High Hydrostatic Pressure Processing of Cheese: Abstract

High Hydrostatic Pressure Processing of Cheese
Yamile Martnez-Rodrguez, Carlos Acosta-Muniz, Guadalupe I. Olivas, Jose Guerrero-Beltran, Dolores Rodrigo-Aliaga, and
David R. Sepulveda
Abstract: High hydrostatic pressure (HHP) is a cutting-edge processing technology attracting research and industrial
interest in the food sector due to its potential to produce microbiologically safe products, modify the functional properties
of proteins and polysaccharides, and alter biochemical reactions without significantly affecting the nutritional and sensory
properties of food. Currently, there are only a limited number of pressure-treated cheese products available in the market.
Nevertheless, results from numerous research studies on various cheese varieties seem promising, especially since HHP
technology is today more cost-effective than in the past. Considering the progress made in the application of HHP on
cheese during the past 15 years, this paper reviews the direct application of HHP treatments to cheese and the effects it
has on its microbiology and ripening process, as well as on quality parameters such as physicochemical, rheological, and
sensory properties. Detailed information of published studies is presented with the aim of providing a clear picture of the
use of this technology on cheese processing. Areas of research in need of more attention are also identified.
Introduction ufacturing, the application of HHP initially focused on pressure-

Consumer demand for more natural, preservative-free, tastier, treating milk and making cheese therefrom, resulting in microor-
and more wholesome foods has led to the search of improved food ganism inactivation, reduced rennet coagulation time, and in-
processing technologies. Many research studies over the years have creased cheese yield, which many research groups have reviewed
shown that high hydrostatic pressure (HHP) technology is capa- (Trujillo and others 2000a, 2002; OReilly and others 2001;
ble of producing microbiologically safe products, with additional Huppertz and others 2002; Lopez-Fandino 2006; San Martn-
advantages for consumers and food processors over thermal pro- Gonzalez and others 2006). However, more recently, researchers
cessing. Unlike thermal pasteurization, HHP can maintain key have applied HHP directly to the pressed curd and/or ripened
quality attributes such as food freshness, nutritional value, and cheese, and studies have centered on 2 main areas: cheese preser-
sensory properties because it only affects noncovalent bonds, thus vation and modification of the ripening process. Pressures applied
amino acids, vitamins, flavor molecules, and other low-molecular- from 200 to 800 MPa have shown the ability to inactivate lactic
weight compounds remain unaffected. Furthermore, HHP can acid bacteria (LAB) and pathogenic and spoilage microorganisms
lower production costs due to energy savings (Toepfl and others present in cheese, whereas a combination of low-pressure treat-
2006; Pereira and Vicente 2010), reduced processing times (Ser- ments followed by high pressure treatments has been employed
rano and others 2004), and fewer handling steps (Serrano and with some degree of success for the inactivation of bacterial spores
others 2005), and modify the functional properties of proteins and in cheese. The effect of HHP on the ripening process has pro-
polysaccharides, which could lead to the development of novel duced varied results in different cheese varieties studied and in their
or improved products. The industrial use of HHP in different physicochemical and sensory characteristics, resulting sometimes
food sectors around the world has risen from 1 in 1990 to 130 in in ripening acceleration and with some others in deceleration.
2009, making acquisition costs more accessible as demand increases This review takes into account all the studies that have been con-
(Purroy 2009). ducted in the past decade dealing with HHP processing of pressed
Based on the isostatic principle, pressure applied in HHP treat- curds and/or cheese, as well as pertinent results and integrates and
ments is instantaneously and uniformly transmitted throughout the critically discusses the most relevant aspects regarding this topic.
food, regardless of size, shape, and composition. In cheese man-
High Hydrostatic Pressure Inactivation of
MS 20120087 Submitted 1/16/2012, Accepted 3/18/2012. Authors Martnez-
Microorganisms in Cheese
Rodrguez, Acosta-Muniz, Olivas, and Sepulveda are with Centro de Investigacion Food scientists have employed HHP technology in cheese pro-
en Alimentacion y Desarrollo A.C., Unidad Cuauhtemoc, Av. Rio Conchos S/N, cessing to inactivate toxigenic and infectious pathogens such as Es-
Parque Industrial. C. P. 31570, Apartado Postal 781, Cd. Cuauhtemoc, Chihuahua, cherichia coli, Staphylococcus aureus, Listeria monocytogenes, Aeromonas
Mexico. Author Guerrero-Beltran is with Univ. de las Americas Puebla, Sta. Cata- hydrophila, Salmonella enterica, and Yersinia enterocolitica, as well
rina Martir, Cholula, Puebla, C.P. 72810, Mexico. Author Rodrigo-Aliaga is with
Instituto de Agroqumica y Tecnologa de Alimentos, CSIC, Apartado Postal 73, as spoilage microorganisms such as Staphylococcus carnosus, En-
46100 Burjassot, Valencia, Espana. Direct inquiries to author Sepulveda (E-mail: terococcus spp., coliforms, yeasts, and molds, and also microbial
[email protected]). spores from Bacillus subtilis, Bacillus cereus, and Penicillium roqueforti
(Table 1). Results have revealed that HHP treatments cause

c 2012 Institute of Food Technologists
doi: 10.1111/j.1541-4337.2012.00192.x Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 399
Table 1Effect of HHP treatments on vegetative forms and microbial spores in cheese.
Microorganism Cheese Moment of application Treatment conditions Initial counts Inactivation

evaluated variety (days of ripening) P (MPa)/ t (min)/T ( C) (log10 cfu/g) (log10 cfu/g) Reference
E. coli CECT 405 Mato 1 400500/515/2, 10 and 25 8 CIa Capellas and others 1996
E. coli K-12 Cheddar cheese slurry 1 400/20/30 7 CI OReilly and others 2000a
E. coli K-12 Cheddar (raw milk cheese) 1 350/5/50 6.5 CI Shao and others 2007
E. coli O157:H7 Raw milk cheese 2 or 50 500/5/10 c
5.11 (control d 60) CI (d 60) Rodrguez and others 2005
E. coli O59:H21 and O157:H7 Washed-curd 1 500/10/20 About 7 CI De Lamo-Castellv and others 2006
S. aureus ATCC 6538 Cheddar cheese slurry 1 600/20/20 7 CI OReilly and others 2000a
S. aureus CECT 976 Raw milk cheese 50 500/5/10 5.30 (control d 60) CI (d 60) Arques and others 2005a
S. aureus CECT 4013 and ATCC 13565 Washed-curd 1 500/10/5 7.5 6 and 4.7 (d 30) Lopez-Pedemonte and others 2007b
High hydrostatic pressure processing of cheese . . .
S. carnosus CECT 4491 Mato 1 500/5/50 8 7 Capellas and others 2000

Coagulase-positive staphylococci Swiss cheese slurry 1 345 or 550/10, or 30/25 3.3 CI Ding and others 2001
Coagulase-positive staphylococci La Serena (raw milk cheese) 2 300400/10/10 3.07 (control d 30) CI (d 30) Arques and others 2006
L. monocytogenes F13 Sainte-Maure de Touraine 14 500/5/11 About 7 5.6 Gallot-Lavallee 1998
L. monocytogenes (serotype 1/2a) Gorgonzola cheese rind 1 700/15/30 7 5 Carminiati and others 2004
L. monocytogenes Scott A Raw milk cheese 50 300/10/10 5.66 (control d 60) CI (d 60) Arques and others 2005b
L. monocytogenes ATCC 19115 and Washed-curd 1 500/10/5, or 20 7.5 about 5 (both strains d 30) Lopez-Pedemonte and others 2007a
Scott A
400 Comprehensive Reviews in Food Science and Food Safety r Vol. 11, 2012
L. monocytogenes ATCC 19115 Turkish white-brined 1 600/10/25 7.5 4.9 Evrendilek and others 2008
Y. enterocolitica O:1, O:3 and O:8 Washed-curd 1 400500/10/20 4.36, 6.03, and 5.28 CI De Lamo-Castellv and others 2005
S. Enteritidis CECT 4300 and Washed-curd 1 400/10/25 6.45 and 6.03 CI De Lamo-Castellv and others 2007
S. Typhimurium CECT 443
Mesophilic and thermophilic LAB Hispanico (raw milk cheese) 1 500/10/8 8.38 and 6.45 2.1 and 1.9 Alonso and others 2011
Lactic fermentation streptococci Edam 8 wkb 400/120/25 9.41 5.06 Reps and others 2009
Total aerobic mesophilic bacteria
Lactococcus spp. Turkish white-brined 1 1600/10/25 7.9, 8.3, and 7.6 5.2, 5.5, and 4.7 Evrendilek and others 2008
Lactobacillus spp.
Lactococcus lactis (227 and 303) Cheddar 1 400/20/25 6.24 and 9.75 2.8 and 3.1 OReilly and others 2002a
Starter and nonstarter LAB Swiss cheese slurry 1 500/30/25 7.7 and 4 1.7 and CI Ding and others 2001
P. roqueforti IMI 297987 spores Cheddar cheese slurry 1 500/20/20 6 CI OReilly and others 2000a

B. subtilis CECT 4491 spores Mato 1 60/210/40500/15/40 About 5 (in milk) 4.9 Capellas and others 2000
B. cereus ATCC 9139 spores Washed-curd (raw milk cheese) 1 60/210/30400/15/30 6 2 Lopez-Pedemonte and others 2003
a CI = complete inactivation; b wk = weeks; c d=day.

