Chapter 12
Microbial Control of Milk and Milk Products
Mustafa Guzel and Yesim Soyer
Abstract Milk has been the one of the main nutrient sources of human diet for
centuries. Microbial studies on milk date back to the seventeenth century, when
Kircher used a microscope, and observed the minute worms in milk. Two centuries
later, in the1850s, Pasteur proved that the spoilage of milk resulting the sour taste
was caused by microorganisms. Pasteur’s discoveries on the effect of heat on undesirable microorganisms in beer and wine opened a new era in food science.
Therefore, the process was named “pasteurization”. In the following years of his
invention, pasteurization was conducted in Germany and the U.S.A. (Jay, Modern
food microbiology. Aspen Publishing, Gaithersburg, MD, 2000). Another breakthrough in milk safety was refrigeration, which became popular after the 1950s.
With the advances in heat treatment and low temperature storage, shelf life of pasteurized milk had been increased significantly. Today, pasteurization, partial sterilization, refrigeration, dehydration, and fermentation are commonly used to increase
the shelf life of milk and dairy products. Besides these traditional methods, there are
also novel methods used to prevent dairy products from spoilage and pathogen contamination such as high pressure processing an UV light.
Keywords Milk preservation • Thermal processes • Novel processes • Non-thermal
processes • Natural antimicrobials
1
Introduction
Milk has been the one of the main nutrient sources of human diet for centuries.
Microbial studies on milk date back to the seventeenth century, when Kircher
used a microscope, and observed the minute worms in milk. Two centuries later,
M. Guzel
Department of Food Engineering, Hitit University, Corum, Turkey
e-mail: mustafaguzel@hitit.edu.tr
Y. Soyer (*)
Department of Food Engineering, Middle East Technical University (ODTU), Ankara, Turkey
e-mail: ysoyer@metu.edu.tr
© Springer Science+Business Media, LLC 2017
V.K. Juneja et al. (eds.), Microbial Control and Food Preservation, Food
Microbiology and Food Safety, https://doi.org/10.1007/978-1-4939-7556-3_12
255
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M. Guzel and Y. Soyer
in the1850s, Pasteur proved that the spoilage of milk resulting the sour taste was
caused by microorganisms. Pasteur’s discoveries on the effect of heat on undesirable microorganisms in beer and wine opened a new era in food science.
Therefore, the process was named “pasteurization”. In the following years of his
invention, pasteurization was conducted in Germany and the U.S.A. (Jay 2000).
Another breakthrough in milk safety was refrigeration, which became popular
after the 1950s. With the advances in heat treatment and low temperature storage, shelf life of pasteurized milk had been increased significantly. Today, pasteurization, partial sterilization, refrigeration, dehydration, and fermentation are
commonly used to increase the shelf life of milk and dairy products. Besides
these traditional methods, there are also novel methods used to prevent dairy
products from spoilage and pathogen contamination such as high pressure processing an UV light.
Shelf-life of dairy products is directly attributed to their microbial quality. Milk
can easily be spoiled by microorganisms developing off-odors, off-colors, and off-­
flavor. Some notable spoilage agents in milk are Pseudomonas, Yersinia (Gram
negatives), Micrococcus, Clostridium, and Bacillus (Gram positives) (Whitfield
et al. 2000). Among these microorganisms, Micrococcus shows thermoresistance,
while Clostridium and Bacillus are sporeformers. Furthermore, microbial quality
is also important for public health as dairy products provide an ideal medium to
pathogens like Listeria monocytogenes, Staphylococcus aureus, and Campylobacter
jejuni (Jayaroa and Henning 2001). Moreover, it has been shown that methicillin
resistant S. aureus (MRSA) can contaminate milk (Normanno et al. 2007). In the
U.S., dairy products are the second most commonly attributed food commodity to
foodborne illnesses after fresh produce, and the most frequent reason of hospitalizations (Painter et al. 2013). Contamination of milk may occur due to inadequate
cleanness of farm environment, cows, and milking equipment, invalid disinfection
before and between milking, and mastitis (Akam et al. 1989; Sanaa et al. 1993;
Chambers 2002). Akam et al. (1989) reported that microorganisms in farm environment might contaminate the animal teats via dirt, and contaminate milk. In
addition, pathogens may transmit to milk via feed. Sanaa et al. (1993) highlighted
that poor quality of silage attributed to Listeria monocytogenes contamination significantly. Similar observations were made for other common foodborne pathogens such as Salmonella and Escherichia coli (Davis et al. 2003; Dargatz et al.
2005). To prevent microbial contamination and growth in milk, good farming
practices, including management of animal health, feed cleanness, farm and facility hygiene, milking, milking and storage equipment are required. (Vissers and
Driehuis 2009).
In this chapter, commonly used traditional methods, as well as promising applications of those methods were evaluated mainly in terms of microbial inactivation
in milk and milk products.
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Microbial Control of Milk and Milk Products
2
Microbial Control Via Thermal Processing Methods
257
Thermal processing of milk includes the processes thermization, pasteurization, and
sterilization. Main goals of thermal treatment are to reduce both pathogen and spoilage microorganisms, inactivate enzymes, and reduce chemical and physical changes
(Lewis and Deeth 2009). The effect of heat on microorganisms has been well studied in terms of reaction kinetics and principles. However, according to Langer et al.
(2012), 48 of 121 outbreaks were associated with pasteurized dairy products, and
resulted in more than 2800 cases between 1996 and 2012. Source of contamination
was able to be determined in 7 of 48 cases, and 4 of those 7 cases were associated
with post pasteurization contamination. The authors suggested that remaining cases
probably linked to temperature abuse in consumer homes. Furthermore, the most
common infectious agent was norovirus in the outbreaks associated with pasteurized dairy products suggesting that poor handling was the reason of the contamination. On the other hand, in non-pasteurized dairy product outbreaks, the causative
agents were bacterial pathogens (Langer et al. 2012). The results of that study
clearly show that although the heat treatment has been applied for a long time, consumption of raw milk and non-pasteurized dairy products still causes foodborne
disease outbreaks.
