High pressure processing of cheese: Lights, shadows and prospects

International Dairy Journal 100 (2020) 104558

Contents lists available at ScienceDirect

International Dairy Journal journal homepage: www.elsevier.com/locate/idairyj

Review

High pressure processing of cheese: Lights, shadows and prospects ~ ez*, Javier Calzada, Ana del Olmo Manuel Nun n y Tecnología Agraria y Alimentaria (INIA), Carretera de La Corun ~ a km 7, Departamento de Tecnología de Alimentos, Instituto Nacional de Investigacio Madrid, 28040, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 12 April 2019 Received in revised form 27 August 2019 Accepted 28 August 2019 Available online 14 September 2019

Under high pressure processing (HPP) treatment conditions commonly used in the food industry, most cheese-borne pathogenic bacteria and spoilage microorganisms are eliminated. However, pressureresistant Bacillus and Clostridium spore-forming bacteria require more severe process parameters or combined strategies for their inactivation. Lactic acid bacteria and other microorganisms with a technological role in cheese manufacture and ripening show a strain-dependent fate after HPP treatment, influencing most product characteristics. Proteins and lipids, the major cheese constituents, are affected by HPP, resulting in modifications to matrix microstructure and cheese texture. Enzymes involved in cheese ripening are inactivated to a variable degree, depending on enzyme, substrate and treatment conditions, with subsequent effects on proteolysis, lipolysis and flavour compound formation. Acceleration and arresting of cheese ripening may be modulated by HPP and the appearance of defects may be prevented. Advantages, disadvantages and future prospects for the HPP of particular cheese types are discussed in this review. © 2019 Elsevier Ltd. All rights reserved.

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 The HPP of cheese: lights . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.1. Safe and long lasting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.1.1. Eliminating pathogenic bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.1.2. Hindering biogenic amine formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.1.3. Stabilising unstable cheeses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 2.2. Speeding up and braking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 2.2.1. HPP as the pedal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 2.2.2. Accelerating ripening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 2.2.3. Slowing down over-ripening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 2.3. Preventing defects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 2.3.1. Reducing bitterness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 2.3.2. Controlling spoilage bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 2.3.3. Dealing with eukaryotes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 The HPP of cheese: shadows . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 3.1. Recovery of HPP-injured cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 3.2. Changes in external appearance and colour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 3.3. Altered sensory properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 The HPP of cheese: prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 4.1. Overcoming limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 4.2. Seizing opportunities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

* Corresponding author. Tel.: þ 34 913476799. ~ ez). E-mail address: [email protected] (M. Nun https://doi.org/10.1016/j.idairyj.2019.104558 0958-6946/© 2019 Elsevier Ltd. All rights reserved.

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5.

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

1. Introduction High pressure processing (HPP) is no longer an emerging technology in the food industry. Installed industrial HPP equipment has sharply expanded from one in 1990 to a number close to 470 in 2018; at the same time, the capacity of HPP equipment has increased to volumes above 500 L with throughputs of 3000 kg h1 (Hiperbaric, 2019). Well-known advantages of HPP over thermal treatments from the perspective of both the nutritional and the sensory characteristics of foods, including dairy products, that rely on the use of low or mild temperatures and relatively short pros, & Guamis, cessing times (Trujillo, Ferragut, Juan, Roig-Sague 2016), are behind the success of this technology. The first results on the application of HPP to cheese were published as a patent (Yokohama, Sawamura, & Motobayashi, 1992), in which a beneficial effect on the acceleration of Cheddar cheese ripening as a result of treatment at 50 MPa for 72 h was reported. Afterwards, HPP treatments with long holding times were investigated for smear-ripened and white mould-ripened cheese (Messens, Foubert, Dewettinck, & Huyghebaert, 2000, 2001), Cheddar cheese (O'Reilly et al., 2003; O'Reilly, O'Connor, Murphy, Kelly, & Beresford, 2000b) and goat milk cheese (Saldo, Sendra, & Guamis, 2001). Independently of their beneficial effects on cheese proteolysis, those lengthy HPP treatments are far from being economically competitive and would not warrant industrial application to accelerate cheese ripening (O'Reilly, Kelly, Murphy, & Beresford, 2001). For this reason, results from studies in which HPP holding times exceed those commonly used at the food industry, generally set in minutes, will not be considered in detail in the present review. Although HPP treatment of cheese has been reviewed (Martínez-Rodríguez et al., 2012), novel information generated on the subject during the present decade has not been gathered in an updated review. Main applications of HPP at the cheese industry reported so far are improvement of product safety, extension of shelf life, acceleration or arrest of ripening, and prevention of quality defects. 2. The HPP of cheese: lights 2.1. Safe and long lasting Cheese is a safe dairy product. The low pH values of most cheese varieties, usually ranging from 4.8 to 5.4, constitute a critical hurdle for pathogen growth, which is also hindered by the organic acids derived from microbial metabolism, other inhibitory compounds of microbial origin such as bacteriocins, and the decrease in water activity (aw) caused by salt addition and moisture loss during ripening. Out of 67 different commercial cheeses, 53 types did not support growth of any pathogen during storage at 25  C whereas 14 types supported growth of Staphylococcus aureus, 6 of Salmonella spp., 4 of Listeria monocytogenes, and 3 of Escherichia coli O157:H7 (Leong et al., 2014). Cheese varieties with particular physicochemical or microbiological traits may require additional tools such as HPP to assure their microbiological safety. Cheese is a stable dairy product. In fact, cheese surged approximately 8000 years ago as a convenient procedure to preserve milk constituents and keep those valuable nutrients available for

consumption during long periods of time. As in the case of microbiological safety, low pH values and decrease in aw of most cheese types confer protection against spoilage microorganisms. However, cheeses manufactured for consumption as fresh products are prone to alterations because of their particular physicochemical characteristics. HPP appears as one of the strategies capable of preserving fresh cheeses. 2.1.1. Eliminating pathogenic bacteria From the point of view of their microbiological characteristics, raw milk cheeses are generally considered to be hazardous for certain population sectors (immunosuppressed individuals, pregnant women, elderly persons, infants) since the milk is not subjected to any technological treatment guaranteeing the elimination of potentially present pathogens. Among the 78 outbreaks attributed to cheeses that occurred during 1998e2011 in the United States, 34 were caused by unpasteurised milk cheeses (21 if cheeses imported from Mexico are excluded) and 44 by pasteurised milk cheeses (Gould, Mungai, & Behravesh, 2014). However, any conclusion from those data must be drawn with caution. During 2009e2014 in the United States, unpasteurised milk, consumed by only 3.2% of the population, and unpasteurised milk cheeses, consumed by only 1.6% of the population, caused 14 outbreaks due to Shiga toxin-producing E. coli, 8 to Salmonella spp., 1 to L. monocytogenes and 53 to Campylobacter spp., while pasteurised milk and pasteurised milk cheese caused 10 outbreaks associated with L. monocytogenes and 1 with Campylobacter spp. (Fig. 1). Ten of those 87 outbreaks were responsible for 17 deaths, 16 linked to L. monocytogenes and 1 to Campylobacter spp. (Costard, Espejo, Groenendaal, & Zagmutt, 2017). In the case of the European Union, out of the 71 outbreaks attributed to cheese during 2010e2013 according to the RASFF database on food safety hazards (Fig. 1), 34 were associated with Salmonella spp., 2 with Campylobacter spp., 3 with E. coli (one of them attributed to raw milk cheese), 3 with L. monocytogenes, 2 with Brucella spp., 23 with Staphylococcus enterotoxins, 2 with Bacillus toxins and 2 with calicivirus (van Asselt, van der Fels-Klerx, Marvin, van Bokhorst-van de Veen, & Nierop Groot, 2017). From the point of view of physicochemical characteristics, the risk of pathogen growth increases as the pH value does not reach or abandons the secure range. Retarded and/or reduced acidification of the curd, which may be caused by a bacteriophage attack to the starter culture, creates a favourable environment for pathogens. Although bacteriophage attack is not a frequent event, it may affect to practically all cheese types and therefore should not be dismissed as a food safety risk (Coffey, Stokes, Fitzgerald, & Ross, 2001; Dupont, Janzen, Vogensen, Josephsen, & Stuer-Lauridsen, 2004). In certain traditional cheese-making technologies, raw milk inoculation with lactic starter cultures is not the common practice, as it negatively influences cheese rheological characteristics ndez del Pozo, Rodríguez-Marín, Gaya, & Nun ~ ez, (Medina, Ferna 1991). The low populations of indigenous lactic acid bacteria (LAB) nowadays present in refrigerated raw milk are insufficient to lower the pH value and thereby create hostile environmental s, Garde, conditions for pathogens in curd and young cheese (Arque ~ ez, 2006). Gaya, Medina, & Nun Also, in the manufacture of some types of fresh cheese, pasteurised milk is directly coagulated without previous starter

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Outbreaks in United States 2009-2014 14

8

E. coli Shiga toxin + Salmonella spp. L. monocytogenes

54 11

Campylobacter spp.