structural and functional alterations in vegetative cells and spores Previous research had associated this behavior to the synthesis of
leading to cell injury or death. These include cell membrane dis- new proteins when bacteria enter the stationary phase, protecting
ruption or increased permeability, ribosomal destruction, collapse cells against adverse conditions (Patterson and others 2006).
of intracellular vacuoles, denaturation of membrane-bound pro-
teins, damage to the proton efflux system, inactivation of key Process conditions
enzymes, including those involved in DNA replication and tran- Like any other food preservation technology, in HHP process-
scription, release of dipicolinic acid and small acid-soluble spore ing, increasing the intensity of treatments or extending their length
proteins, and hydrolysis of spore core and cortex (Black and others of exposure will lead to an increased microbial inactivation rate.
2011). The factors that influence microbial inactivation by HHP Nevertheless, there is a minimum critical pressure below which
treatments can be classified into 3 groups: microbial characteris- microbial inactivation by pressure will not occur irrespective of
tics, process conditions, and product parameters (Manas and Pagan process time.
2005). Several authors have used a combination of HHP treatments Ding and others (2001) observed that higher pressure condi-
with other preservation technologies such as antimicrobial agents tions (345 and 550 MPa) and longer exposure times (10 and 30
to enhance the inactivation rate. min) achieved a greater reduction in numbers of undesirable bac-
teria in the natural microflora of Swiss cheese slurries (coliforms,
Effect of High Hydrostatic Pressure on Vegetative presumptive coagulase-positive Staphylococcus, yeasts, and molds)
Forms of Microorganisms in Cheese and in starter LAB added to milk for acid production and fla-
Microbial characteristics vor development. Fonberg-Broczek and others (2005) found that
Yeasts and molds are the microorganisms most sensitive to HHP A. hydrophila strains (Panstwowy Instytut Weterynaryjny N.98,
treatments. Yeasts are not commonly associated with food-borne Panstwowy Inspekcja Sanitarna N. 98, Inspekcja Sanitarna N. 95)
disease but are important in spoilage (Patterson 2005). Daryaei and in samples of Gouda cheese treated at 100 MPa and 50 C had a
others (2008) reported that pressure treatments 300 MPa applied D-value of 32.05 min, while at 200 MPa the D-value fell to 12.97
for 5 min to fresh lactic curd cheese were capable of effectively min, and to 2.43 min when subjected to 300 MPa. More recently,
controlling the outgrowth of yeasts, therefore, extending product in raw milk Cheddar cheese, an increase in pressure intensity from
shelf-life from 3 to 68 wk. Generally, Gram-positive bacteria are 250 to 350 MPa applied at 25 C resulted in a decrease of D-values
more pressure-resistant than Gram-negative bacteria. However, from 23.5 to 1.4 min for L. monocytogenes Scott A (Shao and others
there are notable exceptions to the previous statement. For exam- 2007).
ple, Shao and others (2007) inoculated raw milk Cheddar cheese Lopez-Pedemonte and others (2007b) studied the efficacy of
with E. coli O157:H7 and L. monocytogenes Scott A and found HHP treatments on the inactivation of S. aureus CECT4013 and
E. coli to be more baroresistant, with decimal reduction values ATCC13565 in washed-curd cheese and the presence of staphylo-
(D-values) at 300 MPa and 25 C of 14.5 and 3.6 min, respec- coccus enterotoxin (SE) A (artificially inoculated) only in cheese
tively. It has been suggested that the lack of teichoic acid in the containing ATCC13565. Inactivation of S. aureus increased as pres-
cell wall of Gram-negative bacteria makes them more susceptible sure increased from 300 to 500 MPa. However, all cheese samples
to HHP treatments than Gram-positive bacteria (Datta and Deeth still contained SE, but it was not clear if it retained its toxic activity
2002). or not. No other research group has addressed the impact of HHP
Several research studies have indicated variations in resistance to on bacterial toxins in cheese. SEs are relatively heat-resistant, with
HHP among bacterial strains. Strains isolated from foods are gen- D-values at 121 C for SE A, B, and C ranging from 8.3 to 34 min
erally more pressure-resistant than strains from culture collections (Tibana and others 1987). Margosch and others (2005) studied the
(Cheftel 1995). De Lamo-Castellv and others (2005) observed effect of HHP and heat on several bacterial toxins in buffer and
that Y. enterocolitica CECT 4055 (setotype O:3) was more baro- reported that pressurization (0.1 to 800 MPa for 30 to 120 min) of
tolerant than 2 other human pathogenic strains (CECT 559 and SE A-E at 5 and 20 C caused no observable effect. A combined
CECT 4054) of Y. enterocolitica in washed-curd cheese treated at heat (80 C) and pressure (0.1 to 800 MPa) treatment led to a
300 MPa. OReilly and others (2000a) showed that food isolates decrease in the immunoreactivity to 20% of its maximum. The
of S. aureus were more pressure-resistant than S. aureus ATCC high barotolerance of SEs is clear from the information provided
6538, but E. coli K-12 was more pressure-resistant than food iso- by this study.
lates, with values varying by approximately 2 log cfu/g for both Temperature including adiabatic heating in HHP processing can
bacterial species in Cheddar cheese slurry pressure-treated at 400 have a significant effect on microbial survival. Adiabatic heating is
MPa for 20 min. Lopez-Pedemonte and others (2007a) assessed approximately 3 C for every 100 MPa, depending on the food
the inactivation of L. monocytogenes NCTC 11994 and Scott A composition (Farkas and Hoover 2000). A greater antimicrobial
in washed-curd cheese at 400 and 500 MPa for 10 min, and re- impact can be achieved with moderate pressure treatments and
ported strain NCTC 11994 to be more sensitive to HHP. OReilly shorter pressure holding times when combining high tempera-
and others (2002a) added 4 Lactococcus lactis strains (303, 223, 227, tures with HHP treatments. However, the use of high temperatures
AM2) in pasteurized milk to make miniature cheese and found could lead to undesirable effects in certain cheese quality param-
that at 400 MPa for 20 min, L. lactis 227 was the most pressure- eters. Capellas and others (2000) noticed that S. carnosus 4491
tolerant with a 2.8 log cycle reduction, while L. lactis AM2 was CECT counts in Mato cheese could not be greatly decreased with
the most pressure-sensitive with a 5.2 log cycle reduction. pressure treatments at 500 MPa for 30 min at 10 or 25 C, whereas
Microbial resistance to HHP depends not only on the intrinsic treatments at 50 C for 5 min achieved a 7 log cycle reduction.
resistance of the microorganisms but also on their physiological However, treatments at 50 C caused high whey losses and unac-
state (Manas and Pagan 2005). OReilly and others (2000a) ob- ceptable textural characteristics. Shao and others (2007) evaluated
served that cells of S. aureus ATCC 6538 and E. coli K-12 in the the effect of HHP treatments at 350 MPa for 5 min at 10 to
exponential phase of growth were more sensitive to HHP treat- 50 C on E. coli K-12 inactivation in raw milk Cheddar cheese.
ments in Cheddar cheese slurry than cells in the stationary phase. They also determined pressure destruction kinetics at 200 to

c 2012 Institute of Food Technologists Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 401
300 MPa at 25 C. The authors reported that inactivation of E. Carminati and others (2004) determined the inactivation ef-
coli became more significant as the temperature applied in HHP fectiveness of HHP treatments applied for 1 to 15 min at 30 C
treatments increased above 40 C. The D-value at 300 MPa was of and 400 to 700 MPa on the inactivation of 7 hemolytic strains
4.4 min. OReilly and others (2000a) also observed that reduction (isolated from the surface of Gorgonzola cheese) belonging to
in total viable numbers of E. coli K-12 in Cheddar cheese slurry serotype 1/2a of L. monocytogenes in Gorgonzola cheese rind. The
increased in parallel with the increase of temperature in pressure authors reported a strong resistance of the microorganism to pres-
treatments above 300 MPa. However, the D-value at 300 MPa sures up to 500 MPa, requiring treatments of 700 MPa for 15
evaluated at 20 C widely differed from that indicated by Shao min to reduce L. monocytogenes at least 5 log cycles. In contrast,
and others, being 22 min. Differences between studies could be Gallot-Lavallee (1998) registered 5.6 log cycle reductions of L.
related to the temperatures used in the experiments, which were monocytogenes F13 in 14-d-old Sainte Maure de Touraine cheese
5 C higher in Cheddar cheese than in slurry. Another plausible applying HHP treatments of 450 MPa for 10 min or 500 MPa
explanation may lie in the cheese matrix, with E. coli more sensi- for 5 min at 11 C. Differences in pH, aw , and the strains studied
tive to pressure in cheese than in slurry as a result of acid injury to could account for the discrepancies encountered in the sensitivity
the bacteria during fermentation (OReilly and others 2000a). to HHP treatments of the microorganism in both studies. The
lower pH of Sainte Maure de Touraine cheese (4.7), compared to
Product parameters the Gorgonzola cheese rind (7.0), and its higher aw may favor a
Cheese is a food consisting of proteins, fats, carbohydrates, salts, greater bacterial inactivation rate.
and minerals. Research studies have indicated that such compo-
nents can influence microbial susceptibility to HHP inactivation, HHP in combination with other preservation technologies
acting as protective colloids to bacterial cells by maintaining the Several authors have reported a synergistic effect between pres-
membrane in a more fluid state during pressure treatments, thus sure and antimicrobial compounds like bacteriocins of LAB.
enhancing their resistance to pressure (Molina-Hoppner and oth- Rodrguez and others (2005) investigated E. coli O157:H7 in-
ers 2004). Carbohydrates are generally more protective than salts activation in raw milk cheese made with bacteriocin-producing
(Smelt 1998). Water activity and pH also play important roles. In LAB and HHP-treated on day 2 and 50 at 300 and 500 MPa.
low aw environments, enhanced survival of microorganisms oc- The authors observed a synergistic effect after 3 d of ripening that
curs due to cell shrinkage, which causes thickening of the cell persisted in 60-d-old cheese. Application of the combined treat-
membrane, thus reducing its permeability (Goh and others 2007). ment at day 50 was more effective than when applied on day 2,
Nevertheless, microorganisms injured by pressure are generally resulting in complete inactivation of E. coli in 60-d-old pressure-
more sensitive to low water activity (Smelt 1998). Bacteria are treated cheese (300 MPa) made with nisin A-producing L. lactis
sensitive to low pH and more sensitive to suboptimal pH after subsp. lactis TAB 50, L. lactis subsp. lactis biovar diacetylactis TAB
pressure treatments, therefore, low pH will not only enhance in- 57 producing noncharacterized bacteriocin TAB 57, enterocin
activation during HHP treatments, but also inhibit outgrowth of I-producing E. faecalis TAB 52, and enterocin AS-48-producing
injured cells (Smelt 1998). E. faecalis INIA 4. The authors attributed the higher inactivation
Morales and others (2006) evaluated the effect of cheese aw rate of HHP treatments applied at 50 d postmanufacture to dif-
and carbohydrate content on the barotolerance of L. monocyto- ferences in the physiological status of cells and to more favorable
genes Scott A. As expected, the higher the aw of the cheese, the conditions (substrate availability) for injured cells to recover at the
higher the inactivation rate, being 3.8 log cycle reductions at 400 beginning stages of manufacturing rather than at more advanced
MPa for 3 min in Hispanico cheese (aw value of 0.983) and 1 log stages. They hypothesized that synergism occurred due to sub-
cycle reduction in Mahon cheese (aw of 0.922) at 400 MPa for lethal injury of the outer membrane of Gram-negative cells or
18 min. Addition of lactose at a concentration of 5 mg/g to an changes in membrane fluidity caused by HHP treatments, facil-
85:15 mixture of Mahon cheese:distilled water did not influence itating the access of bacteriocins through the cytoplasmic mem-
L. monocytogenes barotolerance. On the other hand, galactose at brane. Arques and others (2005a,b) reported similar results when
the same concentration had a protective effect during HHP treat- combining bacteriocin-producing LAB and HHP treatments on
ments and glucose favored L. monocytogenes Scott A survival during S. aureus CECT 976 and L. monocytogenes Scott A survival in raw
refrigerated storage of pressurized samples. milk cheese. One day after pressure treatments, counts of S. au-
De Lamo-Castellv and others (2006) reported that no viable reus in control cheese were 6.46 log cfu/g. Bacteriocin-producing
cells of E. coli O59:H21 and O157:H7 were found in pressure- LAB lowered counts in cheese by up to 0.46 log cfu/g, while
treated (500 MPa) washed-curd cheese manufactured with and HHP treatments at 300 MPa caused a reduction of 0.45 log cfu/g
without starter culture when analyzed immediately after treat- and 2.43 log cfu/g at 500 MPa. Cheese made with bacteriocin-
ments. However, in cheese made with starter (pH 4.78), no cell- producing LAB treated at 300 MPa lowered S. aureus counts on
injury recovery was observed after 15 d of storage at 8 C, whereas day 3 by up to 1.02 log cfu/g and by up to 4.00 log cfu/g at
in cheese made without starter (pH 6.46) injured cells of both 500 MPa. For L. monocytogenes, control cheese had 7.03 log cfu/g,
serotypes recovered reaching counts of up to 6 log cfu/g at the while cheese with bacteriocin-producing LAB had a population of
end of the storage period. In a later study, the same research group 6.41 log cfu/g. Treatments at 300 MPa lowered counts to 6.13 log
evaluated the effect of similar HHP treatment conditions on other cfu/g and the combined effect of both treatments lowered counts
pathogenic bacteria. HHP treatments at 300 and 400 MPa ap- to 3.83 log cfu/g.
plied to cheese made with starter culture (pH about 4.82) caused In summary, HHP can increase the shelf-life and improve the
complete inactivation of S. Enteritidis CECT 4300 and S. Ty- safety of many cheese varieties. Recently, there have been many
phimurium CECT 443 with no recovery following 15 d of storage at disease outbreaks associated with raw or pasteurized cheese con-
12 C (De Lamo-Castellv and others 2007). In cheese made with- sumption all around the world (Table 2), which could be prevented
out starter culture (pH about 6.53) injured cells of both serotypes with the use of HHP alone or in combination with other preser-
recovered reaching counts over 3 log cfu/g after 15 d of storage. vation technologies. The barotolerance of spoilage and pathogenic
Table 2Recent outbreaks associated with cheese contaminated with pathogenic bacteria.
Year Country Cheese variety Pathogen Reference