2.1
asteurization and Ultra High Temperature (UHT)
P
Processing
Heat treatment has been used to process safe milk and milk based products with
extended shelf life for a century. Most common heat treatments include thermization, pasteurization, and UHT processing (Table 12.1). Thermization, also called as
subpasteurization, is a process that applied to milk to extend the shelf life before
further processing. It is carried out to inactivate pyschrotrophs such as Pseudomonas
Table 12.1 Types of heat treatment used in milk preservation (Kelly et al. 2012)
Process type
Thermization
Batch pasteurization
High temperature short time
(HTST)
Higher heat shorter time (HHST)
High temperature pasteurization
(ESL)
Ultra high temperature (UHT)
Process conditions
(temperature, time)
57–68 °C, 15 s
63 °C, 30 min
72–74 °C, 15–30 s
89 °C, 1 s; 94 °C, 0.1 s,
100 °C, 0.01 s
120–130 °C, <1–5 s
135–140 °C, 3–5 s
Targets
Psychrotrophs
Vegetative pathogens
Vegetative pathogens
Vegetative pathogens
Vegetative bacteria and most
spores
All bacteria and spores
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M. Guzel and Y. Soyer
sp. to prevent them to produce spoilage enzymes. After then milk is cold stored until
the manufacture of dairy products such as cheese and milk powder (Senyk et al.
1982; West et al. 1986).
Pasteurization is well defined in terms of target microorganisms and efficacy
indicator. Typically, most heat resistant pathogens, Coxiella burnettii and
Mycobacterium tuberculosis, are targeted, and after the pasteurization the inactivation of alkaline phosphatase enzyme is tested as this enzyme show similar kinetics
with those pathogens. Since pasteurization inactivates all pathogens except
­sporeformers (e.g., Clostridium perfringens, Bacillus cereus), it is assumed that
pasteurization following by cold storage ensures the safety of milk. However, inadequate process conditions, post-process contamination and temperature abuse still
cause foodborne diseases associated with dairy products (Langer et al. 2012).
Furthermore, recent studies show that L. monocytogenes may survive during the
pasteurization (Rebagliati et al. 2009; Wen et al. 2009).
UHT processing is always combined with aseptic packaging to produce commercially sterile milk with a shelf-life between 3 and 12 months at room temperature (Farkas 2007; Lewis and Deeth 2009). Apart from some dormant spores, all
bacteria and spores are inactivated (Kelly et al. 2012). Post process contamination
is not a big concern in UHT processing due to aseptic packaging. Although UHT is
considered as microbiologically safe, nutrient loss and off-flavor development are
big concerns.
Recently, studies on heat treatment are focused on increasing the shelf life while
minimizing effect on nutrient and sensory quality. In this regard, another form of
pasteurization, high temperature pasteurization or extended shelf life (ESL), has
been introduced. ESL is in between HTST and UHT in terms of process conditions.
Unlike UHT, ESL milk should be stored under refrigeration temperatures because
all spores are not inactivated. ESL should be combined with either ultraclean or
aseptic packaging to eliminate/minimize the risk of post process contamination.
While aseptic packaging extends the shelf life of ESL, ultraclean packaging is generally preferred because of the cost (Lewis and Deeth 2009).
Combination of heat with non-thermal treatments (e.g., high pressure, pulsed electric field) or natural antimicrobials (e.g., bacteriocins, essential oils, endolysins) is
aimed to reduce the amount of heat, and thus decrease the effect of heat on organoleptic properties, or increasing the shelf life while using typical pasteurization conditions.
For example, Wirjantoro and Lewis (1996) determined that when pasteurization
(HTST) was combined with nisin, the shelf life of milk increased significantly. Further
studies on the effect of heat combinations on the microorganisms and shelf life of milk
were mentioned in the non-thermal and antimicrobials sections.
2.2
Novel Techniques
Due to quality losses in organoleptic properties of milk as a result of traditional
thermal methods, new thermal processes have been developed to minimize the
losses and saving nutritional qualities of milk while keeping the benefits of
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Table 12.2 The overview of novel thermal processes
Process type
Microwave
Radiofrequency
Ohmic heating
Main process parameters
Frequency, t, T (915–2450 MHz)
Frequency, t, T (13.56–40.68 MHz)
t, T
Reference
Clare et al. (2005)
Tewari and Juneja (2007)
de Alwis and Fryer (1990)
traditional methods (i.e., destruction of most of the spoilage bacteria). In novel processing techniques, radiation is the main mechanism of heat transfer, whereas heat
is transferred via conduction and convection in conventional thermal processes
(Table 12.2). Furthermore, instead of fossil fuels, in novel techniques, heat is generated via electricity, which provides easier manipulation and control, while being
more environmental friendly.
2.2.1
Microwave and Radiofrequency Heating
Microwave is a form of non-ionizing, electromagnetic radiation with wavelengths
between 300 MHz and 300 GHz. In industrial applications, 915 MHz and 2450 MHz
are the most used frequencies. The mechanism of microwave relies on the rotation
of water molecules (electric dipoles), due to the microwave energy. The reorientation of water molecules causes intermolecular frictions, which generate heat.
Microwave heating has some advantages over conventional processing methods.
First, heating process with microwave is faster than traditional methods. Therefore,
it is possible to achieve same microbial reductions as with conventional methods,
while minimizing the negative effects of thermal process on nutrients, flavor, and
sensory characteristics. Furthermore, microwave pasteurization can be applied to
the packaged foods, and thus prevent the post treatment contamination. Some of the
most used packaging materials in dairy industry such as glass, paper and plastic are
suitable for microwave heating.
First published study on the microwave pasteurization of milk was conducted in
1969 (Hamid et al. 1969). Since then, many other researchers have been studied the
effects of microwave on the organoleptic properties of milk. Choi et al. (1993a, b)
studied the effect of microwave heating on Listeria monocytogenes, Yersinia enterocolitica, and Campylobacter jejuni at 71.1 °C. It was reported that complete inactivation occurred at 10, 8, and 3 min for L. monocytogenes, Y. enterocolitica, and C.
jejuni respectively (Choi et al. 1993a, b). Villamiel et al. (1996) compared the shelf
life of cow’s milk pasteurized with a continuous microwave system and conventional plate heat exchanger. The results showed that microwave pasteurization not
only prolonged the shelf life, but also provided higher sensory qualities than plate
heat exchanger. Clare et al. (2005) designed a continuous microwave heating system, and compared that system with indirect UHT. Both systems effectively inactivated microorganisms and provided a long shelf life. Researchers concluded that
microwave might be an alternative processing method of long shelf life milk.