Outbreaks in European Union 2010-2013 2

2

3

34

E. coli enterotoxigenic Salmonella spp.

23

L. monocytogenes Campylobacter spp. Brucella spp. Staphylococcus enterotoxins Bacillus toxins Calicivirus 2

2

3 Fig. 1. Number of outbreaks attributed to milk and cheese in the United States in 2009e2014 and to cheese in the European Union in 2010e2013. Adapted from Costard et al. (2017) and van Asselt et al. (2017).

inoculation, which results in pleasant mild taste but dangerously ~ ez, Bautista, & Nun ~ ez, 1985). Those high pH values (Chavarri, Nun fresh cheese types were traditionally consumed within a few days, but current requirements of large distributors and retailer chains for longer product shelf-life favour the development of psychrotrophic pathogens such as L. monocytogenes, which might contaminate the product during manufacture or storage (Evertndez-Herrero, 2018). Arriagada, Trujillo, Amador-Espejo, & Herna Finally, some cheese varieties, in particular those surface-ripened by moulds such as Brie and Camembert, show an increase in their outer pH values during aging, close to or above neutrality, which permits pathogen growth (Back, Langford, & Kroll, 1993). HPP is an effective tool in eliminating cheese-borne pathogens. Optimal process parameters and the best moment for HPP application may vary depending on the cheese variety and the confirmed or suspected pathogens in the product. Pathogens considered to develop rapidly in the curd during the first hours of cheese manufacture include some genera of Enterobacteriaceae and some species of Staphylococcus. The risk may arise in cheeses made from raw milk with a low population of indigenous LAB or in

pasteurised milk cheeses exposed to post-pasteurisation contamination, particularly if manufactured without starter culture or in the case of bacteriophage attack to the starter culture. Pressure levels of 500 MPa have generally been proven as capable of eliminating most Gram-negative pathogens, even though pressure levels as low as 300 MPa may be lethal for some bacterial species. Counts of E. coli O157:H7 strain ATCC 43894 in model semi-hard cheeses (Fig. 2) declined by 1.3 log units after HPP at 300 MPa for 10 min and by 3.7 log units after HPP at 500 MPa for 5 min with respect to control cheese when cheeses were HPP-treated on day 2, and by 3.8 and 5.8 log units, respectively, when HPP-treated on day 50, all treatments at an initial temperature of 10  C (Rodríguez, s, Nun ~ ez, Gaya, & Medina, 2005). Counts of E. coli O157:H7 Arque strain CETC 5947 in model cheeses decreased after HPP by 2.0 units at 300 MPa and by 6.1 log units at 500 MPa, both treatments for 10 min at an initial temperature of 20  C, in cheeses made with starter culture, and by 2.9 and 6.0 log units, respectively, in cheese made without starter culture (De Lamo-Castellví et al., 2006). The high resistance of E. coli O157:H7 to pressure was confirmed in a kinetics study in which D reduction times of 4.4 and 14.5 min were

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Bacterial counts (log cfu g-1)

8 7 6 5 4 3

Control 300 MPa day 2 500 MPa day 2 300 MPa day 50 500 MPa day 50

2 1 0

EC day 3 EC day 60 SA day 3

SA day 60 LM day 3 LM day 60

Fig. 2. Counts (log cfu g1) of Escherichia coli O157:H7 ATCC 43894 (EC), Staphylococcus aureus CECT 976 (SA) and Listeria monocytogenes Scott A (LM) in 3-day or 60-day model s et al. (2005a,b) semi-hard cheese, non-HPP-treated (control) or HPP-treated at 300 MPa for 10 min or 500 MPa for 5 min on days 2 or 50 after manufacture. Adapted from Arque and Rodríguez et al. (2005).

respectively obtained for E. coli K12 and E. coli O157:H7 inoculated in raw milk cheese that was treated at 300 MPa and 25  C (Shao, Ramaswamy, & Zhu, 2007). In a similar study, counts of two Salmonella enterica strains in model cheeses made with starter culture decreased after HPP by 4.2e4.3 log units at 300 MPa and by 4.3e5.0 log units at 400 MPa, while their counts in model cheeses made without starter culture declined by 2.0e2.7 log units at 300 MPa and by 3.5e4.8 log units at 400 MPa, all treatments for 10 min at an initial temperature of 20  C (De Lamo-Castellví et al., 2007). The decline in counts of three Yersinia enterocolitica strains separately inoculated in model cheeses ranged from 1.9 to 3.5 log units after HPP at 300 MPa, and from 3.4 to 5.0 log units after HPP at 500 MPa, all treatments for 10 min at an initial temperature of 20  C (De Lamo-Castellví et al., 2005). The highest sensitivity to high pressure among Gram-negative pathogens that might contaminate milk or cheese was found for Aeromonas hydrophila, the counts of which declined in milk by 2.8 log units after HPP at 250 MPa and by 9.0 log units after HPP at 350 MPa, both treatments for 10 min at an initial temperature of ~es-Carvalho et al., 2012). In contrast with the high 25  C (Dura sensitivity of most Gram-negative pathogens to HPP, heat-stable E. coli enterotoxin STa withstood treatment at 800 MPa for 30 min at 5  C without loss of reactivity, as determined by a competitive enzyme immunoassay (Margosch et al., 2005). S. aureus has been shown to be generally more resistant to HPP than Gram-negative pathogens. Counts of S. aureus in model Cheddar cheese decreased by 1.2, 3.0 and 4.3 log units, respectively, after HPP at 300, 400 and 500 MPa, all treatments for 20 min at an initial temperature of 20  C, food isolates being more resistant to pressure than collection strains. In model semi-hard cheeses (Fig. 2), S. aureus counts declined by 0.5 log units after HPP at 300 MPa for 10 min and by 2.4 log units after HPP at 500 MPa for 5 min with relative to control cheese when cheeses were HPPtreated on day 2 after manufacture, and by 1.1 and 2.4 log units, respectively, when they were HPP-treated on day 50 after manufacture, all treatments carried out at an initial temperature of 10  C s et al., 2005a). (Arque Counts of coagulase-positive staphylococci in commercial La Serena cheese, made from raw ewe milk and treated on day 2 after manufacture, declined by 0.5 and 1.5 log units, respectively, after

HPP at 300 and 400 MPa for 10 min at an initial temperature of s et al., 2006). Counts of S. aureus strains CECT 4013 and 10  C (Arque ATCC 13565 in model cheeses HPP-treated for 10 min at an initial temperature of 5  C on day 1 after manufacture decreased on average by 0.3, 0.8 and 1.6 log units after treatment at 300, 400 and 500 MPa, respectively, while decreases of 0.6, 1.4 and 2.6 log units, respectively, were achieved by HPP at an initial temperature of  pez-Pedemonte, Roig-Sague s, De Lamo, Gervilla, & 20  C (Lo Guamis, 2007a). In that study, staphylococcal enterotoxins were detected in cheeses inoculated with S. aureus ATCC 13565 and sampled before HPP treatments, after HPP treatments on day 1, and after 30 days of storage at 8  C. Staphylococcal enterotoxin C had been shown to resist even HPP treatment at 800 MPa for 30 min at 20  C, with no loss of reactivity in an enzyme immunoassay (Margosch et al., 2005). L. monocytogenes frequently contaminates cheeses, at rates reported to range from 0.2% in cheese from pasteurised cow milk to 13.6% in cheese from raw ewe milk (Almeida et al., 2013). L. monocytogenes strain F13 inoculated in raw goat milk did not grow during the manufacture and ripening of Sainte Maure de Touraine cheese because of the acid pH values (4.4e4.7); its counts decreased by 5.7 and >6 log units when the cheeses were HPPtreated on day 2 after manufacture at 200 MPa for 20 min or e, 1998). 350 MPa for 5 min, respectively (Gallot-Lavalle However, L. monocytogenes may grow during the manufacture and early ripening of most cheeses as rapidly as other pathogens. Counts of L. monocytogenes Scott A respectively increased by 1.4 and 2.2 log units from milk to cheese on days 1 and 3 after s, Rodríguez, Gaya, Medina, & Nun ~ ez, 2005b), manufacture (Arque while E. coli O157:H7 ATCC 43894 counts increased by 2.4 and 1.9 log units (Rodríguez et al., 2005), and S. aureus CECT 976 counts s et al., 2005a), all data increased by 1.8 and 1.6 log units (Arque obtained in model semi-hard cheeses manufactured following the same protocol. In those studies, L. monocytogenes Scott A showed less resistance to HPP than E. coli O157:H7 ATCC 43894 and S. aureus CECT 976 (Fig. 2), with decreases of 0.9 log units after HPP at 300 MPa for 10 min and 5.0 log units after HPP at 500 MPa for 5 min with respect to control cheese when treatments were performed on day 2 after manufacture, and decreases of 6.2 and >6.2 log units, s et al., respectively, for treatments performed on day 50 (Arque 2005b).