1995 France, Germany, and Italy Soft and semi soft cheese L. monocytogenes Loncarevic and others 1995
1997 USA Raw milk cheese S. Typhimurium DT104 Villar and others 1999
2001 Italy, Germany, Austria, and France Soft and hard cheese L. monocytogenes Rudolf and Scherer 2001
2001 France Cantal cheese S. enterica Haeghebaert and others 2003
2002 Canada Unpasteurized Gouda cheese E. coli O157:H7 AICF 2003
2006 France Raw milk cheese S. enterica Domnguez and others 2009
2007 USA Raw milk fresh cheese S. Typhimurium CDC 2007
2010 USA Cold pack cheese food L. monocytogenes FDA 2010
2010 USA Queso fresco, panela, requeson L. monocytogenes FDA 2010
2010 USA Gorgonzola cheese E. coli O157:H7 FDA 2010
2010 USA Gouda and other cheese E. coli O157:H7 CDC 2010
L. monocytogenes
2010 Canada Grated cheese L. monocytogenes CFIA 2011
2011 USA Queso fresco S. aureus FDA 2011
2011 USA Blue cheese L. monocytogenes FSN 2011
2011 USA Cheddar cheese spread Salmonella spp. Marler 2011
2012 Australia Country cheese E. coli O157:H7 Food Standards 2012
L. monocytogenes
bacteria in cheese follow the order: S. aureus > L. monocytogenes Germination treatments of 60 MPa at 25 C for 210 min, fol-
> E. coli > A. hydrophila > Y. enterocolitica > S. enterica > yeasts, lowed by inactivation treatments of 500 MPa at 25 C for 15 min,
and molds. HHP treatments can achieve complete inactivation of caused a lethality of 2.7 log cycles of B. subtilis 4491 CECT spores
microorganisms in some cases. However, upon prolonged storage in Mato cheese that started with an initial concentration of around
injured cells may recover. Therefore, it is necessary to conduct 5 log cfu/mL in pasteurized milk prior to cheese making (Capellas
shelf-life studies over a period of time to ensure microbial safety. and others 2000). The same combination of treatments applied at
Generally speaking, HHP treatments will cause a higher microbial 40 C caused a 4.9 log cycle reduction. Under similar conditions
inactivation rate in cheese with higher aw and lower pH value. Ad- (60 MPa during 210 min at 30 C, followed by 500 MPa for 5 min
ditionally, the effectiveness of pressure treatments is greater when at 30 C), Lopez and others (2003) reported a 2 log cycle reduction
applied at more advanced stages of ripening, which also guaran- of B. cereus ATCC 9139 spores (initial count of 6 log cfu/g) after
tees safety in cheese contaminated postpasteurization. In certain 15 d of HHP treatments in washed-curd cheese. Additionally, the
cheese varieties, for example, fresh cheese, the use of high tem- same research group assessed the effect of pressure combined with
peratures (above 40 C) in HHP treatments could result in high the addition of nisin or lysozyme to cheese (Lopez-Pedemonte
whey losses and unacceptable textural characteristics. The com- and others 2003). The highest inactivation rate achieved was 2.4
bined effect between HHP treatments and bacteriocin-producing log cycle reductions at a germination cycle of 60 MPa at 30 C
LAB is synergistic, enhancing the rate of microbial inactivation for 210 min, followed by a destruction cycle of 400 MPa at 30 C
as compared to HHP treatments alone. An area of research that for 15 min with the presence of nisin (1.56 mg/L of milk).
needs more attention is the effect of HHP on the inactivation of It is clear from the few studies presented in this section that this
bacterial toxins. The pH of the system affects the susceptibility area of research needs attention in order to gain a better under-
of enterotoxins to thermal inactivation (Erikson 2003). Hence, standing of what factors could help enhance the inactivation of
strategies such as low pH values combined with HHP treatments microbial spores in cheese. Black and others (2011) stated that the
should be investigated. problems with the use of cycle treatments are super-dormancy and
inability to achieve 100% germination, which leads to low inacti-
Effect of High Hydrostatic Pressure on Microbial vation rates. The use of high temperatures (above 40 C) in HHP
Spores in Cheese treatments leads to higher spore inactivation rates as demonstrated
HHP treatment at 400 MPa applied to cheese at room tem- by Capellas and others (2000). However, as previously mentioned,
perature can easily inactivate yeast and mold spores. In Cheddar it may cause negative impacts on other cheese quality attributes.
cheese slurry, OReilly and others (2000a) reported 6 log cycle To avoid the use of high temperatures, the combination of 1 or
reductions of P. roqueforti spores at 400 MPa for 20 min at 20 C, more hurdles with HHP such as bacteriocin-producing LAB or
which did not recover following 72 h of incubation at 8 C. On low pH values should be assessed.
the other hand, bacterial spores can survive temperatures over 100
C and pressures exceeding 1000 MPa (Smelt and others 2002). Effect of High Hydrostatic Pressure on Cheese
Factors such as the low spore core water content, a thick pepti- Ripening and Related Agents
doglycan layer, low permeability of the inner spore membrane to Cheese ripening is a slow and expensive process due to high
hydrophilic molecules, and high levels of minerals and dipicolinic storage costs. Therefore, an efficient way to reduce aging time
acid account for their high resistance (Knorr and others 2011). without significantly affecting other quality attributes would pro-
The mechanism of bacterial spore inactivation by HHP involves vide significant savings to cheese manufacturers (El Soda and Awad
spore sensitization, at 1st by low-pressure treatments resulting in 2011). Proteolysis, lipolysis, and glycolysis along with secondary
the activation of nutrient germinant receptors, followed by high reactions of the products formed are the biochemical events in-
pressure treatments to inactivate the resultant germinated spores volved in ripening, catalyzed by enzymes derived from milk, co-
(Black and others 2007). During inactivation, events such as the agulant, starter LAB, nonstarter LAB, adjunct secondary cultures,
release of dipicolinic acid and small acid-soluble spore proteins, and secondary flora. Numerous research groups have assessed the
the hydrolysis of core and cortex, and the decrease of intracellular application of HHP treatments to accelerate the ripening of cheese.
pH occur (Rendueles and others 2011). The conditions evaluated can be grouped into: high pressure held

Table 3Effect of HHP treatments on the ripening process of different cheese varieties.
Treatment conditions
Cheese variety Moment of application P (MPa)/t (min, hd )/T ( C) Effects Reference
Proteolysis
Cheddar After salting 50/72 h/25 Similar taste and FAAe content of a 6 mo-old Yokoyama and others 1992
commercial cheese obtained in 3 d (Cheddar: 26.5
mg/g, Parmensan: 76.7 mg/g).
Cheddar 2, 7, 14, or 21 da 50/72 h/25 Faster s1 -casein hydrolysis and accumulation of OReilly and others 2000b
s1 -I-casein. Increased pH 4.6 SNf /TNg and FAA
levels.
Cheddar 1d 70400/3.581.5 h/25 Maximum accumulation of s1 -I-casein at 100 MPa OReilly and others 2003
and greatest increase in levels of pH 4.6 SN/TN
below150 MPa. Total FAA decreased as pressure
increased.
Cheddar 1 or 4 mob 200800/5/25 Ripening deceleration at pressure treatments 400 Wick and others 2004
MPa.
Camembert 5 or 10 d 0.1500/4 h/5 Most intense proteolysis at 50 MPa on d 10. Kolakowski and others 1998
Pere Joseph and Paillardin 2d 50/8 h/20 Accelerated proteolysis due to increased enzyme Messens and others 2000, 2001
activity and weakening of hydrophobic
interactions.
Blue-veined 42 d 400600/10/20 Accelerated breakdown of - and s2 -casein and Voigt and others 2010
increased levels of PTAh SN/TN.
Gouda After brining, 5 or 10 d 50 or 500/20100/14 No changes in pH 4.6 SN, PTA SN/TN, FAA content Kolakowski and others 1998;
and SDS-PAGE profiles. Messens and others 1999
Edam After salting, 4, 6, and 8 wkc 200 or 400/30/25 No changes in different fractions of nitrogen Iwanczak and Wisniewska 2005;
compounds.
Extracts of frozen Edam 1d 50 or 100/0.5 h/18 Wachowska 2010
Reduced-fat, low-moisture, 1, 5, 15, 20, and 25 d 400/520/212 5 No effect on the extent of casein degradation, pH 4.6 Johnston and Darcy 2000; OReilly
and immature SN/TN and total levels of FAA. and others 2002b; Sheehan and
mozzarella others 2005
Garrotxa 1d 400/5/14 followed by 50/72 h/14 Ripening period reduced from 28 to 14 d. Saldo and others 2000
Ewes milk cheese 1 or 15 d 200500/10/12 Increased peptidolytic activity and highest amount Juan and others 2007a; Juan and
of FAA at 300 MPa applied on d 1. Treatments of others 2008
500 MPa decelerated primary proteolysis.
Hispanico 15 d 400/5/10 Accelerated casein hydrolysis and increased total Avila and others 2006
FAA content.
La Serena 2 or 50 d 300 or 400/10/10 Levels of proteolysis were higher when HHP Garde and others 2007
treatments were applied at 400 MPa on d 2
compared to other treatments.
Lipolysis
Garrotxa 1d 400/5/14 Decelerated lipolysis due to lactic acid bacteria or Saldo and others 2003
lipolytic enzymes inactivation.
Ewes milk cheese 1 or 15 d 200500/10/12 Lowest concentration of total FFAi at pressure Juan and others 2007b
treatments of 400 to 500 MPa applied on d 15

after 60 d of ripening compared to other
treatments. Highest levels of FFAs were obtained
at 300 MPa applied on day 1 compared to other
treatments.
Hispanico 15 d 400/5/10 Esterase activity was not modified. Negligible Avila and others 2007
differences in individual FFA levels compared to
control.
Full-fat Cheddar 1d 400/10/25 Lipolysis was not significantly different from control Rynne and others 2008
over 180 d
Blue-veined 42 d 400600/10/20 Reduced lipolytic activity of P. roqueforti. Voigt and others 2010
Glycolysis
Full-fat Cheddar 1d 400/10/25 Concentration of total lactate in HHP-treated cheese Rynne and others 2008
was significantly lower compared to the control
after 180 d of ripening.
a d = day; b mo = month; c wk = weeks; d h = time in hours when specified; e FAA = free amino acids; f SN = soluble nitrogen; g TN = total nitrogen; h PTA = phosphotungstic acid; i FFA = free fatty acids.