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M. Guzel and Y. Soyer
Since each of come up and come down profile of microwave heating is much
lower than conventional methods, effect of thermal destruction on milk nutrients is
limited. However, non-uniform distribution is a big concern, as it carries the risk of
microbial survival (Ohlsson 1990). As a consequence, continues-flow systems that
designed specifically for milk have been proposed (Lopez-Fandino et al. 1996;
Villamiel et al. 1996; Clare et al. 2005).
Radiofrequency heating is another form of nonionizing radiation that has a
wavelength between 3 kHz and 300 MHz. In food applications, generally three
frequencies (13.56, 27.12, and 40.68 MHz) are used (Tewari 2007). Because of its
lower frequency, radiofrequency heating has more penetrating power than microwave. Awuah et al. (2005) used a 2 kW, 27.12 MHz radiofrequency applicator to
evaluate the inactivation of surrogates Listeria innocua and Escherichia coli K12
under laminar flow. It was concluded that radiofrequency might be an alternative to
conventional heating exchangers. However, in spite of its high antimicrobial effect
and very short processing time, radiofrequency has been failed to draw attention.
Further studies are needed to rationalize the potential application of radiofrequency
heating under different flow conditions (Marra et al. 2009).
2.2.2
Ohmic Heating
Ohmic Heating, also called electroheating or joule heating, is based on heat generation in foods by application of electric resistance (de Alwis and Fryer 1990). In
ohmic heating, electrodes are in contact with food material that provides more uniform heat distribution compared to microwave heating. Although ohmic heating
was popular in early nineteenth century (Getchel 1935; Moses 1938), it was replaced
with heat exchangers, due to high application costs and short supply of inert materials required for electrodes (Mizrahi et al. 1975; de Alwis and Fryer 1990). However,
the interest in this technology has been increased in the last three decades because
it is possible to produce higher quality products because of faster processing times
(Castro et al. 2003). Microbial inactivation with ohmic heating occurs not only
through thermal but also non-thermal destruction, namely electroporation (Vicente
et al. 2005).
One of the applications of ohmic heating is the pasteurization of milk (Fillaudeau
et al. 2006). Sun et al. (2008) compared the microbial inactivation of ohmic heating
and conventional heating in milk under same temperature conditions. Authors
reported that D values and final microbial counts for ohmic heating were significantly lower than those obtained with conventional heating. It is highlighted that the
difference between two methods occurred due to non-thermal effects of ohmic heating (Sun et al. 2008). Pereira et al. (2007) found that with ohmic heating, the death
kinetics of E. coli in goat milk was significantly lower than conventional heating. It
was reported that observed D values for E. coli were 0.86 and 3.2 min for ohmic
heating and conventional heating respectively. Similar to previous studies, authors
reported that non-thermal effect of ohmic heating was the main reason behind the
difference.
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Microbial Control of Milk and Milk Products
3
Microbial Control Via Non-thermal Processing Methods
261
Conventional heating methods have been used for a long time in dairy industry due
to their effectiveness in microbial control. In addition to microorganisms, heat also
deactivates enzymes that attributed to shelf-life. However, it has been shown that
heat cause undesirable changes in physical and chemical properties of milk. These
changes include, but not limited to loss of nutrients, brown color formation and
cooked flavor (Ansari and Datta 2007; Lima 2007; Marra et al. 2009). In addition to
prevent undesirable changes, and the increasing trend of awareness and consumer
demand to fresh products force the food industry to develop alternative methods to
conventional heating techniques. Non-thermal processing methods aim to provide
the same protective effect of thermal pasteurization, without damaging nutrients
and sensory characteristics (Table 12.3). Furthermore, non-thermal methods
endeavor to achieve lower cost, minimal environmental impact, increased shelf-life,
and additive free products.
3.1
Pulsed Electric Fields
Pulsed electric fields (PEF) is the application of high voltage electric fields (20–
80 kV/cm) for short durations. Contrary to ohmic heating and other electric based
thermal treatments, PEF is a non-thermal treatment that relies on the high intensity
pulses. The electric field is generated in foods in an insulated treatment chamber
with two electrodes positioned 0.1–1 cm away from each other. It has been stated
that the best application of PEF is to liquid and semi liquid foods such as milk and
yogurt as ions are needed for electric charge. The main microbial inactivation mechanism of PEF is a phenomenon called as “electroporation”. An external potential
difference is triggered with electric field generation. When this potential difference
is higher than the maximum potential difference that cell membrane can endure,
Table 12.3 The overview of non-thermal processes (Villamiel et al. 2009)
Process Type
Pulsed electric fields
(PEF)
High pressure
processing (HPP)
Ultrasound (US)
Main process parameters
Frequency, number of pulses, field
strength, (20–80 kV/cm)
Pressure, t, T (13.56–40.68 MHz)
Frequency, t, T
Pulsed light
Wavelength, number of pulses
UV radiation
Wavelength
Microfiltration
Membrane type, flow rate, pressure
Targets
Vegetative pathogens/No
effect on spores
Vegetative pathogens/limited
effect on spores
Limited effect on vegetative
pathogens and spores
Vegetative pathogens/limited
effect on spores
Vegetative pathogens/limited
effect on spores
Vegetative pathogens and
spores
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M. Guzel and Y. Soyer
pores are formed due to breakdown of membrane (Zimmermann 1986). At higher
electric field levels (>25 kV/cm), pore formation is irreversible (van Heesch et al.
2000). Pulse length, number of pulses, initial temperature, pulse number, composition and pH of food, type of microorganism, and electric field strength are the most
important parameters of PEF application.
In one of the first studies, Dunn and Pearlman (1987) treated Salmonella Dublin
inoculated milk with PEF, and stored for 8 days. After PEF application (36.7 kV/
cm), no S. Dublin was detected during storage period. Furthermore, while natural
microflora increased to 107 cfu/mL level in untreated control group, only reached to
4 × 102 cfu/mL level in treated samples. Evrendilek and Zhang (2005) applied PEF
(24 kV/cm) to skimmed milk, and 1.88 log reduction was observed in E. coli population. In a similar study, Dutreux et al. (2000) applied PEF (41 kV/cm) to E. coli
and L. innocua inoculated skimmed milk, and achieved 4.5 and 4 log cfu/mL reduction, respectively. In another study, Fernandez-Molina (2001) applied PEF (50 kV/
cm) to skim milk, and observed 2.6 and 2.7 log reductions in L. innocua and P. fluorescens populations respectively.