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Counts of a cocktail of seven L. monocytogenes strains inoculated onto Gorgonzola cheese rinds decreased by 0.1, 0.5 and 1.2 log units after HPP at 500 MPa for 5, 10 and 15 min while the respective decreases at 600 MPa were 1.7, 2.4 and 3.3 log units, all treatments at an initial temperature of 10  C (Carminati, Gatti, Bonvini, Neviani, & Mucchetti, 2004). Different resistance to HPP in model cheeses was recorded for L. monocytogenes strains NCTC 11994 and Scott A, which counts decreased by 2.9 and 1.5 log units, respectively, at 400 MPa and by 5.1 and 5.7 log units, respectively, at 500 MPa, after treatment for pez-Pedemonte, Roig10 min at an initial temperature of 20  C (Lo s, De Lamo, Herna ndez-Herrero, & Guamis, 2007b). Sague In starter-free Queso Fresco inoculated with a cocktail of five L. monocytogenes strains, HPP treatment at 200 MPa for 20 min at an initial temperature of 20  C had no significant effect on L. monocytogenes counts whereas its counts declined by 2 log units at 400 MPa and by more than 4 log units at 600 MPa (Tomasula et al., 2014). In starter-free fresh cheese, 7.1 and 7.7 log unit reductions of L. monocytogenes CECT 4031 counts were achieved after HPP at 500 and 600 MPa for 5 min at 6  C while the respective reductions of L. monocytogenes Scott A counts were only 2.0 and 4.3 log units (Evert-Arriagada et al., 2018). When 60-day-old Ibores cheese made from raw goat milk naturally contaminated with Listeria spp. was HPP-treated at 400 or 600 MPa for 7 min, at an initial temperature of 10  C, the respective Listeria counts were 3.3, 2.7 and 1.8 log cfu g1 in control, 400 MPa and 600 MPa cheeses immediately after treatment and 1.4, 0.8 and 0.4 log cfu g1 after 30 days of further storage (Delgado, Delgado, Gonz alez-Crespo, Cava, & Ramírez, 2013). The physicochemical characteristics of cheese influence the resistance of L. monocytogenes to HPP treatments. Thus, counts of L. monocytogenes Scott A declined by 5.4 log units in fresh cheese (aw ¼ 0.983; 1.54% NaCl) and by only 0.4 log units in ripe cheese (aw ¼ 0.922; 3.67% NaCl) after treatment at 400 MPa for 9 min at 12  C. In the same study, galactose showed a higher baroprotective effect on L. monocytogenes Scott A when added to cheese slurry than lactose or glucose (Morales et al., 2006). Bacillus cereus is a psychrotrophic spore-forming pathogen that may contaminate and grow on cheese, particularly at the pH values close to neutrality of fresh starter-free cheeses. HPP treatment of fresh goat milk cheese at 400 MPa for 15 min at 30  C had no significant effect on counts of inoculated B. cereus ATCC 9139 spores  pez-Pedemonte, Roig-Xague s, Trujillo, Capellas, & Guamis, (Lo 2003). When skim milk inoculated with B. cereus ATCC 9139 spores was HPP-treated at 600 MPa for 20 min at different temperatures, reductions ranged from 1.0 log units at 38  C to 4.0 log units at 70  C (Evelyn & Silva, 2015). As high processing temperatures cannot be applied to cheese without altering its properties, pre-treatment of cheese at 60 MPa for 210 min at 30  C to induce the germination of B. cereus spores and increase lethality in a further HPP treatment at higher pressure pez-Pedemonte, Roig-Sague s, Trujillo, levels has been suggested (Lo Capellas, & Guamis, 2003). However, lengthy procedures seem unpractical at the industry level. Enterotoxins of B. cereus are at least as pressure resistant as spores. They resisted HPP treatment at 800 MPa for 30 min at 20  C without any loss of activity, as estimated by enzyme immunoassay reactivity and cytotoxicity on Vero cells (Margosch et al., 2005). It has been proven in the above studies that HPP is a reliable tool for the elimination of pathogens potentially present in cheese, although the inactivation of spore-forming bacteria may require additional measures. 2.1.2. Hindering biogenic amine formation Biogenic amines (BAs), low molecular weight compounds with biological activity, consist in an aliphatic, aromatic or heterocyclic

5

structure to which one, two or more amino groups are attached, depending on whether the biogenic amine is a monoamine, a diamine or a polyamine. The main BAs in cheese are tyramine and histamine, monoamines, which are mostly formed by decarboxylase-positive strains belonging to Enterococcus spp. and Lactobacillus spp. under conditions favourable for enzyme activity on the free amino acids (FAAs) generated through the hydrolysis of milk proteins (Loizzo et al., 2013). Different HPP treatments have been applied to cheeses made from raw and pasteurised milk to reduce their BA contents. Treatment of cheese made from pasteurised goat milk at 400 MPa for 5 min at 14  C lowered tyramine content from 10.3 mg kg1 dry matter (DM) in control cheese to 1.1 mg kg1 DM in HPP cheese on day 28 of ripening, although the spermidine content increased from 14.7 mg kg1 DM in control cheese to 26.4 mg kg1 DM in HPP cheese (Novella-Rodríguez, Vecianas, Saldo, & Vidal-Carou, 2002). The authors explained the Nogue reduced tyramine content of HPP-treated cheese by its low counts of non-starter lactic acid bacteria (NSLAB). HPP treatment of Casar cheese made from raw ewe milk at 400 or 600 MPa for 5 min on days 21 or 35 after manufacture (Calzada, del  n, Gaya, & Nun ~ ez, 2013a) reduced total BA content on day Olmo, Pico 60, from 1089 mg kg1 DM in control cheese to 728e794 mg kg1 DM in 400 MPa cheeses and 377e656 mg kg1 DM in 600 MPa cheeses (Fig. 3). The authors associated the lower BA content of HPP cheeses with the reduced counts of enterococci and lactobacilli in HPP-treated cheeses, with the 86.0e99.9% decrease in decarboxylase activity on day 60 caused by HPP and, in the case of 600 MPa cheeses, with the lower concentrations of total FAAs. Likewise, when raw milk Arzúa-Ulloa cheese was HPP-treated at 400 or 600 MPa for 5 min on days 14 or 21 after manufacture ~ ez, 2015a), lower tyramine (Calzada, del Olmo, Picon, Gaya, & Nun contents were found on day 240 after manufacture, with 372 mg kg1 DM in control cheese, 170e176 mg kg1 DM in 400 MPa cheeses and less than 1 mg kg1 DM in 600 MPa cheeses. Putrescine behaved similarly to tyramine, while cadaverine was less affected by HPP treatments. HPP-treated cheeses showed lower counts of enterococci and lactobacilli, lower tyrosine decarboxylase activity, and lower total FAA concentrations than control cheese from day 120 onwards. In blue-veined cheese made from pasteurised ewe milk and HPP-treated at 400 or 600 MPa for 5 min on days 21, 42 or 63 after manufacture, tyramine contents on day 360 decreased from 52.2 mg kg1 DM in control cheese to 20.9e32.0 mg kg1 DM in 400 MPa cheeses and 27.2e33.4 mg kg1 DM in 600 MPa cheeses, while no significant decrease in total BA content occurred, since the formation of tryptamine, phenylethylamine and putrescine was not as affected by HPP as that of tyramine (Calzada, Del Olmo, Picon, ~ ez, 2013b). Gaya, & Nun In Brie cheese made from pasteurised milk and HPP-treated at 400 or 600 MPa for 5 min on days 14 or 21 after manufacture, BA were not detected in control cheese or in cheeses HPP-treated on day 14, but cadaverine was found in cheeses HPP-treated on day 21 at levels that increased from 19.0 mg kg1 DM on day 30e67.2 mg kg1 DM on day 60 (Calzada, del Olmo, Picon, Gaya, & ~ ez, 2014a). Nun In cheeses made from raw goat milk and treated at 400 MPa for ndez-Herrero, & Roig10 min at 2  C (Espinosa-Pesqueira, Herna s, 2018), contents of tyramine, histamine and putrescine on Xague day 60 were lowered from 491.9, 15.4 and 476.4 mg kg1 DM, respectively, in control cheese to 28.9, 4.9 and 79.8 mg kg1 DM, respectively, in HPP-treated cheese. In the same study, when cheese made from raw ewe milk was treated at 400 MPa for 10 min at 2  C, contents of tyramine, histamine, putrescine and cadaverine on day 60 were reduced from 277.3, 91.0, 74.9 and 105.9 mg kg1 DM in

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6

4000

Biogenic amines (mg kg-1 DM)

3500 3000 2500 2000 1500 1000 500 0 day 60 Control 1

400 MPa day 21

day 120

day 180

600 MPa day 21  C)

day 240

400 MPa day 35

600 MPa day 35

 C)

Fig. 3. Total biogenic amines (mg kg dry matter) during ripening (60 days at 8 and storage (further 180 days at 4 of Torta del Casar cheese made from ewe raw milk, nonHPP-treated (control) or HPP-treated at 400 MPa on day 21, 600 MPa on day 21, 400 MPa on day 35 and 600 MPa on day 35. Adapted from Calzada et al. (2013a).