for short times (300 to 600 MPa for 5 to 20 min), low to moderate tidase activity in cheese (Malone and others 2002; Juan and others
pressure retained for long periods of time (50 to 200 MPa for up 2007a). Juan and others (2008) reported autolysis of starter bac-
to 82 h), and combination of shock high pressure treatments fol- teria (L. lactis ssp. lactis and L. lactis ssp. cremoris) to be higher in
lowed by low to moderate pressure treatments (Table 3). Results ewes milk cheese when pressure treated at 300 MPa for 10 min at
have revealed that HHP treatments are able to accelerate cheese 12 C on day 1 of ripening than on day 15, compared to controls
ripening by causing alterations in enzyme structure, conforma- as determined by lactate dehydrogenase activity, yielding values of
tional changes in the casein matrix making it more susceptible 0.39, 0.30, and 0.27 U/g, respectively. These results are consis-
to the action of proteases, and/or bacterial lysis enhancing the tent with those of Malone and others (2002), who observed that
release of microbial enzymes that promote biochemical reactions L. lactis ssp. cremoris MG1363 cell suspensions lysed more rapidly
(Messens and others 1998; OReilly and others 2000b, 2003; Saldo when treated at 300 MPa than those treated between 100 to 200
and others 2000, 2002a; Garde and others 2007; Voigt and others and 600 to 800 MPa for 5 min. In contrast, cell lysis of L. lac-
2010). In addition, HHP treatments increase pH (0.1 to 0.7 units) tis strains 303, 223, 227, and AM2 did not occur in Cheddar
and modify water distribution of certain cheese varieties, leading cheese when subjected to HHP in the range of 100 to 400 MPa at
to enhanced conditions for enzymatic activity (Saldo and others 25 C for 20 min (OReilly and others 2002a). Also, lactate dehy-
2002b). drogenase activity in brined sheep cheese pressure-treated on day
15 of ripening at 200 or 500 MPa for 15 min at 20 C was not
Influence of High Hydrostatic Pressure on Proteolytic statistically different from the control cheese throughout 90 d of
Enzymes in Cheese ripening (Moschopoulou and others 2010).
Primary proteolysis results mainly from the action of plasmin, Aminopeptidase activity increased in ewes milk cheese when
chymosin, and to a lesser extent by pepsin, which are respon- HHP treated from 200 to 500 MPa and held for 10 min at 12 C,
sible for the initial hydrolysis of caseins in milk. Plasmin is the as cheese aged, and was higher in cheese pressure-treated on day
main indigenous proteinase in milk responsible for hydrolyzing 1 of ripening than that treated on day 15 (Juan and others 2007a).
s2 - and -caseins at the same rate and s1 -casein at a slower After 60 d of ripening, cheese pressure-treated at 300 MPa on
rate (Nielsen 2002). It is stable to pressures of up to 800 MPa in day 1 had the highest activity (8.03 nmol of Leu-p-NA/g per
cheese, depending on the temperature employed. For example, h) and cheese treated at 500 MPa on day 15, the lowest (2.19
the application of 800 MPa for 60 min at 8 C did not inactivate nmol of Leu-p-NA/g per h). On the other hand, in 15-d-old
plasmin in 14-d-old Cheddar cheese, while at 20 C its activity brined sheep cheese, aminopeptidase activity was not significantly
was reduced by 15% compared to controls, and at 30 C up to 50% affected by HHP treatments of 200 or 500 MPa for 15 min at
(Huppertz and others 2004). On the other hand, chymosin is the 20 C (Moschopoulou and others 2010).
major proteinase in traditional animal rennet whose role in cheese
making is to hydrolyze the Phe105 -Met106 bond of -casein during Influence of High Hydrostatic Pressure on Cheese
the coagulation of milk (McSweeney and Sousa 2000). Chymosin Proteolysis
is much less barotolerant in cheese than plasmin, being stable to Pioneering research in cheese ripening acceleration by HHP
HHP treatments from 50 to 400 MPa when held between 10 treatments began with work performed by Yokoyama and oth-
and 100 min at temperatures from 2 to 30 C (Messens and others (1993) who significantly reduced ripening times of Japanese
ers 1999; Trujillo and others 2000b; OReilly and others 2002a; Cheddar and Parmesan-type cheese without affecting sensory at-
Huppertz and others 2004; Rynne and others 2008), although tributes. In the case of Cheddar cheese, a 3-d-old cheese made
Saldo and others (2002a) reported that residual coagulant activity with 10 times more starter culture than usual had similar FAA
was reduced to about half the value of control cheese after HHP levels compared to a 6-mo-old commercial Cheddar cheese af-
treatments of 400 MPa for 5 min at 14 C applied to Garrotxa ter undergoing HHP treatments from 5 to 200 MPa for 72 h at
cheese on the 1st day of ripening. Juan and others (2007a) observed 25 C. FAA levels were 16.2, 20.3, 26.5, and 25.3 mg/g after
a similar result in treatments of 400 MPa applied for 10 min at HHP treatments at 5, 15, 50, and 200 MPa, respectively, while in
12 C postmanufacture on semi-hard ewes milk cheese. Chy- control cheese the FAA level was 21.3 mg/g. Taste was consid-
mosin activity reduced by 62% compared to control cheese at day erably superior for the Cheddar cheese HHP-treated at 50 MPa
15 of ripening. and commercial control cheese. For the Parmesan-type cheese,
Other proteinases such as cell envelope proteinase from starter the authors treated cheese curd with added italase and lipase at 50
LAB participate in primary proteolysis by hydrolyzing the MPa for 72 h at 25 C and claimed that the resultant cheese also
intermediate-sized and short peptides produced from the caseins had considerably superior taste just like the controls. FAA levels
by the action of chymosin or plasmin (Upadhyay and others 2004). were 76.7 mg/g for treated cheese and 88.7 mg/g for commercial
However, information on the effect of HHP treatments when ap- control cheese. Since the findings of Yokoyama and others many
plied directly to cheese on these enzymes is scarce. Furthermore, other research groups have attempted to reproduce their results on
there are no published studies on the effect of pressure on the Cheddar and other cheese varieties.
activity of proteolytic enzymes of adjunct secondary cultures (for OReilly and others (2000b) investigated HHP treatments ap-
example, Penicillium roqueforti and Penicillium camemberti), which plied at 50 MPa for 72 h at 25 C on day 2, 7, 14, 21, and 28 of age
have an important role in smear and mold-ripened cheese. on commercial Irish Cheddar cheese ripening. Results showed a
Secondary proteolysis results mainly from the action of starter significant decrease in the levels of s1 -casein and accumulation
peptidases, which degrade peptides and produce free amino acids of s1 -I-casein in cheese during HHP treatments. Pressures ap-
(FAA). Most of these enzymes require autolysis of starter bacteria plied on day 2, 7, and 14 increased pH 4.6 SN/TN by as much
to be released into the cheese matrix, since they are intracellular as 2-fold compared to controls, while those applied at more ad-
enzymes. Results from different studies have shown that pressure- vanced stages of ripening caused no significant differences. The
induced lysis is strain dependent and that HHP treatments can authors found increased levels of FAA by 1.4-(Met) to 3.9-fold
increase the autolysis of starter culture cells and affect aminopep- (Gly, Leu, and Phe) when applying HHP treatments on day 2 of