Combination of PEF with other treatments such as temperature and bacteriocins,
increases the effectiveness of the treatment. For example, Smith et al. (2002b) combined PEF (80 kV/cm at 52 °C) with nisin and lysozyme to inactivate the natural
microflora. Among the combinations, PEF plus lysozyme reduced the microbial
load 3.2 log, while reduction was 5.7 log with PEF plus nisin. When lysozyme and
nisin are used together along with PEF, total reduction was more than 7 log. The
combination of antimicrobials with PEF was tested in different studies, and similar
results were reported (Fernandez-Molina et al. 2005a; Sobrino-López and Martín-­
Belloso 2006; Sobrino-López et al. 2009). Sobrino-López et al. (2009) evaluated
the synergetic effect of PEF, nisin, enterocin AS-48, and lysozyme. It was found that
nisin and enterocin AS-48 increased the effectiveness of PEF treatment. Furthermore,
higher log reduction was achieved when both antimicrobials were added prior to
PEF treatment. It was concluded that antimicrobial addition before PEF treatment
increased the sensitivity of cell membrane for potential difference.
A similar synergetic effect was observed in the combination of PEF and a mild
heat treatment. Fernandez-Molina et al. (2005b) applied PEF (30 kV/cm) following
a heat treatment (80 °C, 6 s) to skim milk and prolonged shelf-life to 30 days. In a
similar study, PEF (35 kV/cm) was applied after heat treatment (72 °C, 15 s), and
more than 60 days of shelf-life was achieved (Sampedro et al. 2007). Yeom et al.
(2004) combined PEF (30 kV/cm) with heat (60 °C, 30 s) in a yogurt based product,
and reported that combined treatment extended the shelf-life for 90 days, which was
three times higher than untreated samples.
3.2
High Pressure Processing
High pressure processing (HPP) also called as high hydrostatic pressure, relies on
an instantaneous and uniform compression from all directions (Neeto and Chen
2014). HPP is one of the most popular non-thermal processing methods since the
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263
early 90’s because of its potential to kill microorganisms without damaging
organoleptic properties (Jung et al. 2011). HPP has some other advantages over
other processing methods like faster process times, and in package processing
(Koutchma 2009). The main mechanism of inactivation is the breakdown of noncovalent bonds (Tewari 2007). It is also believed that HPP affects morphology,
genetic mechanisms and disrupts the cell membrane (Casadei et al. 2002; Patterson
2005). Also, a recent study revealed that inactivation occurs due to cell wall rupture, membrane damage, and DNA degradation (Yang et al. 2012). The application pressure ranges between 100 and 1000 MPa. The efficacy of HPP depends on
pressure level, process temperature, microbial types, water activity, cell growth
phase, and time (Alpas et al. 1999; Manas and Mackey 2004; Tewari 2007). It was
reported that under room temperatures, HPP is capable to inactivate most pathogenic and spoilage bacteria. However, bacterial spores are much more resistant to
pressure (Villamiel et al. 2009).
The first study on the effects of HPP on microorganisms in milk was conducted
more than a century ago by Hite (1899). Since then, many other researchers studied
or reviewed the pasteurization of milk with HPP (Dow and Mathews 1939; Timson
and Short 1965; Rademacher and Kessler 1996; Balci and Wilbey 1999; Datta and
Deeth 1999; Alpas and Bozoglu 2000; Lopez-Fandino 2006). Garcia-Risco et al.
(1998) reported that when milk was pasteurized with HPP at room temperature
(400 MPa for 30 min), no psychrophilic bacteria was detected. However, after
45 days of storage at 7 °C, psychrophilic bacteria count exceeded 7 log cfu/mL
level. It was proposed that microorganisms might be injured sub-lethally after the
treatment, and covered slowly during the storage (Garcia-Risco et al. 1998). In a
study, Patterson et al. (1995) treated UHT milk with HPP at 20 °C to determine the
inactivation of pressure resistant strains of pathogens E. coli O157:H7, S. aureus,
and L. monocytogenes. Only <2 and 2 log cfu/mL reductions were observed in the
population of E. coli O157:H7 and S. aureus subjected to 600 MPa for 15 min,
while <1 log cfu/mL reduction was achieved at 375 MPa for 15 min in the population of L. monocytogenes, which was reportedly the most resistant strain among
those three pathogens. It was proposed that the low reductions in the pathogen populations might be due to breakdown of heat sensitive anti-microbial compounds in
UHT milk, and the results might be different in raw milk (Datta and Deeth 1999).
Gallot-Lavallee (1998) reported that HPP at 450 MPa for 10 min reduced the
L. monocytogenes level by more than 5 log in goat milk cheese.
HHP can be combined with other treatment methods to increase the microbial
reduction and reduce the operational costs. Combined processes also enable milder
treatment parameters, and thus limits the nutrient losses. Also known as the pressure
assisted thermal sterilization, HPP with a mild heat treatment is the most well
known process combination. With this combination, it is possible to inactivate bacterial spores which is a drawback of HPP alone. Alpas et al. (2000) evaluated the
effectiveness of HPP (345 MPa) and temperature (50 °C) combination on several
pathogens in pasteurized milk. Apart from a S. aureus strain, more than 8 log reduction was observed in pathogen (L. monocytogenes, E. coli, O157:H7, and Salmonella
ssp.) populations. After 3 days of incubation period, L. monocytogenes cells were
recovered, while Gram-negative pathogens were not detected. In the same study,
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M. Guzel and Y. Soyer
Alpas et al. (2000) also evaluated the addition of bacteriocin at the same pressure
(345 MPa) and temperature (50 °C) conditions. More than 8 log reductions were
observed in both S. aureus and L. monocytogenes populations. Furthermore, milk
was stored at 25 °C for 30 days, and no cfu was detected. It was concluded that
when combined with other treatments, HPP could effectively destroy the aforementioned pathogens in milk. Combination of HPP and bacteriocin (nisin) was also
extended the shelf-life of cheese (Ray 1992). Similar to bacteriocins, essential oils
like carvacrol (Karatzas et al. 2001), and antimicrobials like lactoperoxidase
(Garcia-Graellis et al. 2003) were combined with HPP successfully to reduce pathogen concentrations in milk.