control cheese, respectively, to 32.7, 7.1, 5.2 and 28.5 mg kg1 DM in cheeses HPP-treated on day 1. The marked reduction in the levels of biogenic amines achieved by HPP, mostly by eliminating NSLAB with amino acid decarboxylating activity, as reported in the above studies, contributes to assure healthier properties of certain cheeses. 2.1.3. Stabilising unstable cheeses Low pH values and low aw values are by far the key hurdles for controlling microbial growth in cheese. These hurdles are generally in place for hard and semi-hard cheeses, which have undergone lactic fermentation by starter cultures, have been dry- or brinesalted, and have lost a considerable proportion of moisture during ripening. In contrast, fresh cheeses have high moisture content and low salt concentration, which result in high aw values, and LAB are not necessarily involved in their manufacture. Cheeses made for consumption as fresh products are therefore prone to alterations because of their particular physicochemical characteristics. The manufacturing process of fresh lactic curd cheeses such as cottage and quark relies on the acid coagulation of milk mediated by the metabolic activity of LAB, which results in the isoelectric precipitation of caseins. In the direct-acid or direct-set procedure, LAB inoculation is replaced by acid addition to milk. Those cheeses varieties exhibit low pH values, ranging from 5.0 to 4.6, which impede growth of spoilage bacteria. In contrast, the manufacture of  depends fresh rennet curd cheeses such as Burgos and Mato exclusively on the enzymatic coagulation of milk by rennet, without inoculation of starter cultures, on the aim of achieving their mild non-acidic taste associated with high pH values. Those starter-free cheeses, with pH values close to 6.5, lack the main hurdle for controlling bacterial growth. Fresh lactic curd cheeses are susceptible only to growth of contaminating yeasts and moulds capable of developing at the low pH value of the product. Although antifungal additives such as sorbic acid or potassium sorbate may be used for their control, HPP looks a more attractive procedure when aiming to preservative-free dairy products; however, there is little information on the subject. Commercial fresh lactic curd cheese was HPP-treated at 300e600 MPa to extend its shelf-life (Daryaei, Coventry, Versteeg,

& Sherkat, 2008). The pH value of control cheese was 4.33 on day 0 and 4.25e4.30 through storage for 56 days at 4  C, and yeast counts were close to 2 log cfu g1 on day 0, almost 4 log cfu g1 on day 14, and 6 log cfu g1 on day 56. In contrast, cheeses HPP-treated at 300, 400 and 600 MPa for 5 min had yeast counts close to 4, 3 and 2 log cfu g1, respectively, on day 56, and their pH values did not differ from those of control cheese (Daryaei et al., 2008). The sensory properties of the fresh lactic curd cheeses were not affected by HPP treatments, although it must be noted that herbs and flavourings had been added as ingredients (Daryaei, Coventry, Versteeg, & Sherkat, 2006). Fresh rennet curd cheeses are clear candidates for shelf-life extension. Their physicochemical characteristics, in particular their high pH values, may result in unacceptable high counts of contaminating bacteria such as staphylococci and coliforms in  cheese is a fresh commercial cheeses (Chavarri et al., 1985). Mato rennet curd cheese for which DM content of 33.0e45.3%, pH values of 5.0e6.7, and aw values of 0.981e0.999 were reported in commercial samples (Capellas, Mor-Mur, Sendra, Pla, & Guamis, 1996).  cheese at 450 MPa for 5 min lowered aerHPP-treatment of Mato obic mesophilic counts by 1.8 log units at 10  C and 2.7 log units at 25  C, while HPP at 500 MPa for 10 min lowered counts by 2.5 log units at 10  C and 3.0 log units at 25  C, with no bacterial growth in HPP-treated cheeses during refrigerated storage for 60 days  cheese was treated at 500 MPa (Capellas et al., 1996). When Mato its composition did not vary and no structural differences between cheeses were observed by scanning electron microscopy, but HPPtreated cheeses lost more whey than control cheese and showed higher values of apparent fracture stress and b* colour parameter (Capellas, Mor-Mur, Sendra, & Guamis, 2001). In fresh rennet-curd cheese treated at 50e291 MPa, pH value on day 1, hardness and b* colour parameter increased as the pressure level increased while lipid oxidation decreased (Okpala, Piggott, & Schaschke, 2010). HPP treatment of starter-free fresh cheese at 300 and 400 MPa for 5 min at 6  C prolonged its shelf-life to 14 and 21 days, respectively, while control cheese had a shelf-life of only 7 days, considering 6 log cfu g1 aerobic mesophiles as the threshold for consumption. Firmer texture and more yellowish colour were found for HPP-treated cheeses than for control cheese (Evert-

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Arriagada, Hern andez-Herrero, Juan, Guamis, & Trujillo, 2012). In a commercial scale experiment, treatment at 500 MPa for 5 min at 16  C achieved a shelf-life of 18e20 days for starter-free fresh cheese while that of control cheese was 8e10 days (Fig. 4), considering a spoilage threshold of 6 log cfu g1 (Evert-Arriagada, Hern andez-Herrero, Guamis, & Trujillo, 2014). When the volatile compounds of the latter cheeses were determined after storage for 7 days at 4  C, the levels of alcohols, acids and ketones in cheese treated at 500 MPa were 15.7%, 66.2% and 95.4% of the respective levels in control cheese, but there were no significant differences in ndezthe levels of aldehydes or lactones (Evert-Arriagada, Herna n, Juan, & Trujillo, 2013). Herrero, Gallardo-Chaco Starter-free Queso Fresco only suffered slight compositional changes in moisture and protein content after treatment at 200, 400 or 600 MPa for 5e20 min, with previous warming of cheese to 20 or 40  C, but a consistent decrease in a* colour parameter was recorded as the pressure level was increased (Van Hekken, Tunick, Farkye, & Tomasula, 2013). HPP treatments caused microstructural changes, with the cheese matrix becoming slightly tighter and the micelles losing their individual appearance and fusing into thicker strands, although cheese textural characteristics were not altered by HPP at an initial temperature of 20  C. As reported in the above studies, the shelf life of fresh cheeses can be considerably extended by means of HPP treatments at mild temperatures, which control microbial growth without negative effects on cheese characteristics. 2.2. Speeding up and braking 2.2.1. HPP as the pedal The microbial metabolism of lactose and citrate, together with breakdown of proteins and lipids, are primary biochemical events occurring during cheese manufacture and early ripening. Subsequently, secondary biochemical events including hydrolysis of peptides, catabolism of FAAs and free fatty acids (FFAs), and metabolism of lactate give rise to the formation of flavour and aroma compounds during mid and late ripening of cheese (Collins, McSweeney, & Wilkinson, 2003; McSweeney & Sousa, 2000; Yvon & Rijnen, 2001). All these biochemical events continue during refrigerated storage of already ripe cheese at dairies, retailers and homes, and may result in unwanted over-ripening. Ammonia, amines, alcohols, aldehydes, carboxylic acids and thiol compounds formed through FAA catabolism, and FFA and methylketones derived from lipids, are among the main causative agents for

7

off-flavour defects associated to over-ripening when they exceed a ~ ez, 2014b). certain threshold (Calzada, del Olmo, Picon, Gaya, & Nun HPP at high pressure levels has been shown to reduce the activity of most cheese-related enzymes, which may come from milk, microorganisms or coagulants. However, activation of some of those enzymes may occur under milder treatment conditions. It must be taken into account that the baroresistance of enzymes in cheese may differ from that of enzymes in milk or buffer. Activity of Lactococcus lactis cell envelope proteinase in cell-free extracts suspended in buffer increased at 100 MPa, did not vary at 200 MPA, decreased at 300 MPa and was lost at 400e800 MPa (Malone, Wick, Shellhammer, & Courtney, 2003). In the same study, activity of Lactococcus lactis X-prolyl-dipeptidyl aminopeptidase and aminopeptidase N did not vary at pressures up to 300 MPa and was lost at higher levels, activity of aminopeptidase C increased up to 700 MPa and only declined at 800 MPa, and activity of aminopeptidase A was unaffected up to 800 MPa. Activity of Streptococcus thermophilus PepX aminopeptidase increased up to 24.8% with mild treatments of 100e200 MPa at 20  C or 100 MPa at 30  C, undergoing slight changes in its secondary structure (Giannoglou et al., 2018). However, higher temperatures or higher pressure levels inactivated the enzyme, which lost 97.8% activity after 10 min at 300 MPa and 30  C. Glycolytic enzymes such as Lactococcus lactis subsp. lactis phospho-b-galactosidase, S. thermophilus b-galactosidase and Lactobacillus acidophilus b-galactosidase were affected by HPP treatments of cells in buffer for 5 min at 22  C, respectively losing 11.0%, 20.6% and 19.3% of their activity at 300 MPa and 94.0%, 97.5% and 26.6% at 600 MPa (Daryaei, Coventry, Versteeg, & Sherkat, 2010). In the same study, acid production by resting cells of Lactococcus lactis subsp. lactis in the presence of 5% lactose decreased 16% and 93% after treatment at 300 and 600 MPa, respectively, when determined after 3 h of incubation but gradually recovered along 40 h of incubation. Milk plasmin retained 97.2%, 90.4% and 88.9% activity, respectively, in 14-day-old Cheddar cheese HPP-treated at 400, 600 or 800 MPa for 15 min at 20  C (Fig. 5) while chymosin only retained 96.8%, 6.7% and 3.5% activity, respectively (Huppertz, Fox, & Kelly, 2004). In 1-day-old cheese made from pasteurised ewe milk and treated at 400 or 500 MPa for 10 min at 12  C (Fig. 5), milk plasmin retained 95.7% and 79.3% activity, respectively, and chymosin 65.9% and 20.6% activity (Juan, Ferragut, Buffa, Guamis, & Trujillo, 2007a). In the latter study, aminopeptidase from the starter culture lost 10.2%, 57.1%, 38.8% and 28.6% activity after treatment of 1-day-old