ripening. A few years later, the same research group studied the tense proteolysis at pressures of 50 MPa for 10-d-old cheese. In
acceleration of Cheddar cheese ripening at more intense pressure 42-d-old Irish blue-veined cheese, HHP treatments at 400 and
conditions (70 to 400 MPa for 3.5 to 81.5 h at 25 C) (OReilly 600 MPa for 20 min at 20 C accelerated primary and secondary
and others 2003). HHP treatments of 100 MPa held for 70 h proteolysis as a result of enzyme activation or changes in protein
resulted in increased degradation of s1 -casein and maximum ac- conformation (Voigt and others 2010). Two-dimensional SDS-
cumulation of s1 -I-casein, while treatments performed between PAGE gel electrophoresis indicated accelerated breakdown of -
350 and 400 MPa resulted in reduced accumulation. Treatments and s2 -casein at 400 and 600 MPa. Levels of phosphotungstic
below 150 MPa caused the greatest increases in levels of pH 4.6 acid (PTA) SN/TN after 14 and 28 d of pressure treatments were
SN/TN in cheese. Production of total FAA decreased as pressure 8.65% and 10.79%, respectively, while those of control cheese were
increased from 100 to 400 MPa. Conversely, increasing process- 4.56% and 9.04%. Contradictory results were found by Messens
ing time up to 60 h, raised total FAA levels. Overall, data from and others (1999) and Kolakowski and others (1998) who did
these research studies on Cheddar cheese ripening clearly demon- not observe any significant differences in proteolysis rates between
strate that HHP treatments enhanced proteolysis. However, results pressure-treated Gouda cheese and control cheese after applying
were not as significant as those obtained by Yokoyama and oth- HHP treatments between 50 and 500 MPa held for 20 to 100
ers (1993). OReilly and co-workers attributed differences to the min at 14 C as determined by pH 4.6 soluble nitrogen (SN),
type (more proteolytic) and quantity of starter culture used in the PTA SN, FAA content, and SDS-PAGE profiles, despite finding
manufacturing process of Japanese Cheddar cheese. Other relevant higher pH values in pressure-treated cheese. Moreover, Messens
findings from these studies were that while HHP enhanced prote- and others (1999) also tested the same HHP treatment conditions
olysis, it did not lead to altered pathways of proteolysis, thus flavor employed by Yokoyama and others (1993) to accelerate Ched-
and texture development is very similar in HHP-treated Cheddar dar cheese ripening and reported no acceleration of Gouda cheese
cheese and in traditional commercial Cheddar cheese. ripening. Differences encountered in these studies could be related
On the other hand, Wick and others (2004) subjected 1- and to the proteolytic activity of peptidases from secondary cultures
4-mo-old commercial cheese to pressures ranging from 200 to and to the levels and activity of residual rennet in each cheese va-
800 MPa for 5 min at 25 C and reported that HHP treatments riety. Proteolysis is more pronounced in mold- and smear-ripened
400 MPa could be useful in arresting ripening. FAA levels in cheese than in bacterially ripened cheese since not only proteinases
1-mo-old cheese treated at pressures of 400, 500, and 800 MPa and peptidases from starter bacteria, plasmin, and rennet partic-
were approximately 0.09, 0.06, and 0.04 mmol/g after 160 days ipate, but also exo- and endopeptidases from secondary cultures
after the pressure treatments, respectively, while those treated at (Voigt and others 2010). Unfortunately, as previously stated, the
lower pressures (200 and 300 MPa) had the same FAA content effect of HHP treatments applied directly to cheese on the ac-
as the controls (0.16 mmol/g). Pressure treatments (500 to 800 tivity of proteolytic enzymes of adjunct secondary cultures is not
MPa) applied to 4-mo-old cheese resulted in significantly lower well known. Concerning residual rennet activity, levels range from
FAA content than control cheese beyond 56 d of storage. Similarly, 15% in Gouda cheese to about 50% in Camembert cheese, typi-
Rynne and others (2008) suggested that HHP conditions of 400 cally being higher in Camembert, followed by Cheddar and lower
MPa for 10 min at room temperature applied to 1-d-old full-fat in Gouda cheese (Bansal and others 2007, 2009). Hence, low-
Cheddar cheese may be useful to arrest or slow down ripening. intensity HHP treatments may enhance chymosin activity to a
These studies along with those performed by OReilly and others greater extent in certain cheese varieties in comparison with oth-
indicate that low to moderate HHP treatment conditions (50 to ers depending on natural residual activity level.
150 MPa) applied to young Cheddar cheese are effective at ac- More recently, Wachowska (2010) applied HHP treatments at
celerating proteolysis, whereas higher HHP treatment conditions 50 and 100 MPa for 0.5 h at 18 C to extracts of frozen Edam
(400 MPa) may help cheese manufacturers arrest the ripening cheese after 1, 4, 6, and 8 wk of ripening in order to, 1st, induce
process at a desired stage, thus maintaining optimum commercial lysis of starter culture cells and, second, enhance enzyme activity.
attributes for a longer period of time. Results showed no significant differences in the proteolytic activ-
Accelerated proteolysis due to HHP treatment has also been ity of enzymes from controls and frozen pressurized cheese. These
achieved in other cheese varieties such as smear and mold-ripened results were similar to those reported by Iwanczak and Wisniewska
cheese, Garrotxa, and ewes milk cheese, but not in Gouda, Edam, (2005) in which Edam cheese subjected to pressurization at 200
or mozzarella cheese. and 400 MPa for 30 min at room temperature directly after salting,
The application of 50 MPa for 8 h at 20 C to Pere Joseph and and after 4, 6, and 8 wk of ripening, did not differ in proteolysis
Paillardin cheese accelerated proteolysis near the rind (Messens indexes from controls as measured by levels of nonprotein nitro-
and others 2000, 2001). The authors noted increased pH in HHP- gen, amino acid nitrogen, and pH 4.6 SN. In Garrotxa cheese
treated cheese, which probably resulted in a higher amount and/or pressurized at 50 MPa for 72 h at 14 C 1 d after salting, levels
activity of proteolytic enzymes of Brevibacterium linens and Peni- of proteolysis were only slightly different from those in control
cillium camemberti, and in higher activity of peptidases of starter cheese, with differences being less apparent after 28 d of ripening
culture. They also observed higher levels of 12% TCA-SN/TN (Saldo and others 2002a). However, treatments at 400 MPa for 5
and FAAs near the center of HHP-treated cheese, probably as a min enhanced the production of FAAs, reaching twice the value
result of diffusion toward the center of small peptides and amino found in control cheese after 28 d. An increase in peptidase activity
acids formed at the rind. In addition to the pH effect, Messens and (produced by cell lysis) favored by high moisture content and pH
others attributed the enhancement of proteolysis to a weakening (33.6%, 5.0 in controls and 39.7%, 5.4 in pressure-treated cheese)
of hydrophobic interactions, which might have led to an increased caused the acceleration of secondary proteolysis. The combination
exposure of susceptible bonds that are cleavable by proteolytic of these last 2 conditions (shock high pressure treatment at 400
enzymes. Similarly, in Camembert cheese exposed to HHP treat- MPa for 5 min at 14 C, followed by a low-pressure treatment
ments from 0.1 to 500 MPa for 4 h at 5 C after 5 or 10 d of 50 MPa for 72 h), reduced the ripening period of Garrotxa
of ripening Kolakowski and others (1998) observed the most in- from 28 to 14 d as determined by noncasein nitrogen, nonprotein
nitrogen, and FAA levels (Saldo and others 2000). According to phthaldialdehyde test, was highest in cheese treated at 400 MPa on
the authors, the treatment at 400 MPa caused a release of micro- day 2 after 60 days of ripening. Levels of Ile, Ser, Pro, Met, and Thr
bial enzymes into the cheese matrix, and the 50 MPa treatment more than doubled compared with control cheese. In this study,
enhanced enzyme activity. To a certain extent, the use of different higher aminopeptidase activity on Lys-p-NA favored by higher
starter cultures in Edam cheese and Garrotxa cheese could have pH values and conformational changes in peptide structures were
led to the different outcomes observed during secondary protein part responsible for enhanced proteolysis. In contrast, the re-
olysis in these cheese varieties after pressure treatments. Starter sults reported by Juan and others (2007a) show that cheese treated
bacteria in Garrotxa cheese are lysed after an HHP treatment of at 300 or 400 MPa on day 2 exhibited lower casein degradation
400 MPa, causing a release of peptidases that accelerate secondary than controls after 60 d of ripening. Possible differences in the
proteolysis, whereas in Edam cheese, this effect does not occur. outcomes between studies could be related to the use of rennets
With regard to primary proteolysis, Saldo and others (2000) no- from different origin. Juan and others (2007a) used calf rennet,
ticed an increase in the proteolytic activity of rennet during HHP which contains chymosin and to a lesser extent pepsin, whereas
treatments, whereas Iwanczak and Wisniewska (2005) reported Garde and others (2007) used Cynara cardunculus aqueous extracts
no significant differences in the proteolytic activity of enzymes in that contain cardosin A and B, which could be affected more than
pressurized cheese and control, based on analysis of the content chymosin and pepsin by HHP treatments. The effect of pressure
of 12% trichloroacetic acid (TCA)-soluble nonprotein nitrogen on proteinases from this type of rennet has not been studied.
compounds and 2% TCA-soluble compounds. To summarize, the application of HHP treatments accelerates
In mozzarella cheese, HHP treatments have not resulted in ac- or arrests proteolysis in cheese depending on cheese variety and
celerated proteolysis under the conditions tested. Sheehan and on the intensity of treatments. Up to now, the most effective com-
others (2005) applied 400 MPa for 5 min at 21 C to 1-d-old bination of treatments employed to accelerate (Cheddar) cheese
reduced-fat mozzarella cheese (10.7% fat) and reported no signif- proteolysis without negatively affecting its sensory properties has
icant effect of HHP treatments on mean levels of pH 4.6 SN or been to add an abnormally large quantity of starter culture (up
PTA SN over 35 d of ripening. In a similar manner, OReilly to 10 times) followed by low-pressure treatment (Yokoyama and
and others (2002b) reported no significant differences in proteol- others 1993). Research focused on evaluating the direct applica-
ysis indexes in pressure-treated (400 MPa for 20 min at 25 C) tion of HHP treatments to cheese and the effects it causes on
low-moisture mozzarella cheese compared to controls at different enzymes from starter and secondary adjunct cultures are not avail-
stages of ripening (every 5 d starting from day 1 up to day 25). able and could help optimize treatment conditions to accelerate
There was no effect on the extent of casein degradation, pH 4.6 or decelerate cheese ripening. For commercial purposes, it would
SN/TN, and total levels of FAA. These results coincide with those be interesting to compare the results in proteolysis acceleration
of Johnston and Darcy (2000) on immature mozzarella cheese, in employing current methods individually (elevated ripening tem-
which proteolysis as indicated by water soluble nitrogen, was un- peratures, modified starters, and so on) and those obtained by
affected by HHP treatments. Chymosin inactivation in mozzarella HHP (OReilly and others 2001).
cheese, due to the utilization of high cooking temperatures during
manufacture, could, to a certain extent, explain the results from Influence of High Hydrostatic Pressure on Cheese
the previously described studies. Past research has demonstrated Lipolysis and Glycolysis
that among different cheese varieties, evaluated for the extent of Limited information is available on the impact of HHP treat-
residual coagulant activity, low-moisture part-skim mozzarella and ments on cheese lipolysis and glycolysis (Table 3). Lipolysis is the
mozzarella di bufala Campana have the lowest values (Bansal and major biochemical event in blue and Italian cheese varieties, car-
others 2009). ried out by esterases and lipases that catalyze the hydrolysis of the
Juan and others (2007a) evaluated changes in proteolysis of ester bond in milk triglycerides, yielding free fatty acids and glyc-
ewes milk cheese after HHP treatments from 200 to 500 MPa for erol and mono- and diglycerides (Avila and others 2007). Pressure
10 min at 12 C applied on the 1st and 15th d of ripening. At treatments 400 MPa applied to Garrotxa, blue-veined, ewes
60 d of ripening, pressures of 300 and 400 MPa applied on day milk, and Hispanico cheeses have resulted in decelerated lipolysis,
1 and pressures of 200 to 500 MPa applied on day 15 enhanced with a reduction of LAB counts or inactivation of enzymes as the
primary proteolysis, as determined by casein degradation, as a main factors causing this effect.
consequence of the barostability of plasmin combined with con- HHP treatments applied to Garrotxa cheese at 400 MPa for
formational changes in the casein structure. HHP treatments of 5 min at 14 C postmanufacture decelerated lipolysis, resulting in
500 MPa on day 1 produced the highest level of intact s1 -casein cheese with lower amounts of free fatty acid (FFA) (C4:0 , C6:0,
and para--casein as a result of chymosin inactivation. The authors and C8:0 ) compared to controls (Saldo and others 2003). Factors
observed increased peptidolytic activity and the highest amount considered having influenced results were reduction of lactococci
of FAA in cheese after treatment of 300 MPa applied on day 1, counts (3 log units) or inactivation of lipolytic enzymes from sec-
which favored the lysis of starter bacteria, enhancing the release ondary microbiota in cheese caused by HHP treatments. Voigt and
of intracellular aminopeptidases into the cheese matrix. Avila and others (2010) reported similar observations at more intense HHP
others (2006) reported similar results in Hispanico cheese manu- treatment conditions in a 42-d-old blue-veined cheese. Levels of
factured with a mixture of cows and ewes milk. HHP treatments FFAs decreased to a greater extent in HHP-treated cheese than
at 400 MPa for 5 min at 10 C applied after 15 days of ripening in control cheese over 28 d of storage. According to the au-
accelerated the hydrolysis of casein and increased total FAA con- thors, this observation could reflect reduced lipolytic activity of P.
tent. Also, Garde and others (2007) assessed the effect of HHP roqueforti, consistent with the 3.42 log cycle reduction caused by
treatments at 300 or 400 MPa for 10 min at 10 C applied on treatment of 600 MPa for 10 min at 20 C compared to control
days 2 or 50 of ripening on the proteolysis of La Serena cheese cheese which experienced a 2.68 log cycle reduction during the
made from raw sheep milk. Proteolysis, as determined by the o- same time period. In ewes milk cheese pressure-treated at 400 to