3.3
UV Radiation
Although UV light has been used for equipment sanitation for a long time, it has
also been used in food industry for microbial inactivation as a non-thermal technique. Main inactivation mechanism of UV lies in nucleic acid level. UV light can
interrupt replication by forming pyrimidine dimers in DNA and RNA (Cutler and
Zimmerman 2011). Based on the wavelength, UV rays are categorized as UV-A,
UV-B, and UV-C. Among them, UV-C (200–280 nm) is used in food safety applications, while others are used for different purposes such as water disinfection. The
effect of UV light on microbial load in milk and dairy products depends on the
product type, soluble solids, type of the microorganism, and UV absorptivity.
Because of high soluble solid content and opaque color, milk is not an ideal medium
for UV treatment. However, UV light has gained interest in dairy industry because
of low initial and operational costs and easy application possibilities at ambient
temperatures.
Microbial inactivation kinetics of UV light treatment has been studied extensively. Matak et al. (2005) found that a 2 s treatment of UV light at 15.8 ± 1.6 mJ/
m2 resulted in more than 5 log reduction in L. monocytogenes, E. coli, and
Cryptosporidium parvuum populations in goat’s milk. Pereira et al. (2014) inoculated whole milk with several pathogens, and treated with UV light under continuous flow process. After the treatment L. monocytogenes, Salmonella spp., E. coli, S.
aureus, and Streptococcus spp., reduced by 3.2, 3.7, 2.8, 3.4, and 3.4 log cfu/mL,
respectively. However, reduction in Mycobacterium smegmatis population was not
found significant. Similar observations were reported by Altic et al. (2007) in a
study, where 1 kJ/L UV light treatment reduced only 0.5 and 1 log Mycobacterium
avium subsp. paratuberculosis population in whole and semi skimmed milk, respectively. It might be concluded that Mycobacterium species were resistant to UV light.
Although it is possible to achieve higher reductions with higher doses of UV light,
application dose should be 1 kJ/L at most for sensory quality (Reinemann et al.
2006). In fact, even at lower doses such as 15.8 ± 1.6 mJ/m2 sensory parameters
such as odor affected negatively (Matak et al. 2005). Oxidation of milk proteins,
formation of volatile compounds, and losses in micro nutrients were also highlighted
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Microbial Control of Milk and Milk Products
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as serious drawbacks of UV light treatment (Scheidegger et al. 2010; Webster et al.
2011; Guneser and Karagul Yuceer 2012).
To overcome these drawbacks, several reactors were designed. For example,
SurePure Turbulator™, a commercially available UV light applicator, aims to
negate the drawbacks associated with UV treatment. Several studies showed that
new designs might be valuable alternatives to conventional processing techniques in
milk and cheese production (Rossitto et al. 2012; Cilliers et al. 2014; Cappozzo
et al. 2015). Kim et al. (2015) developed UVC light emitting diodes (LED) to overcome the technological limitations of common UV lamps. In addition to technical
advantages, newly developed UV LEDs showed significantly different reduction
compared to standard UV lamps. Following the UV LED treatment at 3 mJ/cm2,
L. monocytogenes, E. coli O157:H7, and Salmonella typhimurium counts reduced
by 4–5 log in sliced cheese.
3.4
Pulsed Light
Pulsed light (PL), also called as high intensity pulsed light, is an emerging technology that inactivates microorganisms with intense, very short duration pulses
(flashes) of light from inert gas lamps. The frequency region covers a broad spectrum from UV light (180 nm) to infrared rays (1100 nm). The inactivation mechanism relies on photophysical, photochemical, and photothermal effects (Palmieri
and Cacacea 2005; Krishnamurthy et al. 2010; Miller et al. 2012). These photo
related effects damages cells morphologically at the nucleic acid level (Palmieri and
Cacacea 2005). Although PL may harm nutrients at high doses, occurrence of negative effects can be controlled nature of the process (Demirci and Krishnamurthy
2011).
PL can be modified to use UV as the only source of light which is named as
pulsed UV light (PUVL). PUVL was found to be more than two times effective than
continuous UV light systems (Palgan et al. 2011). One of the most important features of PUVL was reported that microorganisms did not show innate resistance,
means that unlike temperature or pressure, there is no PUVL resistant bacteria
(Dunn et al. 1995). Also, negative effects on product quality is very limited due to
very short treatment times (Demirci and Panico 2008) and limited oxidation reactions (Krishnamurthy et al. 2007).
Smith et al. (2002a) treated milk with PL, and investigated fate of mesophilic
bacteria. After the PL treatment (25 J/m2) mesophilic bacteria was under detection
limits. What is more, there was no sign of recovery after 21 days as no growth was
observed. Krishnamurthy et al. (2007) studied the effect of treatment parameters
(distance from source, number of passes, and flow rate) on the effectiveness of a
continuous PL system. S. aureus inoculated milk was treated with PL at different
exposure rates. It was reported that complete inactivation achieved when the sample passed 8 cm distance from source at 20 mL/min flow rate (Krishnamurthy
et al. 2007).
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3.5
M. Guzel and Y. Soyer
Ultrasound
Ultrasound (US), also referred as sonication and ultrasonication, is the sound waves
with the frequency above 20 kHz. Based on the intensity level, US can be categorized under two groups; high intensity US with low frequency, and low intensity US
with high frequency. Although both categories have different food applications,
high intensity US is found to be more efficient in terms of antimicrobial activity
(Demirdöven and Baysal 2009). High intensity US, also called as power US, covers
the frequency range between 20 and 100 kHz. As ultrasound travels through media,
alternating compression and expansion cycles are created. In the expansion cycles,
microbubbles (cavities) are formed. These bubbles eventually implode and generate
shockwaves, turbulence, local temperature rise and pressure. The antimicrobial
activity of US comes from this phenomenon that is also called as cavitation
(Ashokkumar et al. 2004, 2010; Ashokkumar and Grieser 2007).
It was reported that Gram-positive and cocci shaped bacteria are more resistant to
ultrasound than Gram-negative and rod shaped cells (Hulsen 1999; Feng et al. 2008).