Microbial counts (log cgu g-1)

9 8 7 6 5 4 3 2 1 0 TOT TOT LAC LAC PSE PSE ENT ENT SPO SPO FUN FUN day 7 day 21 day 7 day 21 day 7 day 21 day 7 day 21 day 7 day 21 day 7 day 21 500 MPa

Control

Fig. 4. Counts (log cfu g1) of total aerobic mesophiles (TOT), Lactococcus (LAC), Pseudomonas (PSE), Enterobacteriaceae (ENT), spores (SPO) and moulds þ yeasts (FUN) in control and HPP-treated fresh cheese after 7 and 21 days at 4  C. Adapted from Evert-Arriagada et al. (2013, 2014).

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~ ez, 2013c). In the case of Penicillium camemberti Gaya, & Nun esterase, its activity increased by 44.1% and 26.9% (Fig. 5), respectively, after treatment of 14 day-old pasteurised milk Brie cheese at 400 or 600 MPa for 5 min at 10  C, a result which was explained by the authors as due to the enhanced release of lipolytic enzymes from dead or injured mould cells (Calzada, del Olmo, Picon, & ~ ez, 2014d). Nun Milk constituents are affected by HPP treatments. In the case of milk proteins, the major changes are the disruption of casein micelle structure and the denaturation of a-lactalbumin and, more extensively, of b-lactoglobulin (Huppertz, Kelly, & Fox, 2002). The milk fat globule size did not vary significantly with HPP treatments at 100e600 MPa for 30 min at 20  C, although the volume weighted mean diameter of fat globules increased after 30 min at 600 MPa (Huppertz, Fox, & Kelly, 2003). The authors reported an increase in milk protein associated with fat globules after HPP treatments, with a maximum at 200 MPa. The effects of HPP treatments on the activity of enzymes and the stability of milk constituents, which influence enzyme-driven biochemical events and conformational changes in the cheese protein matrix, open the possibility of different HPP-based strategies. In this respect, applications of HPP oriented to mastering cheese maturation would include both the acceleration and the arrest of the ripening process.

cheese at 200, 300, 400 or 500 MPa, respectively, if determined on day 1 (Fig. 5) but showed increases of 58.2%, 102.9%, 101.7% and 14.6%, respectively, if determined on day 30 (Juan et al., 2007a). nico cheese at After treatment of 15-day-old pasteurised milk Hispa 400 MPa for 5 min at 10  C, aminopeptidase retained 56.4% and 53.0% activity with Lys-p-nitroanilide or Leu-p-nitroanilide as the  ~ ez, 2006b) respective substrates (Avila, Garde, Gaya, Medina, & Nun while starter culture esterase retained 94.2% activity (Fig. 5) after  cheese treatment under the same conditions (Avila, Calzada, Garde, ~ ez, 2007). & Nun HPP treatment causes death and lysis of lactococci and increases the permeability of the cell membrane, releasing intracellular enzymes to the outer medium, some strains of lactococci being more resistant than others to HPP-induced lysis (Malone, Shellhammer, & Courtney, 2002; O'Reilly, O'Connor, Murphy, Kelly, & Beresford, 2002). On the other hand, HPP inactivates aminopeptidases although enzymes are more protected against HPP-induced damage while inside the cell than once they have been released to the cheese matrix (Calzada et al., 2015a). Determination of the residual activity of microbial enzymes in HPP-treated cheese jointly evaluates the release of intracellular enzymes by HPP, which gradually increases from 200 to 600 MPa, and the inactivation of the partially or totally released enzyme by HPP, which increases more sharply from 400 to 600 MPa. Depending on whether release or inactivation predominates, apparent increases or decreases in enzymatic activity will be observed in cheese for intracellular microbial en zymes (Avila et al., 2006b). If the determination of enzymatic activity is carried out some days after the HPP treatment of cheese, it is feasible that diffusion of intracellular enzymes through the damaged cell envelopes occurs in the meantime, and higher activity values will presumably be obtained. Milk lipase retained 69.9% and 50.9% activity (Fig. 5), respectively, after treatment of 14 day-old raw milk Arzúa-Ulloa cheese at 400 or 600 MPa for 5 min at 10  C (Calzada, del Olmo, Picon, & ~ ez, 2015b). Regarding fungal enzymes, Penicillium roqueforti Nun esterase retained 75.5% and 27.9% activity (Fig. 5), respectively, after treatment of 21 day-old pasteurised ewe milk blue-veined cheese at 400 or 600 MPa for 5 min at 10  C (Calzada, Del Olmo, Picon,

2.2.2. Accelerating ripening After the reported beneficial effect of HPP on Cheddar cheese ripening (Yokohama et al., 1992), HPP treatments with shorter holding times have been applied to different cheese types with the objective of accelerating their ripening process. High pressure can influence cheese proteolysis through conformational changes in proteins, activation or inactivation of proteinases, and inhibition or acceleration of microbial growth and metabolism (Kolakowski, Reps, & Babuchowski, 1998). These authors investigated the effect of HPP at pressures ranging from 200 to 1000 MPa and holding times of 10 and 15 min on samples of Gouda and Camembert cheeses. Treatment at 400, 600 and 800 MPa for 10 min lowered microbial counts in 14 day-old Gouda samples by approximately 2,

Milk plasmin in Cheddar cheese Milk plasmin in ewe milk cheese Milk lipase in semi-hard cheese Chymosin in Cheddar cheese Chymosin in ewe milk cheese Starter aminopep dase in ewe milk cheese Starter esterase in Hispánico cheese P. roquefor esterase in blue-veined cheese P. camember esterase in Brie cheese

0

400 MPa

20

500 MPa

40

60 80 100 Residual ac vity (%)

600 MPa

120

140

160

800 MPa

Fig. 5. Baroresistance (residual activity, %) of cheese-related enzymes after HPP treatment of different cheeses at pressure levels in the range 400e800 MPa. Adapted from Huppertz  et al. (2004), Avila et al. (2007), Juan et al. (2007a) and Calzada et al. (2013c, 2014d, 2015b).

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4 and 5 log units, and counts in 10 day-old Camembert samples by approximately 1, 4 and 5 log units. Increased proteolysis, associated with a higher proteolytic activity in cheese, was recorded for Camembert samples, particularly after treatment at 50 MPa for 4 h, but not for Gouda samples. According to the authors, HPP-treated Gouda samples had a more elastic texture and superior sensory properties than control samples, while HPP-treated Camembert samples showed whey syneresis and sensory properties similar to those of control samples. Gouda cheese samples treated on day 3 after manufacture at 50e400 MPa for 20e100 min did not show significant differences in pH 4.6-soluble nitrogen, phosphotungstic acid-soluble nitrogen, FAAs or electrophoretic patterns with respect to control samples, although HPP influenced cheese pH, with higher values in 225 or 400 MPa samples than in control or 50 MPa samples (Messens, Estepar-Garcia, Dewettinck, & Huyghebaert, 1999). When the volatile compounds of HPP-treated and control Gouda cheese samples were determined, the main differences were found for 3hydroxybutanone, present at lower levels in 50, 225 and 400 MPa samples than in control samples, and butyric acid, found at lower levels in 225 and 400 MPa samples than in control samples (Butz, ndez, Koller, Messens, & Tauscher, 2000). In a study on Ferna Edam cheeses HPP-treated at different stages of ripening at 200 or 400 MPa for 30 min at room temperature, their pH values were approximately 0.1 units higher than in control cheese, while pH 4.6-soluble nitrogen and amino acid nitrogen were lower in HPPtreated cheeses than in control cheese (Iwanczak & Wisniewska, 2005). Garrotxa cheeses manufactured from pasteurised goat milk were treated at 400 MPa for 5 min at 14  C (Saldo, Sendra, & Guamis, 2000). HPP-treated cheeses showed higher pH values than control cheese, 0.2 units higher on day 14 and 0.4 units higher on day 28, and enhanced proteolysis, with levels of non-casein nitrogen, non-protein nitrogen and total FAAs approximately 40%, 30% and 60% higher in HPP-treated cheese than in control cheese on day 28. The authors suggested that the higher pH value of HPPtreated cheese was more favourable for the activity of starter peptidases and might have enhanced proteolysis (Saldo et al., 2000). Miniature Cheddar cheeses separately made using four Lactococcus lactis strains as starter cultures were HPP-treated at

