05a47d292f376afc5a6fcdd8a7a3b6. OUTBREAKS.
Balasubramaniam, V. M.(B.), Martínez-Monteagudo, S. I., & Gupta, R. (2015). Principles
and application of high pressure-based technologies in the food industry. Annual
Review of Food Science and Technology, 6(1), 435–462. https://doi.org/10.1146/
annurev-food-022814-015539
Barrere, V., Tompkins, E., Armstrong, M., Bird, P., Bastin, B., & Goodridge, L. (2020).
Optimization of Salmonella detection in garlic, onion, cinnamon, red chili pepper
powders and green tea. International Journal of Food Microbiology, 316, 108440.
https://doi.org/10.1016/j.ijfoodmicro.2019.108440
Bhilwadikar, T., Pounraj, S., Manivannan, S., Rastogi, N. K., & Negi, P. S. (2019).
Decontamination of microorganisms and pesticides from fresh fruits and vegetables:
A comprehensive review from common household processes to modern techniques.
Comprehensive Reviews in Food Science and Food Safety, 18(4), 1003–1038. https://
doi.org/10.1111/1541-4337.12453
Bonilauri, P., Grisenti, M. S., Daminelli, P., Merialdi, G., Ramini, M., Bardasi, L., et al.
(2019). Reduction of Salmonella spp. populations in Italian salami during production
process and high pressure processing treatment: Validation of processes to export to
the. U.S. Meat Science, 157, 107869. https://doi.org/10.1016/j.meatsci.2019.06.005
Bover-Cid, S., Belletti, N., Aymerich, T., & Garriga, M. (2017). Modelling the impact of
water activity and fat content of dry-cured ham on the reduction of Salmonella
enterica by high pressure processing. Meat Science, 123, 120–125. https://doi.org/
10.1016/j.meatsci.2016.09.014
Daryaei, H., Yousef, A. E., & Balasubramaniam, V. M. (2016). Microbiological aspects of
high pressure food processing: Inactivation of vegetative microorganisms and spores.
In V. M. Balasubramaniam, G. V. Barbosa-Cánovas, & H. L. M. Lelieveld (Eds.), High
R. Agregán et al.
pressure processing of food: Principles, technology and applications (pp. 271–294). New
Orleans: Springer. https://doi.org/10.1007/978-1-4939-3234-4.
De Alba, M., Bravo, D., & Medina, M. (2015). Inactivation of Listeria monocytogenes and
Salmonella Enteritidis in dry-cured ham by combined treatments of high pressure and
the lactoperoxidase system or lactoferrin. Innovative Food Science & Emerging
Technologies, 31, 54–59. https://doi.org/10.1016/j.ifset.2015.06.013
D’Souza, T., Karwe, M., & Schaffner, D. W. (2014). Effect of high hydrostatic pressure on
Salmonella inoculated into creamy peanut butter with modified composition. Journal
of Food Protection, 77(10), 1664–1668. https://doi.org/10.4315/0362-028X.JFP-14-
062
EFSA. (2019). Salmonella the most common cause of foodborne outbreaks in the European
Union. Retrieved https://www.efsa.europa.eu/en/news/salmonella-most-common
-cause-foodborne-outbreaks-european-union. (Accessed 25 September 2020).
Gieraltowski, L., Higa, J., Peralta, V., Green, A., Schwensohn, C., Rosen, H., Libby, T.,
et al. (2016). National outbreak of multidrug resistant Salmonella Heidelberg
infections linked to a single poultry company. PLoS ONE, 11(9), 1–13.
Gurtler, J. B., Juneja, V. K., Jones, D. R., & Purohit, A. (2019). Thermal inactivation
kinetics of three heat-resistant Salmonella strains in whole liquid egg. Journal of Food
Protection, 82(9), 1465–1471. https://doi.org/10.4315/0362-028X.JFP-18-438
Hoffmann, M., Luo, Y., Monday, S. R., Gonzalez-Escalona, N., Ottesen, A. R.,
Muruvanda, T., Wang, C., et al. (2016). Tracing origins of the Salmonella Bareilly
strain causing a food-borne outbreak in the United States. J. Infect. Dis., 213(4),
502–508. https://doi.org/10.1093/infdis/jiv297
Hurtado, A., Picouet, P., Jofré, A., Guàrdia, M. D., Ros, J. M., & Bañón, S. (2015).
Application of high pressure processing for obtaining “fresh-like” fruit smoothies.
Food and Bioprocess Technology, 8(12), 2470–2482. https://doi.org/10.1007/s11947-
015-1598-5
Inns, T., Lane, C., Peters, T., Dallman, T., Chatt, C., McFarland, N., et al. (2015). A multi-
country Salmonella enteritidis phage type 14b outbreak associated with eggs from a
German producer: ‘Near real-time’ application of whole genome sequencing and
food chain investigations, United Kingdom, may to september 2014. Euro
Surveillance, 20(16). https://doi.org/10.2807/1560-7917.ES2015.20.16.21098
Jiang, M., Zhu, F., Yang, C., Deng, Y., Kwan, P. S. L., Li, Y., et al. (2020). Whole-genome
analysis of Salmonella enterica serovar Enteritidis isolates in outbreak linked to online
food delivery, Shenzhen, China, 2018. Emerging Infectious Diseases, 26(4), 789–792.
https://doi.org/10.3201/eid2604.191446
Keerthirathne, T. P., Ross, K., Fallowfield, H., & Whiley, H. (2017). Reducing risk of
salmonellosis through egg decontamination processes. International Journal of
Environmental Research and Public Health, 14(3). https://doi.org/10.3390/
ijerph14030335
Li, C., Huang, L., & Chen, J. (2014). Comparative study of thermal inactivation kinetics of
Salmonella spp. in peanut butter and peanut butter spread. Food Control, 45,
143–149. https://doi.org/10.1016/j.foodcont.2014.04.028
López-Pedrouso, M., Pérez-Santaescolástica, C., Franco, D., Carballo, J., Zapata, C., &
Lorenzo, J. M. (2019). Molecular insight into taste and aroma of sliced dry-cured
ham induced by protein degradation undergone high-pressure conditions. Food
Research International, 122, 635–642. https://doi.org/10.1016/j.
foodres.2019.01.037
Malekmohammadi, S., Shah, M. K., Townsend Ramsett, M. K., & Bergholz, T. M. (2020).