Cameron et al. (2009) demonstrated that 10 min ultrasonication reduced the populations of E. coli by 100% and L. monocytogenes by 99%, whereas Pseudomonas fluorescens population reduced by 100% after 6 min, without damaging total protein and
casein content. However, it was reported that combination of ultrasound with other
treatments such as temperature and pressure generally preferred because of the
increased efficiency and reduced power as well as time consumption (Ordonez et al.
1984). In milk and other dairy products, ultrasound with temperature, called as thermosonication or ultrasound assisted thermal treatment, is a well studied combination
(Earnshaw et al. 1995; Villamiel et al. 1999; Villamiel and de Jong 2000; BermudezAguirre et al. 2009; Riener et al. 2009). Bermudez-Aguirre and Barbosa-­Canovas
(2008) reported that when milk was sonicated (24 kHz) at 63 °C, growth of mesophilic microorganisms was less than 2 log at room temperature for 16 days. In another
study, Bermudez-Aguirre et al. (2009) achieved 5 log reduction in Listeria innocua
and mesophilic bacteria count in raw milk with the same experimental setup (24 kHz
at 63 °C). Zenker et al. (2003) reported that although energy consumption remains the
same with conventional methods, microbial load reduction was achieved in lower
temperatures with thermosonication. Gera and Doores (2011) calculated the D values
for E. coli and L. monocytogenes in whole milk, skim milk and phosphate buffer. Both
E. coli (2.43 min in milk, 2.19 min in buffer) and L. monocytogenes (9.31 min in milk,
7.63 min in buffer) showed higher resistance in milk. It was suggested that milk might
show “sonoprotective effect” (Gera and Doores 2011).
3.6
Other Methods
Apart from the aforementioned applications, there are some important non-thermal
treatments worth mentioning. One of these applications is microfiltration (MF).
Microfiltration process contains a semi permeable membrane with 0.1–1 μm pores.
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267
Besides some technological advantages like defatting, microfiltration can also be
used to reduce microbial load in milk (Maubois 2002). Elwell and Barbano (2006)
treated milk with a MF and heat combination and achieved 5.6 log reduction in
natural microflora. In another study, Walkling-Ribeiro et al. (2011) evaluated the
effectiveness of PEF plus MF combination and compared that combination with
thermal pasteurization treatment. Thermal treatment (75 °C, 24 s) reduced the
microbial count (4.6 log) more than PEF alone (2.5 log) and MF alone (3.7 log)
applications. MF-PEF combination with different process parameters resulted in
4.1, 44, and 4.8 log reductions. However, when combination was reversed, MF was
applied after PEF, the microbial reduction was increase to 4.9, 5.3, 5.7, and 7.1 log.
Another potential application is cold plasma. Cold plasma (CP), also called as
cold atmospheric plasma or non-thermal plasma, is a novel method that causes
structural and metabolical damages on microbial cells. Song et al. (2009) showed a
potential application of cold plasma on sliced cheese. The viable L. monocytogenes
cells were reduced by 5.8 log after 120 s treatment at 125 W.
4
Microbial Control Via Natural Antimicrobials
Natural antimicrobials are the compounds that can be derived from biological
sources without alteration (Li et al. 2011). The biological source can be animal (e.g.,
lysozyme, lactoperoxidase system), plant (e.g., essential oils) or microbiological
(e.g., bacteriocins). Milk has several antimicrobials such as conglitunin, lactoferrin,
lactoferricin, lactoperoxidase system, and lysozyme. Combinations of the treatments may be synergistic, additive, or antagonistic. A synergistic effect occurs
when the effect of the combination was greater than the sum of individual treatments. In antagonistic interactions, combined effect is lower than individual treatments, when in additive interactions the effect is equal to the sum of individual
effects (Branen and Davidson 2004).
4.1
Essential Oils and Other Plant Based Antimicrobials
There has been an increasing interest to plants and their extracts due to their effectiveness against foodborne pathogens, moulds, and mycotoxins. Essential oils (EO)
and plant by products such as tannins and phenolic acids are the main antimicrobial
substances derived from plants. Although the inactivation mechanism of EOs are
not clearly understood, it has been proposed that EOs penetrate through cell membrane due to their lipophilic characteristics, and show inhibitory effect on microorganisms (Li et al. 2011).
Pan et al. (2014) evaluated the effectiveness of free and nanoencapsulated thymol by sodium caseinate. Although minimal inhibitory concentration (MIC) and
minimal bactericidal concentration (MBC) of thymol was higher in skim milk than
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tryptic soy broth, both free and encapsulated thymol showed antilisterial activity.
Cava et al. (2012) tested the antimicrobial activity of vanillin extract and cinnamon—clove combination against L. monocytogenes and E. coli O157:H7 in tripticase soy broth, whole, and semi skim milk. MIC and MBC of the antimicrobials
were lower in broth than milk. Authors suggested that fat molecules in milk might
have showed protective effect against antimicrobials. Also, MIC and MBC values
for L. monocytogenes were higher than E. coli O157:H7 in all mediums. In a similar
study, Cava et al. (2007) reported that cinnamon bark, cinnamon leaf and clove
showed inhibitory effect on L. monocytogenes in milk. The authors suggested that
because these compounds had been used as milk flavor worldwide, the consumer
acceptance would be high for these essential oils as antimicrobial additives. Chen
et al. (2015) co-encapsulated thymol and eugenol and observed inhibitory effect
against the L. monocytogenes and E. coli O157:H7 growth. Abdalla et al. (2007)
evaluated the antimicrobial properties of mango seed kernel extract and oil, and
reported that kernel extract reduced the total bacterial counts and inhibited the
growth of coliforms in pasteurized milk. Shah et al. (2013) reported that although
free eugenol was more effective than nanoencapsulated eugenol in TSB, in milk,
antimicrobial activity of eugenol was higher in nanodispersed form compared to
free eugenol.
Essential oils can also be used as a component in combined treatments. Karatzas
et al. (2001) reported that addition of carcavrol after HP treatment showed a synergistic effect on L. monocytogenes cells in semi skimmed milk, by preventing the
recovery of sub-lethality injured cells. Similarly, Pina-Perez et al. (2012) reported
that combination of cinnamon and PEF showed synergistic effect on S. typhimurium
in skim milk. In another study, Pina-Pérez et al. (2013) combined PEF with
polyphenol-­rich cocoa powder to inactivate the Cronobacter sakazakii in infant
milk formula. It was reported that cocoa powder increased the effectiveness of
PEF. The sequence of combination affected the impact of the treatment significantly, and the maximum inactivation occurred when cocoa powder was added to
formula 4 h after PEF treatment.