9

100e400 MPa for 20 min at 25  C on day 1 after manufacture (O'Reilly et al., 2002). HPP brought about reductions in Lactococcus lactis counts of 1e2 log units at 300 MPa and 2e5 log units at 400 MPa, depending on the strain. Higher b-casein (f106e149) levels were observed in cheeses made with the four strains when treated at 400 MPa than in the respective control cheeses on day 30 while there was no apparent increase in the levels of pH 4.6-soluble nitrogen in HPP-treated cheeses. FAA concentration in cheese made with Lactococcus lactis 223 and treated at 400 MPa was 41.4% higher on day 30 than in the respective control cheese while FAA levels were 14.7%e22.5% lower in cheeses made with the other three Lactococcus lactis strains and treated at 400 MPa than in the respective control cheeses (O'Reilly et al., 2002) (Fig. 6). Cheeses made from pasteurised ewe milk were treated at 200, 300, 400 and 500 MPa for 10 min at 12  C on days 1 and 15 after manufacture (Juan, Ferragut, Guamis, Buffa, & Trujillo, 2004). The highest FAA levels on day 60 were those of cheeses treated at 300 MPa on day 1 while treatments at 500 MPa lowered the FAA levels. The authors attributed the enhanced proteolysis to cell lysis and enzyme release, although admitting that pressure-induced conformational changes of the protein cheese matrix could also have played a role (Juan et al., 2004). Degradation of aS1-casein during ripening of those cheeses was enhanced at 200e400 MPa and retarded at 500 MPa when cheeses were HPP-treated on day 1, with a minimum of 61.2% residual aS1-casein in 200 MPa cheese, a maximum of 99.1% in 500 MPa cheese and 66.0% in control cheese on day 15, and enhanced at all the pressure levels when cheeses were HPP-treated on day 15 (Juan et al., 2007a). Residual aS2-casein showed a similar pattern to that of aS1-casein. An opposite effect was recorded for b-casein, which on day 15 had declined to 99.8% in control cheese, 97.1% in 200 MPa cheese and 78.8% in 500 MPa cheese for treatments on day 1, and underwent only slight decreases afterwards (Juan et al., 2007a). Regarding the lipolysis of those ewe milk cheeses, a significant increase in the level of FFA was found only for cheese treated on day 1 at 300 MPa, which was 95.6% higher than in control cheese immediately after HPP and 17.2% higher on day 15 (Juan, Ferragut, Buffa, Guamis, & Trujillo, 2007b). In cheeses made from pasteurised ewe milk and treated at 300 MPa for 10 min on days 1 or 15 after manufacture and ripened for 90 days, b-casein hydrolysis was enhanced at all stages of

100 90

Residual casein (%)

80

70 60 50 40 30

% on total N

20 10 0 αs1-casein day 15

αs1-casein day 60

Control

β-casein day 15

200 MPa

β-casein day 60

300 MPa

Water-soluble N Water-soluble N day 15 day 60

400 MPa

500 MPa

Fig. 6. Residual caseins (% on initial caseins) and water-soluble nitrogen (% on total nitrogen) during ripening of ewe milk cheese non-HPP-treated (control) and HPP-treated at 200, 300, 400 and 500 MPa for 10 min on day 1 after manufacture. Adapted from Juan et al. (2004, 2007a).

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ripening in cheeses treated on days 1 or 15 and FAA formation only in cheeses treated on day 1 (Juan, Ferragut, Guamis, & Trujillo, 2008). Levels of FFAs were lower in cheeses treated on day 1 than in cheeses treated on day 15 or in control cheese. nico cheeses, made from a mixture of pasteurised cow and Hispa ewe milk using Lactococcus lactis subsp. lactis and S. thermophilus as starter cultures, were treated on day 15 at 400 MPa for 5 min at  10  C and further ripened until day 50 (Avila et al., 2006b). S. thermophilus counts were 0.9 log units lower on day 15 and 1.4 log units lower on day 50 in HPP-treated cheese than in control cheese while Lactococcus lactis subsp. lactis counts were 0.1 and 0.5 log units lower, respectively. A faster proteolysis of a- and b-casein was recorded in HPP-treated cheese, with levels of hydrophobic peptides, hydrophilic peptides and FAAs on day 50 respectively 27.5%, 22.5% and 75.6% higher than in control cheese. The texture of HPP-treated cheese was less firm than that of control cheese, with lower values for breaking force, energy to breaking point and  elasticity on day 50 (Avila et al., 2006b). Short-chain, mediumchain and long-chain FFA were found at lower concentrations in nico cheese than in control cheese, which were HPP-treated Hispa associated with the lower esterase activity of the former cheese  nico cheese showed higher (Avila et al., 2007). HPP-treated Hispa levels of hexanal, 3-hydroxy-2-pentanone, 2-hydroxy-3-pentanone and hexane than control cheese and lower levels of 1-propanol and  ~ ez, butanoic acid (Avila, Garde, Fern andez-García, Medina, & Nun 2006a). Cheddar cheese was HPP-treated on day 1 after manufacture at 400 MPa for 10 min at room temperature and ripened at 8  C for 180 days (Rynne et al., 2008). Starter lactococci counts fell by almost 2 log units immediately after treatment and were 4 log units lower than in control cheese on day 90. Counts of NSLAB in HPPtreated cheese were approximately 1 log unit lower than in control cheese until day 90 and 0.5 log units lower on day 180. The pH of HPP-treated cheese reached during ripening values 0.10e0.15 units higher than in control cheese. Plasmin and chymosin activity was not significantly affected by HPP in spite of which aS1-casein breakdown was more intense in HPP-treated cheese from day 21 onwards with a slight increase of pH 4.6-soluble nitrogen, but not of FAA levels. The concentration of FFA increased during ripening without significant differences between HPP-treated and control cheeses. HPP treatment did not affect cheese firmness but increased fracture strain and fracture stress values with respect to control cheese (Rynne et al., 2008). Proteolysis of Reggianito cheese was accelerated by HPP treatment at 400 MPa for 5 or 10 min at 20  C (Costabel et al., 2016). Cheese treated at 400 MPa for 10 min showed higher plasmin activity than control cheese or cheeses treated at 100 MPa, similar residual coagulant activity, lower starter culture counts and higher levels of total FAAs, which were 1.89-fold higher than those of control cheese on day 45 and 1.24-fold higher on day 60. Sensory characteristics of the miniature (250 g) cheeses used in experiments were not evaluated. Cheeses made from raw ewe milk that were treated at 200, 300, 400 and 500 MPa for 10 min at 14  C on day 7 had similar pH and dry matter values than control cheese on day 60. Levels of FAAs were significantly higher in cheeses treated at 200, 300 or  400 MPa, in spite of their lower aminopeptidase activity (Avila,  mez-Torres, Delgado, Gaya, & Garde, 2017a). Regarding volaGo tile compounds, cheeses treated at 300, 400 or 500 MPa had lower levels of 2-butanone, 2-butanol, 2-propen-l-ol, 1-butanol and acetic acid than control cheese, cheeses treated at 400 or 500 MPa lower levels of 1-propanol, 2-pentanol, butyric acid and hexanoic acid, and those treated at 500 MPa lower levels of  ethanol, 3-methyl-l-butanol and 3-methyl-2-buten-1-ol (Avila et al., 2017a).