500 MPa on day 15 of ripening for 10 min at 12 C, Juan and Influence on Physicochemical Properties
others (2007b) reported the lowest concentration of total FFAs HHP treatments do not change total solid, ash, fat, protein,
compared to controls at 60 d of evaluation. They attributed this moisture, and nutrient contents in cheese (Capellas and others
result to reduced water availability for the enzyme at this stage 2001; Sandra and others 2004; Serrano and others 2004; Sheehan
of ripening or to lipid-protein interactions, which could have and others 2005; Rynne and others 2008; Moschopoulou and
protected lipid hydrolysis by enzyme action. On the other hand, others 2010; Koca and others 2011). On the other hand, pressure
cheese pressure-treated on day 1 of ripening at 300 MPa exhibited treatments modify the pH to an extent that depends on treatment
the highest levels of C8:0 , C10:0 , C14:0 , and C18:1 FFAs after 60 d conditions and cheese age. Research studies have shown a higher
of ripening presumably as a result of faster release of intracellular pH value of pressure-treated cheese compared to controls in vari-
enzymes into the cheese induced by pressure treatments. eties such as Camembert (Kolakowski and others 1998), Cheddar
Avila and others (2007) investigated the effect of HHP treat- (Rynne and others 2008), ewes milk cheese (Juan and others
ments applied after 15 d of ripening at 400 MPa for 5 min at 10 C, 2007a, 2008), fresh cheese (Sandra and others 2004; Okpala and
separately or combined with addition of bacteriocin-producing others 2010), Edam (Iwanczak and Wisniewska 2005), Garrotxa
LAB, on the release of intracellular esterases and cheese lipolysis (Saldo and others 2000, 2002a), Gouda (Kolakowski and oth-
in Hispanico cheese. On day 15, the esterase activity value found ers 1998; Messens and others 1998, 1999), Manchego (Pavia and
in pressure-treated cheese was similar to that of controls (0.49 and others 2000), mozzarella (Johnston and Darcy 2000), La Serena
0.52 pmol of -naphthol released/min/g of cheese, respectively), (Arques and others 2006, Garde and others 2007), Pere Joseph
with no significant differences after 50 d of ripening (0.99 and (Messens and others 2000), and Paillardin (Messens and others
1.08 pmol of -naphthol released/min/g of cheese, respectively), 2001). This result is more pronounced at higher pressure levels,
indicating a notable barotolerance of the enzyme. However, total longer exposure times, and when applying treatments at an early
FFAs (C4:0 -C18:2 ) were lower in treated cheese (579.90 mg/kg stage of ripening, due to the release of colloidal calcium phosphate
of cheese) than in control cheese (612.47 mg/kg of cheese) after into the aqueous phase of cheese, LAB inactivation, or reduced
50 d as a result of LAB inactivation. Combined treatments, includ- ability of LAB to produce acid even when there is no apparent loss
ing addition of bacteriocin-producing LAB and cheese pressuriza- of cell viability as a result of damage to the glycolytic enzymes.
tion, produced the highest value of esterase activity after 50 d of However, pH differences between treated and nontreated samples
ripening in comparison to other treatments, with 1.38 pmol of become less significant during the ripening process.
-naphthol released/min/g of cheese due to lysis of LAB cells, fol- HHP treatments also alter water and salt distribution in the
lowed by the release of esterases into the cheese matrix. In general, cheese matrix. Messens and others (1999) observed a reduction in
HHP-treated cheese with bacteriocin-producing LAB showed the water loss during brining of Gouda cheese at pressures from 300
same pattern of lipolysis (release of FFAs) than controls. In full-fat to 500 MPa. Explanations offered for this phenomenon were the
Cheddar cheese, treated postmanufacture at 400 MPa for 10 min conversion of free water into protein-bound water and a reduced
at room temperature, lipolysis was not significantly different from compliance of the cheese matrix during pressure brining. Saldo
controls over 180 d of ripening (Rynne and others 2008). Total and others (2001) made similar observations on Garrotxa cheese
FFA levels in the treated cheese were numerically higher than treated at 50 MPa for 72 h at 25 C. Results showed that treated
those in the control cheese up to 42 d, but were lower thereafter, samples and controls had the same moisture contents, but water
with approximately 1100 mg/kg of cheese in treated cheese at 180 retention was different. HHP-treated cheese had 12.7% free wa-
d of ripening and 1200 mg/kg of cheese in control cheese. ter and 27.6% bound water, whereas control cheese had 18.9%
The metabolism of residual lactose, lactate, and citrate (glycol- free water and 21.4% bound water. They also observed that so-
ysis) is essential in the early stage of ripening in all cheese varieties lute diffusion improved by pressure treatments as enhanced salt
(McSweeney 2004), but is the least studied in regard to HHP treat- distribution occurred in treated cheese. Likewise, Juan and others
ments. Only 1 research group has evaluated changes in glycolysis (2008) observed better salt diffusion in ewes milk cheese pressure-
in cheese after HHP treatments. Employing the same conditions treated at 300 MPa for 10 min at 12 C on day 1 or 15 of ripening.
previously described in the study of lipolysis, Rynne and others HHP-treated cheese showed higher levels of salt-in-moisture con-
(2008) observed the mean concentration of total lactate in HHP- tent in the medium and interior sectors than control cheese at 15
treated cheese to be significantly lower compared to controls after and 60 d of ripening, respectively. In contrast, HHP treatments
180 d of ripening, with 1.1 g/100 g of cheese in treated cheese and from 50 to 500 MPa applied to Gouda cheese and Manchego
1.4 g/100 g in control cheese. The authors attributed the result cheese during brining did not significantly affect salt uptake or salt
to the inactivation of starter bacteria as a consequence of HHP diffusion (Messens and others 1999; Pavia and others 2000). Saldo
treatments. The mean concentration of D (-)- and L (+)-lactate also and others (2001) stated that the preliminary step of salt intake by
decreased significantly with the pressure treatment. capillarity seems necessary to allow the increase in solute mobility
observed in cheese samples subjected to HHP.
Effect of High Hydrostatic Pressure on Color is another parameter significantly affected when apply-
Physicochemical, Rheological, and Sensory ing HHP to cheese, and the factors that influence this attribute
Properties of Cheese the most are treatment temperature, pressure intensity, and hold-
The physicochemical and sensory properties of cheese are the ing time. Total color difference values of 1-d-old Mato cheese
most valued. Almost all varieties have special characteristics that treated at 500 MPa for 5, 15, and 30 min at 10 C were higher
make them different in commercial terms. Therefore, ensuring that than those of cheese treated at 25 C and in 5 min cycles, mainly
the processing technologies applied to them do not affect these due to L value changes which were lower compared to con-
identity attributes in a negative fashion is of utmost importance. trols (Capellas and others 2001). The b value was the index that
Table 4 summarizes the results from studies conducted on cheese changed the most in all treatments, increasing as pressure holding
in regard to the impact HHP treatments have on physicochemical, time increased. The authors related increase in lightness and yel-
rheological, and sensory properties. lowness of the cheese surface to microstructural changes. Control

Table 4 Effect of HHP treatments on cheese quality parameters.
Parameter Moment of Treatment conditions

evaluated Cheese variety application P (MPa)/t (min)/T ( C) Impact Reference
Color Mato 1 da 500/5, 10, or 15/10 L and a decreased, whereas b increased compared to Capellas and others 2001
control cheese.