4.2
Bacteriophages
Bacteriophages (phages) are considered as natural biocontrol agents due to their
ability to inactivate the target bacteria without disturbing natural microbiota (Bueno
et al. 2012). Phages are bacterial viruses that are ubiquitous in the environment,
highly host specific, and harmless to human cells. In addition, phages can be used
as a food safety tool against antibiotic resistant bacteria. At the end of the lytic
cycle, endolysins, phage encoded enzymes, are released. These enzymes degrade
the peptidoglycan layer of cell wall, and allow newly formed virions out of the cell.
When used externally, endolysins effectively destroys Gram positive bacteria due
the lack of an outer membrane.
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269
García et al. (2007) determined the effectiveness of phages against S. aureus during curd manufacture. A cocktail of phages Φ88 and Φ35 reduced the S. aureus
count by 6 log in UHT milk. Also complete inactivation occurred in 1 h at 30 °C in
renneted curd, and in 4 h at 25 °C in acid curd. In another study, Bueno et al. 2012
used a bacteriophage cocktail to inactivate S. aureus in fresh and hard-type cheese.
In fresh cheese S. aureus counts were below detection limits. In the hard-type cheese
however, 1.24 log cfu/g S. aureus was found after ripening, compared to 6. 73 log
cfu/g in control samples. Similar results were reported by Jeddi et al. (2014), where
bacteriophages effectively reduced the E. coli count below detection limits in milk.
In one of the first endolysin studies in milk, Obeso et al. (2008) evaluated the
effectiveness of ΦH5, a S. aureus bacteriophage, endolysin against S. aureus. In that
study, endolysin coding gene cloned in E. coli, and after characterization, the purified protein showed significant resemblance with other hydrolyses. The purified
protein then tested in milk as an antimicrobial, and rapidly inactivated S. aureus.
The pathogen could not be detected after 4 h of incubation.
Phages and endolysins can also be used in combination with other treatments.
For instance, Tabla et al. (2012) combined HPP and phages to inactivate S. aureus
in milk. The authors determined that 400 MPa pressure combined with a phage
cocktail reduced the S. aureus count in milk below detection limits (<10 cfu/mL).
Garcia et al. (2010) combined LysH5 endolysin with nisin to inactivate S. aureus in
milk. The antimicrobials showed strong synergistic effect, MIC of LysH5 and nisin
reduced by 16- and 64-fold, respectively. On the other hand, Martínez et al. (2008)
showed that although bacteriophages and nisin showed synergistic effect in short
term, nisin adapted cells reduced the bacteriophage activity in milk. When the nisin
adapted cells were taken from the environment, phage susceptibility was restored.
The authors highlighted that the combination should be applied with care to effectively reduce S. aureus in milk.
4.3
Bacteriocins
Bacteriocins are antimicrobial peptides or proteins produced by various groups of
bacteria (Jack et al. 1995). The lactic acid bacteria (LAB) produces a number of
bacteriocins that has been studied or reviewed extensively (Table 12.4). Since LAB
are naturally present in many foods, their bacteriocins are generally regarded as safe
(GRAS) by FDA. LAB bacteriocins are also pH and heat tolerant, non-toxic to
eukaryotic cells, and have a positive effect on gut microbiota (Gálvez et al. 2007).
Bacteriocins can be applied either by adding LAB as the starter culture or in isolated
purified-concentrated form. Although inactivation mechanism may differ for various bacteriocins, dissipation of membrane chemicals is suggested as the common
mechanism (Kaur et al. 2013). For instance, the main antimicrobial mechanism of
nisin comes from the hydrophobic and electrostatic interactions between the nisin
and membrane phospholipids (Bauer and Dicks 2005).
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Table 12.4 Overview of bacteriocins produced by LAB (O’Bryan et al. 2015)
Bacteriocin
Nisin
Pediocin AcH
Enterocin A & B
Lacticin 3147
Lacticin 481
Lactocin 705
Lactacin B
Sakacin
Source
L. lactis subsp. lactis
P. acidilactici
E. faecium
L. lactis subsp. lactis
L. lactis subsp. lactis
L. casei
L. acidophilus
L. sakei
Targets
Gram-positive
Gram-positive, Listeria, LAB
Gram-positive
Gram-positive
Gram-positive
Listeria, LAB, streptococci
Lactobacilli, L. lactis
Lactobacilli, Listeria
Fat globules in milk decrease the antibacterial effect of bacteriocins. Jung et al.
(1992) demonstrated that antilisterial effect of nisin decreased by 33% in skim milk,
and 50% in milk with 1.29% fat. Similarly, Bhatti et al. (2004) reported that nisin
was able to reduce the L. monocytogenes numbers in skim milk to <10 cfu/
mL. However, L. monocytogenes was able to regrowth in whole milk after a decline.
Authors confirmed that either raw or pasteurized milk, nisin lost the antilisterial
effect in homogenized whole milk.
Samelis et al. (2003) reported that addition of nisin to anthotyros (a traditional
Greek cheese) prevented post process contamination with L. monocytogenes, and
changed the natural microflora Gram positive to Gram negative. Ananou et al.
(2010) evaluated the effectiveness of spray dried enterocin AS-48 on L. monocytogenes and S. aureus in skim milk, and found that L. monocytogenes cells completely
inactivated early, while S. aureus population inhibited partially. Martinez et al.
(2016) determined the effect of free and encapsulated commercial nisin and their
combinations on L. monocytogenes and B. cereus in whole and skim milk under
refrigeration. It was reported that combination of free and encapsulated nisin
showed the greatest inhibitory effect on L. monocytogenes, while both bacteriocin
forms were effectively controlled the germination and growth of B. cereus. It was
also reported that encapsulated form protected the antimicrobial effect for 90 days.
Farías et al. (1999) highlighted that enterocin CRL35 (10,400 AU/mL) reduced the
L. monocytogenes population by 9 log in goat cheese without affecting the quality.
In another study, Lauková et al. (2001) achieved around 5 log reduction in L. monocytogenes population in Saint-Paulin cheese with enterocin CCM 4231 addition.