Enhanced primary and secondary proteolysis appears as the most visible effect of HPP treatments at mild pressure levels, within the range 200e400 MPa. Consequences on cheese sensory properties will be discussed later in this review. 2.2.3. Slowing down over-ripening The reported effects of high pressure levels on most cheese microorganisms and enzymes, which were partially or totally inactivated at 600 MPa, opened the possibility of using HPP treatments for retarding the biochemical events involved in cheese ripening. Commercial Cheddar cheeses were HPP-treated 30 or 120 days after manufacture, at 200e800 MPa for 5 min at 25  C (Wick, Nienaber, Anggraeni, Shellhammer, & Courtney, 2004). In cheeses treated on day 30, pressure levels of 200 or 300 MPa did not affect starter Lactococcus lactis counts, 400 MPa caused a decline of 4 log units with Lactococcus lactis recovering during ripening, and pressure levels of 500 and 800 MPa caused declines of 6 log units with no recovery of Lactococcus lactis. In cheeses treated on day 120, pressure levels of 500e800 MPa caused declines of 4e5 log units with no recovery of Lactococcus lactis. After HPP at 200 or 300 MPa, no differences in FAA concentration were recorded with respect to control cheese during further ripening, while in cheeses treated at higher pressures the FAA concentration was lower than in control cheese, independently of cheese age at treatment. Among the rheological characteristics of cheese treated on day 30, fracture stress suffered slight changes at all pressure levels, fracture strain increased at 400 MPa and higher levels, fracture work increased only at 800 MPa, and elasticity declined at 200e500 MPa but did not vary with respect to control at 800 MPa. According to the authors, the textural changes taking place during ripening might have been arrested by the most severe treatments (Wick et al., 2004). La Serena cheese made from raw ewe milk was HPP-treated on days 2 or 50 after manufacture, at 300 or 400 MPa for 10 min at s, Gaya, Medina, & 10  C, and ripened until day 60 (Garde, Arque ~ ez, 2007). Cheese pH was higher on day 3 in cheeses treated Nun on day 2 than in control cheese, but there were no significant differences between cheeses on day 60. Aminopeptidase activity on day 3 was lower in cheeses treated on day 2 than in control cheese with differences between cheeses decreasing along ripening. Residual aS1-, aS2- and b-caseins reached higher levels on day 60 in cheeses treated on day 2, with respective levels of 9.1%, 31.3% and 40.5% in control cheese, 18.7%, 33.7% and 38.5% in 300 MPa cheese and 10.0%, 15.7% and 30.2% in 400 MPa cheese. Hydrophobic peptides on day 60 did not vary with HPP treatment, hydrophilic peptides on day 60 increased in cheese treated at 400 MPa on day 2, and FAA levels on day 60 increased in cheeses treated at 300 or 400 MPa on day 2 with respect to control cheese. All texture parameters (force at breaking point, energy at breaking point and elasticity) increased markedly with HPP treatment on day 2 independently of the pressure level (Garde et al., 2007). HPP treatments on day 2 enhanced the formation of 2-alcohols, except 2-butanol, and branched-chain aldehydes and retarded that of n-aldehydes, 2methyl ketones, dihydroxy-ketones, n-alcohols, unsaturated alcos, hols, ethyl esters, propyl esters and branched-chain esters (Arque ndez-García, Gaya, & Nun ~ ez, 2007). HPP-treatments of Garde, Ferna cheese on day 50 had less marked effects than treatments on day 2. Irish blue-veined cheeses were HPP-treated at 400 or 600 MPa for 10 min at 20  C on day 42 of ripening and further stored at 4  C for 28 days (Voigt, Chevalier, Qian, & Kelly, 2010). Immediately after treatment, counts of lactococci, NSLAB, enterococci, yeasts and moulds respectively declined by 1.9, 3.0, 2.4, 2.1 and 2.7 log units at 600 MPa, while only lactococci, NSLAB and moulds declined at 400 MPa, at a lesser extent than at 600 MPa. At the end of storage, the pH of control cheese had increased from 5.8 to 6.6, while the pH

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of HPP-treated cheeses remained stable. On day 28 of storage, minor differences were observed for pH 4.6-soluble nitrogen, trichloroacetic acid-soluble nitrogen, phosphotungstic acid-soluble nitrogen and FFA levels between control and HPP-treated cheeses. Methyl ketones, the most abundant volatile compounds in blueveined cheeses, were generally found at lower levels in HPPtreated cheeses, particularly if treated at 600 MPa, than in control cheese at the end of storage, although the differences were not significant. The authors concluded that treatment of blue-veined cheese at 600 MPa might serve to arrest ripening (Voigt et al., 2010). Ibores cheeses made from raw goat milk were treated on days 1, 30 and 50 after manufacture at 400 and 600 MPa (Delgado, Gonz alez-Crespo, Cava, & Ramírez, 2012a). LAB counts declined 1.1 and 5.8 log units after treatment on day 1 at 400 or 600 MPa while the respective declines after treatments on day 30 or 60 were generally lower. Levels of water-soluble nitrogen on day 60 increased from 18.35% in control cheese to 18.51e21.98% in 400 MPa cheeses and 22.26e23.27% in 600 MPa cheeses, and nonprotein nitrogen on day 60 also increased, from 6.53% in control cheese to 8.72e10.46% in 400 MPa cheeses and 9.52e10.70% in 600 MPa cheeses. Adhesiveness values on day 60 declined with HPP treatment on day 1 while cohesiveness, springiness, gumminess and chewiness values increased with HPP treatment on days 1 and 30 (Delgado et al., 2012a). Levels of short-chain FFAs in Ibores cheese HPP-treated on days 1, 30 and 50 of ripening, at 400 and 600 MPa for 7 min, declined with respect to control cheese only in cheeses treated at 600 MPa on day 1 while medium- and longchain FFAs did not vary with any of the HPP treatments (Delgado, Gonz alez-Crespo, Cava, & Ramírez, 2012b). The levels of volatile acids of 60-day Ibores cheese declined with HPP treatment on day 1, alcohols and esters declined with HPP treatment on days 1 and 30, and ketones and some individual compounds such as 3methylbutanal, ethylbenzene, p-xylene and limonene increased with HPP treatment on days 1 and 30 (Delgado, Gonz alez-Crespo, Cava, & Ramírez, 2011). Torta del Casar cheeses made from raw ewe milk were HPPtreated at 400 or 600 MPa for 5 min at 14  C on days 21 or 35 of ripening (Calzada et al., 2014b). On day 240, after 60 days of ripening and 180 days of refrigerated storage, pH values were 5.71e5.73 in 400 MPa cheeses and 5.56e5.64 in 600 MPa cheeses, lower than the pH of 6.14 in control cheese. Casein breakdown was retarded by HPP, in particular in 600 MPa cheeses, which had residual aS-casein levels 30e33% higher than control cheese on day 240 while the levels of residual b-casein were 100e103% higher. Hydrophilic peptides were at significantly higher levels in control cheeses than in HPP-treated cheeses on day 240, but HPP had no influence on hydrophobic peptides (Calzada et al., 2014b). Cheeses treated at 600 MPa had on day 60 levels of FAAs similar to those of control cheese and lower than those of 400 MPa cheeses while on day 240 they had 16.47e17.47 mg FAAs g1 DM, lower values than the 23.31 mg FAAs g1 DM of control cheese and the 25.40e26.05 mg FAA g1 DM of 400 MPa cheeses (Calzada et al., 2013a). Cheeses treated at 600 MPa showed increased firmness and elasticity with respect to control and 400 MPa cheeses (Calzada et al., 2014b). HPP retarded the formation of some free carboxylic acids, which showed lower levels in 240-day experimental cheeses than in 60-day control cheese. Thus, propionic acid reached 1.29 mg g1 DM in 60-day control cheese and 2.99, 0.34 and 0.74 mg g1 DM in 240-day control cheese and cheeses treated at 400 or 600 MPa on day 21, respectively, while branched-chain carboxylic acids reached 0.76, 1.15, 0.40 and 0.30 mg g1 DM, respectively, and short-chain FFAs 1.93, 8.69, 1.11 and 2.34 mg g1 DM, respectively. The effect was not so marked for medium- and ~ ez, 2014c). long-chain FFAs (Calzada, del Olmo, Picon, Gaya, & Nun

11

Regarding volatile compounds, aldehydes and esters decreased significantly in 400 or 600 MPa cheeses, alcohols only in 600 MPa cheeses, and ketones, acids, aromatic compounds and hydrocarbons did not vary. HPP had its most marked effect on sulphur compounds, which increased 467-fold in control cheese from day 60 to day 240 and only 9-fold and 10-fold, respectively, in cheeses treated at 400 or 600 MPa on day 21. Arzúa-Ulloa cheese made from raw milk was HPP-treated at 400 or 600 MPa on days 21 or 35 of ripening (Calzada et al., 2015a). LAB counts declined by 2 log units at 400 MPa and 6 log units at 600 MPa immediately after treatment followed by complete recovery in 400 MPa cheeses and only partial recovery in 600 MPa cheeses. The pH of HPP-treated cheeses lagged behind that of control cheese along ripening, reaching on day 240 values of 5.68 in control cheese, 5.59 in 400 MPa cheeses and 5.39e5.40 in 600 MPa cheeses. From day 1 to day 240, the concentrations of aS-, b-, k- and para-k-caseins in control cheese declined by 46%, 64%, 65% and 35%, respectively, while in HPP-treated cheeses they declined by 41e66%, 84e92%, 75e81% and 69e88%, respectively. HPP-treated cheeses showed higher levels of hydrophilic peptides and hydrophobic peptides than control cheese from day 60 onwards, in agreement with the enhanced hydrolysis of caseins. In contrast, total FAAs reached on day 240 lower concentrations in 400 MPa cheeses (22.00e22.81 mg g1 DM) or 600 MPa cheeses (11.44e11.74 mg g1 DM) than in control cheese (31.68 mg g1 DM); this was associated with lower aminopeptidase activity. Higher elasticity values were recorded in HPP-treated cheeses than in control cheese at the last stages of ripening, but differences in firmness were less marked (Calzada et al., 2015a). The lower shortchain FFA concentration in 400 MPa cheeses (0.147e0.148 mg g1 DM) or 600 MPa cheeses (0.086e0.0.087 mg g1 DM) than in control cheese (0.190 mg g1 DM) on day 240 was explained by their lower esterase activity (Calzada et al., 2015b). On day 240, aldehydes and ketones showed higher levels and alcohols lower levels in 600 MPa cheeses than in control or 400 MPa cheeses, sulphur compounds were at higher levels in HPP-treated cheeses than in control cheese, and the other groups of volatile compounds did not vary with HPP treatment (Calzada et al., 2015b). Blue-veined cheese made from pasteurised ewe milk was HPPtreated at 400 or 600 MPa for 5 min at 12  C on days 21, 42 and 63 and stored until day 360. Treatments at 400 or 600 MPa on day 21 were the most effective in retarding b-casein degradation, inactivating aminopeptidases and reducing FAA formation. Hydrophilic peptides were at similar levels in HPP-treated and control cheeses from day 90 onwards, but hydrophobic peptides were at higher levels in HPP-treated cheeses (Calzada et al., 2013b). Cheese treated at 600 MPa on day 21, which showed the lowest esterase activity, had the lowest FFA concentration on day 360, as low as that of control cheese on day 90. HPP influenced the levels of 97 of the 102 individual volatile compounds and of the 10 chemical groups of volatile compounds. The lowest levels of most groups of volatile compounds were recorded for cheese treated at 600 MPa on day 21 (Calzada et al., 2013c). Brie cheese HPP-treated at 400 or 600 MPa for 5 min at 14  C on days 14 or 21 showed a pH value increase of less than 0.3 units from day 21 to day 60, while in control cheese the pH increased by 2.0 units (Calzada et al., 2014a). Cheeses treated at 600 MPa showed the highest levels of residual caseins, and control cheese the lowest levels, during refrigerated storage. A 7.6-fold increase of hydrophobic peptides was recorded from day 21 to day 60 in control cheese and only 0.8- to 1.6-fold increases in HPP-treated cheeses. Control cheese showed the maximum aminopeptidase activity and cheeses treated at 400 MPa the highest FAA concentration. Cheeses treated at 400 or 600 MPa on day 14 had the firmest texture (Calzada et al., 2014a). HPP treatments lowered total FFA contents