Garrotxa 1d 400/5/14 Lower lightness and higher chroma values than control Saldo and others 2002c
cheese.
Queso fresco 1d 400/20/20 More yellowish after 1 d posttreatment than control cheese, Sandra and others 2004
but not after 8 d.
Cheddar, Turkish white-brined 1d 50400/5, 10, or 15/2225 Increasing pressure intensity and holding time did not affect Koca and others 2011; Rynne
L , but a decreased and b increased compared to and others 2008
control cheese.
Rheological properties Stirred and milled-curd Cheddar 1d 345 or 483/3 or 7/N.S.c Accelerated shredability (microstructure and sensory Serrano and others 2004;
properties of 27-d-old commercial cheese obtained in 1 d). Serrano and others 2005
Cheddar 1 and 4 mob 200800/5/25 Pressures up to 300 MPa applied to 1-mo-old cheese had no Wick and others 2004
significant effect. At 800 MPa, cheese had similar fracture
stress and Youngs modulus as control cheese. Pressure
applied to 4-mo-old cheese increased fracture work.
Cheddar 1d 400/10/25 Increased fracture strain and fracture stress values, lower Rynne and others 2008
fluidity, flowability, and stretchability increased up to 21
d, but to a lesser extent than in control cheese.
Low-moisture mozzarella 1 and 5 d 400/20/25 Reduced time required to attain satisfactory cooking OReilly and others 2002b
performance (by 15 d). Increased fluidity, flowability,
stretchability, and reduced melting time on heating at
280 C.
Reduced-fat mozzarella 1d 400/5/21 No significant effect on rheological properties. Sheehan and others 2005
Gouda 3d 50, 225, or 400/1 h / 14 Less rigid and solid-like, more viscoelastic, and had less Messens and others 2000
resistance to flow at longer times.
Ewes milk cheese 1 or 15 d 200500/10/12 Moderate pressures applied on day 1 enhanced firmness and Juan and others 2007c
cheese treated at higher pressures showed highest
deformability, lowest fracturability, and rigidity.
Garrotxa 50/72 h/25 More fluid and less elastic than controls. Saldo and others 2001
La Serena 2 or 50 d 300 or 400/10/10 Highest fracturability, hardness, and elasticity in cheese Garde and others 2007
treated on day 2.
Sensory properties Hispanico 15 d 400/5/10 Treatments applied to immature cheese limit the formation Avila and others 2006
Ewes milk cheese 1 or 15 d 200 or 500/10/12 of volatile compounds. However, differences become less Juan and others 2007d
significant during ripening.
La Serena 2 or 50 d 300 or 400/10/14 Treatments applied at more advanced stages do not cause Arques and others 2007
Raw goat milk cheese 1, 3, or 50 d 400 or 600/7/10 significant differences compared to control cheese. Delgado and others 2011
a d = day; b mo = month; c N.S. = not specified.
Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 409
cheese displayed longitudinal concavities on the surface, whereas cooking performance (OReilly and others 2002b). HHP-treated
pressure-treated cheese had a more uniform and smoother surface. cheese showed an increase in fluidity, flowability, stretchability,
Trained panelists also perceived HHP-treated queso fresco cheese and reduced melting time on heating at 280 C due to an en-
(400 MPa for 20 min at 20 C) to be more yellow than controls hanced development of age-related swelling of the paracasein ma-
when evaluated 1 d after pressurization (Sandra and others 2004). trix and increased protein hydration. In contrast, Sheehan and
However, cheese evaluated 8 d after pressure treatments displayed others (2005) reported no significant effect on rheological prop-
no significant differences in comparison with controls. erties of reduced-fat mozzarella cheese after an HHP treatment
Saldo and others (2002c) evaluated color changes in HHP- of 400 MPa for 5 min. They attributed the differences between
treated Garrotxa cheese at 400 MPa for 5 min at 14 C 3 d their study and that of OReilly and others to the higher protein
postpressurization, during ripening, and 60 d after pressure treat- and lower fat levels in their cheese, moment of application, and
ment. L-values were significantly lower in pressure-treated cheese pressure holding times. Rynne and others (2008) evaluated sim-
from day 3 to 30, after which they became similar to the val- ilar conditions to those tested in low-moisture mozzarella cheese
ues observed in control cheese, whereas a- and b-parameters were on Cheddar cheese. They reported that HHP treatments at 400
higher throughout the evaluation period with treated cheese hav- MPa applied for 10 min at room temperature 1-d postmanu-
ing a more yellow-orange color. Saldo and others did not assess facture did not significantly affect the mean values for firmness,
changes in the microstructure of cheese at the treatment con- but increased fracture strain and fracture stress values throughout
ditions employed, but stated that changes in cheese color after 180 d of ripening. Pressure negatively affected viscoelastic and
HHP treatments could be related to differences in microstructure cooking properties. Treated cheese had lower fluidity and flowabil-
between treated and untreated cheese. More recently, Koca and ity than control cheese. Although stretchability increased up to 21
others (2011) pressure-treated Turkish brined white cheese in the d, it did so to a lesser extent than control cheese (24.5 cm at day 1 to
range of 50 to 400 MPa held for 5 and 15 min at 22 C and did 30 cm at day 21 compared to 13.7 cm at day 1 to 66.3 cm at day
not observe any effect on the L value. However, higher pressure 21). According to the authors, differences in both studies could
levels and longer pressure-holding times resulted in significantly be related to insufficient hydration of the paracasein matrix in the
lower a values and higher b values, making treated cheese more HHP-treated Cheddar cheese at the conditions evaluated.
greenish and yellowish. Cheese treated at 50 and 100 MPa had Juan and others (2007c) studied the effect of pressure treaments
a sponge-like structure with fat globules of different sizes and from 200 to 500 MPa for 10 min at 12 C, applied on day 1
also large mechanical holes in the protein matrix, similar to un- or 15 after manufacture, on ewes milk cheese rheological and
pressurized cheese, while those treated at 200 and 400 MPa had textural characteristics. Cheese treated on day 15 was similar to
denser and more continuous casein structures. Rynne and oth- control cheese. Moderate pressures (200 to 300 MPa) enhanced
ers (2008) made similar observations on 1-d-old full-fat Cheddar firmness and cheese treated at higher pressures (500 MPa) showed
cheese treated at 400 MPa for 10 min at room temperature. Color the highest deformability and the lowest fracturability and rigidity.
analysis of HHP-treated cheese indicated that L-values remained Juan and others related their results to higher water retention ca-
constant, a-values decreased, and b-values increased in compari- pacity, higher pH value, and a more homogeneous microstructure
son with controls, resulting in cheese being more green and yellow in HHP-treated cheese, which contributed to higher disposition
throughout the evaluation period of 6 mo. to deformation and to a reduction of possible areas of fracture.
Trained panelists evaluated textural properties of cheese at 30 and
Influence on Rheological Properties 60 d of ripening and found cheese treated at 500 MPa to be less
The rheological properties of cheese are important to manu- crumbly and to be the most elastic cheese among all the cheeses
facturers since they influence texture, eating quality, and phys- subjected to different HHP conditions. Other research studies have
ical behavior, which depend on composition, microstructure, reported similar observations in other cheese varieties at high-
macrostructure, and physicochemical state of components (Guinee pressure conditions. Low-pressure treatments (50 MPa for 72 h at
2011). Serrano and co-workers have described one of the most sig- 25 C) applied to Garrotxa cheese made it more fluid and less elas-
nificant findings of the impact of HHP on cheese rheology. Mod- tic than controls (Saldo and others 2001). Hardness and shortness
erate pressure treatments (345 and 483 MPa) applied to unripened remained higher in control cheese, indicating a softening of cheese
milled or stirred-curd Cheddar cheese for up to 7 min modified its due to a weakening of the casein matrix. Higher pressure treat-
microstructure and textural properties, which resulted in acceler- ments (400 MPa for 5 min at 14 C) resulted in cheese being less
ated shredability (Serrano and others 2004, 2005). Results showed crumbly and more elastic than controls (Saldo and others 2000).
similar visual and tactile sensory properties for 27-d-old shred- In queso fresco cheese, controls and HHP-treated cheese (400
ded control cheese and 1-d-old pressure-treated shredded cheese. MPa for 20 min at 20 C) were not significantly different in most
Furthermore, HHP treatments reduced the amount of crumbles, textural attributes evaluated (Sandra and others 2004). The most
increased mean shred particle length, improved length unifor- notable difference found in this study was that pressure-treated
mity, and enhanced surface smoothness in shreds produced from cheese was less crumbly than controls. Texture profile analysis in-
unripened cheese. The authors stated that their results could re- dicated that firmness, gumminess, and chewiness were higher in
duce manufacturing costs to cheese processors that shred Cheddar treated cheese than in control cheese 1 d after pressure treatments,
cheese as a means of adding value to their product, by at least US but significantly lower after 8 d.
$30/1000 kg, when shredding immediately after block-cooling, Messens and others (2000) determined the rheological prop-
and suggested that their results could be applicable to other cheese erties of HHP-treated Gouda cheese (50, 225, and 400 MPa for
varieties. 1 h at 14 C applied 3 d after brining) immediately after pressure
In a study conducted on a low-moisture mozzarella cheese, release (day 0), and after 21 and 42 d of ripening. At day 0, the vis-
HHP treatments (400 MPa for 20 min) also accelerated age-related coelastic properties of cheese treated at 225 and 400 MPa differed
changes in microstructure, protein hydration, and cooking char- significantly from those of untreated cheese. HHP-treated cheese
acteristics, which reduced the time required to attain a satisfactory was less rigid and solid-like, more viscous, and had less resistance
to flow. According to the authors, these rheological changes were mal) were not significantly affected by any of the HHP treatments
due to the weakening of hydrophobic interactions and not to applied on day 2 or 50.
changes in the pH, water content, or proteolysis level. At day 42, Juan and others (2007d) investigated the effect of pressure condi-
there were no significant differences in the rheological properties tions between 200 and 500 MPa applied on day 1 or 15 of ripening
between treated and untreated cheese. Wick and others (2004) for 10 min at 12 C on the volatile profile of cheese made from
assessed the effects of HHP treatments ranging from 200 to 800 ewes milk. Cheese pressurized after 15 d of ripening and that
MPa for 5 min at 25 C on the rheological properties of 1- and treated on day 1 at 200 MPa were similar to controls. Higher pres-
4-mo-old Cheddar cheese. Pressures up to 300 MPa applied to 1- sure treatments applied on day 1 altered microbial populations and
mo-old cheese had no significant effect on fracture stress, fracture enzyme activities, enhancing or limiting the formation of volatile
strain, fracture work, and Youngs modulus. In a similar manner, compounds. Cheese pressure-treated at 300 MPa showed higher
extremely high pressure (800 MPa) resulted in cheese with similar levels of FFAs, ethanol, ethyl esters, and branched-chain aldehydes,
fracture stress and Youngs modulus across 160 d of storage than whereas cheese treated at 500 MPa showed the highest amounts
controls. HHP treatments applied to 4-mo-old cheese had no sig- of 2,3-butanedione, pyruvaldehyde, and methyl ketones and the
nificant effect on rheological properties, except for fracture work, lowest amount of alcohols.
which increased in HHP-treated cheese. Garde and others (2007) Avila and others (2006) investigated the effect on volatile com-
reported that fracturability, hardness, and elasticity were higher pounds, odor, and aroma of 15-d-old Hispanico cheese HHP-
throughout ripening in La Serena cheese, pressure-treated at 300 treated at 400 MPa for 5 min at 10 C made with and with-
or 400 MPa for 10 min at 10 C on day 2 of ripening, than in out bacteriocin-producing LAB culture. Treated cheese showed
control cheese and in cheese pressure-treated on day 50. Results higher levels of hexanal, 3-hydroxy-2-pentanone, 2-hydroxy-3-
showed a strong correlation between residual s1 - and -caseins pentanone, and hexane and lower levels of ethanal, ethanol,
and cheese hardness. HHP treatments on day 2 had a negative 1-propanol, ethyl acetate, ethyl butanoate, ethyl hexanoate, 2-
effect on texture preference when evaluated by trained panelists. pentanone, and butanoic acid in comparison with untreated
cheese. HHP-treated cheese received higher milky odor de-
Influence on Sensory Properties scriptor scores and lower scores for odor quality and intensity,
One of the most frequently cited benefits of employing HHP as well as, for buttery, yogurt-like, and caramel odor de-
in food processing over traditional methods, such as heating, is scriptors. Addition of the bacteriocin-producing LAB culture, en-
ensuring microbiological safety while still retaining the sensory hanced the formation of 3 aldehydes, 3 alcohols, 3 ethyl esters,
quality characteristics of fresh food products. In cheese, this is trueand 3 ketones, but decreased levels of 7 ketones and butanoic acid.
if treatment conditions are not too intense and not applied in Cheese made with bacteriocin-producing LAB received higher
the early stages of ripening. This behavior is mainly due to the scores for aroma intensity and for yogurt-like and cheesy
higher inactivation rates observed in HHP treatments applied on aroma descriptors.
immature cheese, which hinders the formation of certain volatile Alonso and others (2011) pressure-treated curds made from
compounds and lowers enzymatic activity. Ding and others (2001) sheep milk immediately after manufacture at 400 and 500 MPa
found more intense pressure treatments (550 MPa compared to for 10 min at 8 C and froze them for 4 mo. After thawing,
345 MPa) held for longer periods of time (30 min compared to 10 the authors mixed treated curds (20%) with fresh cow milk curd
min) to cause a greater reduction in microorganism counts with (80%) for the manufacture of Hispanico cheese. Cheese obtained
less outgrowth during ripening, which resulted in Swiss cheese with curds treated at 400 MPa showed the highest concentrations
slurries with less aroma development. Delgado and others (2011) of short-chain and long-chain FFAs, 2-propanol, 2-butanol, 2-
observed that lower pressure treatments (400 MPa compared to pentanol, and ethyl hexanoate after 30 and 60 d of manufacture,
600 MPa) applied at more advanced stages of ripening (50 d com- while those treated at 500 MPa had the lowest concentrations of
pared to 30 or 1 d) produced less intense changes in the volatile all compounds identified, except for 2,3-butanedione on day 60.
profile of treated raw milk goat cheese compared to controls. HHP All treatments (including controls) caused similar counts of to-
treatments applied on day 1 decreased the amount of most volatile tal viable bacteria, mesophilic LAB, and thermophilic LAB, but
compounds due to LAB inactivation, but enhanced the formation cheese treated at 400 MPa had higher enzyme activity compared
of ketones, hydrocarbons, and -decalactone. to controls as a result of cell lysis. The authors also stated that wild
Arques and others (2007) evaluated volatile compounds, odor, strains of LAB surviving HHP could be responsible for differences
and aroma of La Serena cheese HHP-treated at 300 or 400 MPa in the profile of cheese volatiles.
for 10 min at 10 C on day 2 or 50 after manufacture. HHP treat- The changes induced by HHP treatments described in the lit-
ments applied on day 50 did not influence either the volatile com- erature in regard with the physicochemical, rheological, and sen-
pound profile or the sensory characteristics of 60-d-old cheese. sory properties of cheese are not necessarily negative and in some
On the other hand, pressure treatments on day 2 enhanced the cases are even beneficial, economically speaking. Even though
formation of branched-chain aldehydes and 2-alcohols except 2- changes in these attributes can be observed when HHP treatments
butanol, but retarded the formation of n-aldehydes, 2-methyl ke- are applied in the early stages of ripening, they are minimized
tones, dihydroxy-ketones, n-alcohols, unsaturated alcohols, ethyl or even disappear during ripening. However, novel or distinctive
esters, propyl esters, and branched-chain esters. Differences in the cheese textures, aromas, tastes, and appearances can be obtained
levels of some volatile compounds between treated and untreated depending on treatment conditions which could be appealing to
cheeses disappeared during ripening. The odor quality and inten- consumers.
sity of 60-d-old cheese were not significantly affected by HHP
treatments on day 2, but aroma quality and intensity of cheese Commercial Applications and Opportunities for HHP
treated at 400 MPa resulted in significantly lower sensory scores Processing of Cheese
than obtained for the control cheese. Scores for families of odor The decision to implement HHP processing as a commer-
and aroma descriptors (lactic, vegetable, floral, toasted, and ani- cial preservation or ripening acceleration method requires careful