Bacteriocins show synergetic effect with other treatment methods such as HPP
and PEF. The combination of HP (250 MPa) and lacticin 3147 reduced the L. monocytogenes and S. aureus populations more than 6 log, while the log reductions were
only 2.2 log and 1 log for HP and lacticin 3147 when they used alone (Morgan et al.
2000). Black et al. (2005) combined nisin and HPP to inactivate L. innocua, E. coli,
P. fluorescens, and Lactobacillus viridescens. It was reported that 500 MPa for
5 min HP and 500 IU/mL nisin was sufficient to reduce tested strains by 8 log.
Muñoz et al. (2007) showed that the combination of enterocin CCM 4231 with a
mild heat treatment (65 °C, 5 min) reduced the Staphlyococci population below
detection limits for the first 8 h, and prevent the overgrowth in 24 h. Gallo et al. (2007)
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observed a synergistic effect against L. innocua when nisin was added to whey
before PEF. However, nisin addition after PEF treatment did not show same effect.
Authors suggested that alterations in cell envelope and medium might have reduced
the nisin activity. Combination of nisin with other antimicrobial substances increases
the antibacterial activity. Boussouel et al. (2000) added nisin, lactoperoxidase
system, and their combinations to skim milk to inactivate L. monocytogenes. When
used alone, although both substances provided bacteriostatic phase for limited times,
L. monocytogenes was able to grow. However, when lactoperoxidase system was
added 4 h later than nisin, maximum inhibitory effect was reached, and L. monocytogenes was below detection limits in skim milk for 15 days.
Bacteriocin like substances (BLS) are produced by bacteria and show similar
antibacterial effect with bacteriocins. Malheiros et al. (2012a) evaluated the effectiveness of nanovesicle encapsulated BLS P34, an antimicrobial peptide produced
by Bacillus sp. P34, against L. monocytogenes in milk, and found that both free and
encapsulated BLS P34 showed inhibitory effect at 1600 IU/mL level. In another
study, Malheiros et al. (2012b) encapsulated nisin and BLS P34 in PC-1 liposomes
to inhibit the L. monocytogenes growth in Minas frescal cheese. Authors reported
that both substances showed increased inhibitory effect against L. monocytogenes
compared the control group.
4.4
Antimicrobials from Other Sources
Apart from the antimicrobials mentioned above, effect of some enzymes (e.g.,
lysozyme) and antimicrobials from animal origin (e.g., lactoferrin), and organic
acids have also been tested in milk.
Murdock and Matthews (2002) used lactoferrin hydrolysate with pepsin in UHT
milk to inactivate L. monocytogenes and E. coli O157:H7. Result of that study
showed that at pH 4 lactoferrin hydrolysate reduced the populations of both pathogens approximately by 2 log. On the other hand, at pH 7, inhibitory effect was
shown only in E. coli O157:H7 cells. It was also reported that addition of EDTA did
not increase the effectiveness of lactoferrin hydrolysate. McLay et al. (2002) combined lactoperoxidase system with various lipids to inhibit the growth of E. coli
O157:H7 and S. aureus in milk. The highest inhibitory effect achieved when lactoperoxidase (5–200 mg/kg) combined with monolaurin (50–1000 ppm). Researchers
concluded that lactoperoxidase monolaurin combination showed synergistic effect
on the pathogens and inhibited the growth significantly (McLay et al. 2002).
Arqués et al. (2008) evaluated the antibacterial effect of combinations of reuterin
with nisin and lactoperoxidase against Gram-negative bacteria in milk. Reuterin is an
antimicrobial compound produced by Lactobacillus reuteri. While nisin did not
increase the bactericidal activity of reuterin, the combination of lactoperoxidase
system and reuterin showed synergistic effect against E. coli O157:H7, Yersinia
enterocolitica, Aeromonas hydrophila, Campylobacter jejuni, and Salmonella
enterica. In another study, Arqués et al. (2011) combined reuterin and LAB bacteriocins
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nisin, lacticin 481, and enterocin AS-48 to inactivate C. jejuni, Y. enterocolitica,
A. hydrophila, E. coli, S. enterica, L. monocytogenes and S. aureus in milk. Among the
bacteriocins, only nisin showed synergistic effect with reuterin against L. monocytogenes and S. aureus, and prevented the growth of the pathogens after 12 days.
Similarly, Stevens et al. (2011) reported that reuterin showed inhibitory effect
against Gram positive and Gram negative pathogens. Tsai et al. (2000) evaluated the
effectiveness of a chitosan mixture against several pathogenic and spoilage bacteria.
The mixture reduced the mesophilic and psychotropic counts by more than 3 logs
without affecting pH significantly. Moreover, the mixture inhibited the Salmonella
growth and reduced the Staphylococcus spp. counts.
Organic acids (OA), mainly lactic acid, provide antimicrobial effect in some of the
dairy products including yogurt and kefir by reducing pH. OA may also be used in combinations with other antimicrobials and non-thermal treatment methods. For example,
whey protein-based film containing nisin and various organic acids was tested
against L. monocytogenes in cheese. Although all of the organic acids (lactic, malic, and
citric) increased the inhibitory effect of nisin, malic acid plus nisin incorporated film
provided the best antimicrobial results against L. monocytogenes (Pintado et al. 2009).
5
Conclusion
Milk is one of the most favorable food commodity to pathogenic and spoilage bacteria. As a result, safety of milk and other dairy products, while keeping nutrients
and sensory quality is still a big concern. In the near future, the authors expect the
application of more than one treatment in combination will draw more attention.
The combination of applications, as called hurdle technology, was discussed in each
treatment sections.
Hurdle technology is the intentional combination of hurdles (e.g., acidity, water
activity, preservatives) to improve the microbial, sensory, and nutritional quality of
foods (Leistner 2000). Multitarget preservation is the employment of more than one
hurdles at the same time with different inactivation mechanisms or targets (e.g., cell
membrane, DNA, enzymes) (Leistner 1995). With the synergistic effect, it is possible
to use gentler version of current applications in milk and dairy products. In other
words, it is possible to reach higher microbial quality by employing more than one
application with small intensity compared to one application with high intensity.
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