Survival and thermal resistance among four Salmonella serovars inoculated onto
flaxseeds. Food Microbiology, 91, 103516. https://doi.org/10.1016/j.
fm.2020.103516
Modzelewska-Kapitula, M., & Maj-Sobotka, K. (2014). Salmonella sp. occurrence in
minced meat, meat preparations and mechanically separated meat in Poland. Journal
of Food Safety, 34(2), 126–131. https://doi.org/10.1111/jfs.12105
37
Trends in Food Science & Technology 107 (2021) 31–37
Moffatt, C. R. M., Musto, J., Pingault, N., Miller, M., Stafford, R., Gregory, J., et al.
(2016). Salmonella Typhimurium and outbreaks of egg-associated disease in
Australia, 2001 to 2011. Foodborne Pathogens and Disease, 13(7), 379–385. https://
doi.org/10.1089/fpd.2015.2110
Montiel, R., Martín-Cabrejas, I., & Medina, M. (2015). Reuterin, lactoperoxidase,
lactoferrin and high hydrostatic pressure on the inactivation of food-borne
pathogens in cooked ham. Food Control, 51, 122–128. https://doi.org/10.1016/j.
foodcont.2014.11.010
Mukhopadhyay, S., Sokorai, K., Ukuku, D., Fan, X., Juneja, V., Sites, J., et al. (2016).
Inactivation of Salmonella enterica and Listeria monocytogenes in cantaloupe puree by
high hydrostatic pressure with/without added ascorbic acid. International Journal of
Food Microbiology, 235, 77–84. https://doi.org/10.1016/j.ijfoodmicro.2016.07.007
Mąka, Ł., & Popowska, M. (2016). Antimicrobial resistance of Salmonella spp. isolated
from food. Roczniki Panstwowego Zakladu Higieny, 67(4), 343–358.
Petrus, R., Churey, J., & Worobo, R. (2020). High-pressure processing of apple juice: The
most effective parameters to inactivate pathogens of reference. British Food Journal.
https://doi.org/10.1108/BFJ-03-2020-0178 (in press).
Priyadarshini, A., Rajauria, G., O’Donnell, C. P., & Tiwari, B. K. (2019). Emerging food
processing technologies and factors impacting their industrial adoption. Critical
Reviews in Food Science and Nutrition, 59(19), 3082–3101. https://doi.org/10.1080/
10408398.2018.1483890
Saleh, S., Van Puyvelde, S., Staes, A., Timmerman, E., Barbé, B., Jacobs, J., et al. (2019).
Salmonella Typhi, Paratyphi A, enteritidis and typhimurium core proteomes reveal
differentially expressed proteins linked to the cell surface and pathogenicity. PLoS
Neglected Tropical Diseases, 13(5), Article e0007416. https://doi.org/10.1371/
journal.pntd.0007416
Shahbaz, H. M., Yoo, S., Seo, B., Ghafoor, K., Kim, J. U., Lee, D. U., et al. (2016).
Combination of TiO2-UV photocatalysis and high hydrostatic pressure to inactivate
bacterial pathogens and yeast in commercial apple juice. Food and Bioprocess
Technology, 9(1), 182–190. https://doi.org/10.1007/s11947-015-1614-9
Souza, P. M. de, de Melo, R., Santos, M. A. de A., Lima, F. R., & Vieira, K. H. (2019). Risk
management of egg and egg products: Advanced methods applied. In T. E. Coldea
(Ed.), Food engineering (pp. 1–23). IntechOpen. https://doi.org/10.5772/
intechopen.82691.
Usda -FSIS. (2017). Salmonella compliance guidelines for small and very small meat and
poultry establishments that produce ready-to-eat (RTE) products and revised Appendix A.
June 2017, 7.
Wei, X., Lau, S. K., Chaves, B. D., Danao, M. G. C., Agarwal, S., & Subbiah, J. (2020).
Effect of water activity on the thermal inactivation kinetics of Salmonella in milk
powders. Journal of Dairy Science, 103(8), 6904–6917. https://doi.org/10.3168/
jds.2020-18298
Wei, Z., Xu, X., Yan, M., Chang, H., Li, Y., Kan, B., et al. (2019). Salmonella Typhimurium
and Salmonella Enteritidis infections in sporadic diarrhea in children: Source tracing
and resistance to third-generation cephalosporins and ciprofloxacin. Foodborne
Pathogens and Disease, 16(4), 244–255. https://doi.org/10.1089/fpd.2018.2557
Whiley, H., & Ross, K. (2015). Salmonella and eggs: From production to plate.
International Journal of Environmental Research and Public Health. https://doi.org/
10.3390/ijerph120302543
Zhang, Z. H., Wang, L. H., Zeng, X. A., Han, Z., & Brennan, C. S. (2019). Non-thermal
technologies and its current and future application in the food industry: A review.
International Journal of Food Science and Technology, 54(1), 1–13. https://doi.org/
10.1111/ijfs.13903