Treatment conditions
Pressure / Time / Temperature
Microorganisms Enzymes
S. aureus >
Plasmin >
L. monocytogenes >
E. coli >
Pepsin >
A. hydrophila >
Y. enterocolitica >
Chymosin
S. enterica >
yeasts and molds
Impact in cheese
Figure 1Schematic representation of the effect of HHP on microorganisms and enzymes in cheese.
planning based on technical and business plans (Farkas 2011). At at a constant pressure would imply costs of US $0.159/kg, while
the present moment, there are some cheeses and cheese-related 10 min would cost US $0.21/kg, 15 min US $0.263/kg, and 20
products processed with HHP technology available in the Euro- min US $0.316/kg.
pean market. These include sandwich fillings (based on cheese Several research studies have shown that pressure treatments at
mixed with other ingredients), cream cheese, Cheddar cheese 500 to 600 MPa applied to cheese for 5 to 20 min are sufficient
snacks, and cheese jerky which are pathogen-free, have increased to achieve over 5 log cycle reductions of S. aureus, L. monocyto-
shelf-life, and are being marketed as clean label products (Hiper- genes, and E. coli when applied soon after manufacture or at more
baric 2011). An advantage of HHP processing is the possibility advanced stages of ripening. Less severe pressure conditions (345
of reducing or eliminating additives and preservatives from food MPa for 3 min) are needed to accelerate Cheddar cheese shred-
products. Rodilla is a company located in Spain that reduced dability. Typical operating conditions for seafood, juice, and ready
production costs and increased refrigerated shelf-life of their sand- to eat products are 300, 450, and 590 MPa applied for 1, 1, and 3
wich fillings from 46 to 21 d by pressurizing at 500 MPa for min, respectively (Purroy 2009). Overall, depending on operating
several minutes without changing texture and flavor character- parameters and on the scale of operation, the cost of HHP pro-
istics (Tonello 2011). According to Purroy (2009), the costs of cessing is around US $0.05 to 0.5/kg of food (Rastogi and others
HHP processing are related to equipment capacity, pressure in- 2007). Undoubtedly, the costs of implementing HHP could seem
tensity, pressure holding time, and to the costs of labor, power, very high compared to traditional processing technologies. How-
and maintenance. The initial investment on HHP equipment can ever, product recalls can cost company large amounts of money
range from US $650,000 up to US $2,600,000 depending upon and permanently damage their brand. The human cost associ-
equipment capacity (55 to 425 L). Small and medium sized com- ated can be even more severe. In addition, reducing processing
panies that cannot afford HHP equipments or do not have suf- times through cheese ripening acceleration can have significant
ficient floor space can outsource contract service providers like impacts on production costs. Most types of soft cheese, including
HHP Food Services in California, APC in Wisconsin, Deli 24 in unpasteurized soft cheeses which have recently been implicated
Buckinghamshire, GL Foods in Texas, Millard in Nebraska, Safe in disease outbreaks such as panela, requeson (ricotta), and fresco
Pac in Pennsylvania, and Universal Cold Storage in Nebraska. are good candidates for HHP processing due to their high wa-
The HHP treatment cost per kilogram of food will depend on ter activity. Cheese varieties with low pH values (pH about 4.75)
the operating pressure intensity and pressure holding time. Present could also benefit from HHP pasteurization as confirmed by De
HHP processing costs at fixed processing times are approximately Lamo-Castellv and others (2006, 2007).
US $0.096/kg when treated at 300 MPa, US $0.112/kg at 400
MPa, US $0.129/kg at 500 MPa, and US $0.145/kg at 600 MPa. Final Remarks
The cost of wear parts are US $0.015/kg, US $0.026/kg, US The application of any new food processing technology presents
$0.034/kg, and US $0.05/kg for the stated pressure conditions, significant challenges to food technologists and scientists. HHP
respectively. With regard to processing times, 5 min holding time processing of cheese can ensure microbial safety and extend
product shelf-life. However, depending on the intensity of treat- Arques JL, Rodrguez E, Gaya P, Medina M, Nunez M. 2005b. Effect of
ment conditions and moment of application, physicochemical, combinations of high pressure treatments and bacteriocin-producing lactic
acid bacteria on the survival of Listeria monocytogenes on raw milk cheese. Intl
rheological, and sensory properties may be altered. Therefore, a Dairy J 15:893900.
good balance must be attained between ensuring microbial safety Avila M, Calzada J, Garde S, Nunez, M. 2007. Effect of a
and maintaining traditional cheese quality attributes. Although bacteriocin-producing Lactococcus lactis strain and high-pressure treatment on
immature cheese is more sensitive to changes induced by pressure the esterase activity and free fatty acids in Hispanico cheese. Int Dairy J
treatments, most of the observed changes are reversible and HHP- 17:141523.
induced differences become less significant compared to nonpres- Avila M, Garde S, Gaya P, Medina M, Nunez M. 2006. Effect of
high-pressure treatment and a bacteriocin-producing lactic culture on the
surized cheese during ripening. With regard to cheese ripening, proteolysis, texture, and taste of Hispanico cheese. J Dairy Sci 89:
application of HHP has mainly focused on ripening acceleration 288293.
to reduce production costs. Noteworthy accomplishments have Bansal N, Fox PF, McSweeney PHL. 2007. Factors affecting the retention of
been the reduction in ripening time from 6 mo to 3 d of Cheddar rennet in cheese curd. J Agric Food Chem 55:921925.
cheese without negatively affecting sensory attributes (which to Bansal N, Fox PF, McSweeney PHL. 2009. Comparison of the level of
residual coagulant activity in different cheese varieties. J Dairy Res
our knowledge has not been further investigated and evaluated on 76:29093.
a commercial scale), the acceleration of Cheddar cheese shred- Black EP, Setlow P, Hocking AD, Stewart CM, Kelly AL, Hoover DG.
ability, which could reduce manufacturing costs by at least US 2007. Response of spores to high-pressure processing. Compr Rev Food Sci
$30/1000 kg, and the reduction in time required to attain satisfac- Food Safety 6:10319.
tory cooking properties of mozzarella cheese. Current trends are Black EP, Stewart CM, Hoover, DG. 2011. Nonthermal processing
technologies for food. In: Zhang HQ, Barbosa-Canovas GV,
to apply HHP treatments at a desired stage in order to decelerate Balasubramanian VM, Dunne CP, Farkas DF, Yuan JTC, editors.
the ripening process and, therefore, extend optimal commercial Nonthermal processing technologies for food. Oxford: Wiley-Blackwell.
quality by controlling enzyme and bacterial participation. Gen- p 5171.
eral conclusions from this review can be schematically seen in Capellas M, Mor-Mur M, Gervilla R, Yuste J, Guamis B. 2000. Effect of
Figure 1. high pressure combined with mild heat or nisin on inoculated bacteria and
mesophiles of goats milk fresh cheese. Food Microbiol 17:63341.
Capellas M, Mor-Mur M, Sendra E, Guamis B. 2001. Effect of high-pressure
Nomenclature processing on physico-chemical characteristics of fresh goats milk cheese
(Mato). Intl Dairy J 11:16573.
HHP = high hydrostatic pressure Capellas M, Mor-Mur M, Sendra E, Pla R, Guamis B. 1996. Populations of
LAB = lactic acid bacteria aerobic mesophiles and inoculated Escherichia coli during storage of fresh
D-value = decimal reduction value goats milk cheese treated with high pressure. J Food Prot 59:58287.
Leu--NA = leucine-p-nitroanilide Carminati D, Gatti M, Bonvini B, Neviani E, Muchetti G. 2004.
High-pressure processing of Gorgonzola cheese: influence on Listeria
FAA = free amino acid monocytogenes inactivation and on sensory characteristics. J Food Prot
FFA = free fatty acid 67:167175.
TCA = trichloroacetic acid CDC (Centers for Disease Control and Prevention). 2007. Salmonella
PTA = phosphotungstic acid Typhimurium infection associated with raw milk and cheese consumption,
Pennsylvania, 2007 [Internet]. Atlanta, GA. Available from:
SN = soluble nitrogen http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5644a3.htm.
TN = total nitrogen Accessed Feb, 2012.
SDS-PAGE = sodium dodecyl sulfate polyacrylamide gel elec- CDC (Centers for Disease Control and Prevention). 2010. Investigation
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Acknowledgments CFIA (Canadian Food Inspection Agency). 2011. Certain grated cheese
Author Y. Martnez-Rodrguez acknowledges support from product with Parmesan may contain Listeria monocytogenes [Internet].
CONACYT (Mexico) via a Ph.D. fellowship (ref. 179692). The Available from: http://www.inspection.gc.ca/english/corpaffr/recarapp/
2011/20110301e.shtml. Accessed Feb, 2012.
authors thank Marvin Martnez for his valuable comments on the
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High Hydrostatic Pressure Processing of Cheese: Abstract

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High Hydrostatic Pressure Processing of Cheese

Introduction ufacturing, the application of HHP initially focused on pressure-

Microorganism Cheese Moment of application Treatment conditions Initial counts Inactivation

S. carnosus CECT 4491 Mato 1 500/5/50 8 7 Capellas and others 2000

c 2012 Institute of Food Technologists

Year Country Cheese variety Pathogen Reference

c 2012 Institute of Food Technologists

Parameter Moment of Treatment conditions

c 2012 Institute of Food Technologists

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