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of cheeses by up to 88.5% on day 120. Levels of alcohols, aldehydes, acids, esters and ethers were respectively up to 3.4-, 1.9-, 43.8-, 18.7- and 5.6-fold in HPP-treated cheeses than in control cheese on day 120 (Fig. 7) while the levels of ketones, hydrocarbons, sulphur compounds, pyrazines and amines were respectively up to 88.6%, 48.9%, 96.9%, 99.3% and 99.4% lower in HPP-treated cheeses than in control cheese (Calzada et al., 2014d). Mature Torta del Casar cheeses made from raw ewe milk were treated on day 60 of ripening at 200 or 600 MPa for 5 or 20 min, at 10  C (Delgado, Rodríguez-Pinilla, M arquez, Roa, & Ramírez, 2015). The pH of control cheese was 5.39 on day 60 and 5.57 on day 240 while it ranged from 5.43 to 5.48 in HPP-treated cheeses on day 240. Nitrogen soluble at pH 4.4 increased in control cheese from 42.28% on day 60 to 50.10% on day 240, time at which it reached 52.93%, 52.81%, 47.29% and 42.88% in cheeses treated at 200 MPa for 5 min, 200 MPa for 20 min, 600 MPa for 5 min and 600 MPa for 20 min, respectively. There were no significant differences in FAA levels on day 240 between control and HPP-treated cheeses. On day 240, residual para-kappa-, aS1-, aS2- and b-caseins were at higher levels in 600 MPa cheeses than in control cheese while only parakappa- and aS2-caseins were at higher levels in 200 MPa cheeses than in control cheese. Firmness reached 11.39, 10.80, 13.05, 8.15 and 7.62 N on day 240 in control cheese and in cheeses treated at 200 MPa for 5 min, 200 MPa for 20 min, 600 MPa for 5 min and 600 MPa for 20 min, respectively (Delgado et al., 2015). HPP treatments, particularly at 600 MPa, are effective in retarding proteolysis and lipolysis in most cheese varieties, and also in reducing the formation of some undesirable volatile compounds, generally achieving a beneficial effect on cheese sensory characteristics. 2.3. Preventing defects Defects of enzymatic or microbial origin in cheese can be controlled by means of HPP treatments. Examples are flavour defects such as bitterness occurring in different cheese types, colour

and appearance defects caused by spoilage bacteria, yeasts, moulds and mites, and texture and flavour defects such as early blowing or late blowing caused by different groups of contaminating bacteria. 2.3.1. Reducing bitterness Bitterness is a flavour defect generally associated with the presence of high levels of hydrophobic peptides in cheese, which may be induced by reduced salt content. To investigate the possibility of controlling bitterness in Cheddar cheese by means of HPP treatment, low salt-in-moisture (0.2e2.5%) and regular salt-inmoisture (5.3%) cheeses were treated on day 7 after manufacture at 405 MPa for 3 min at 9  C (Ozturk, Govindasamy-Lucey, Jaeggi, Johnson, & Lucey, 2013). Reducing salt concentration increased the formation of b-casein (f1e189/192) hydrophobic bitter peptide as well as of bitter, acid and metallic flavour notes with respect to those of regular cheese. Despite the objective of the research, HPP treatment at 405 MPa had no significant effect on the formation of the b-casein (f1e189/192) peptide and the sensory characteristics of low salt cheeses. Higher pressure levels or earlier application of HPP were suggested by the authors as possible strategies to reduce bitterness in low salt Cheddar cheese. In contrast, HPP treatment of Brie cheese at 400 or 600 MPa for 5 min on days 14 or 21 after manufacture resulted in lower bitterness scores than those of control cheese from day 60 onwards, which were positively correlated with low contents of hydrophobic peptides and negatively correlated with high flavour quality scores (Calzada et al., 2014d). Bitterness was also reduced in Feta-type cheese made from pasteurised ovine milk by treatment at 200 MPa for 20 min at 20  C, which resulted in Pep A and Pep X aminopeptidase activities higher than those in control cheese (Giannoglou et al., 2016). Similarly, bitterness scores of Torta del Casar cheese on days 120 and 240 after manufacture were reduced by treatment on day 60 at 600 MPa for 20 min, with further storage at 6  C for 180 days, in comparison with those of the respective control cheeses (Delgado-Martínez, Carrapiso, Contador, & Ramírez, 2019).

50 45

Arbitrary area units

40 35 30 25 20 15

10 5 0

Control

400 MPa

600 MPa

Fig. 7. Levels of volatile compounds in Brie cheese non-HPP-treated (control) and HPP-treated at 400 and 600 MPa for 5 min on day 15 after manufacture (expressed in chromatographic area units). Cheeses were ripened at 12  C for 21 days and further stored at 4  C until day 120. Adapted from Calzada et al. (2014d).

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2.3.2. Controlling spoilage bacteria Among cheese defects of microbial origin, the increase in the incidence of blue discoloration in mozzarella and some fresh cheese types in Europe and USA is causing alarm among cheese producers and consumers (Martin, Murphy, Ralyea, Wiedmann, & Boor, 2011; Nogarol et al., 2013; RASFF, 2011). This particular type of spoilage, which is induced by quorum sensing mechanisms and enhanced by the availability of aromatic FAAs, was associated to specific contamination of fresh cheese by certain Pseudomonas fluorescens strains (Andreani et al., 2015; Carrascosa et al., 2015; del ~ ez, 2018). The effect of HPP on the functional Olmo, Calzada, & Nun and rheological properties of Mozzarella cheese has been investigated (Ozturk, Govindasamy-Lucey, Jaeggi, Johnson, & Lucey, 2018; Sheehan et al., 2005). However, there is no available information on the effect of HPP treatments on the Ps. fluorescens strains responsible for the blue discoloration defect in mozzarella and other cheese varieties. As indicated above, treatment of fresh goat milk cheese at 450e500 MPa lowered aerobic mesophilic counts by 1.8e3.0 log cfu g1 on day 1 after manufacture, depending on processing pressure, time and temperature, with no bacterial growth taking place in HPP-treated cheeses during refrigerated storage for 60 days (Capellas et al., 1996). Also, treatment of starter-free fresh cheese at 500 MPa for 5 min at 16  C on day 1 after manufacture lowered counts of psychrotrophs to 5.5 log cfu g 1 on day 21 while they attained 8.6 log cfu g 1 in control cheese, and Pseudomonas spp. to counts below detection level in 500 MPa cheese while they reached 7.5 log cfu g 1 in control cheese (Evert-Arriagada et al., 2014). Likewise, treatment of mozzarella cheese at 500 or 600 MPa for 3 min at 7  C lowered counts of contaminating NSLAB to 3.5 and 2.7 log cfu g 1, respectively, while they reached 4.8 log cfu g 1 in control cheese after 140 days of refrigerated storage (Ozturk et al., 2018). A beneficial effect of HPP was also recorded for fresh cheese made from ultrafiltered milk (Ribeiro, Leite, & Cristianini, 2019). Treatment of fresh cheese at 600 MPa for 5 min at 25  C lowered counts of psychrotrophs on day 28 by at least 6 log units, reduced soluble N concentration, yielded a firmer texture and extended product shelf life. In view of the results obtained so far, HPP treatment of mozzarella and fresh cheeses appears as a reliable and useful tool for preventing the blue discoloration defect and extending their shelf life by restraining the growth of psychrotrophs during refrigerated storage. Other cheese colour defects associated with growth of spoilage bacteria have been reported. Cottage cheese contaminated with Rahnella aquatilis developed a rusty-brown discoloration when milk was acidified with glucono-d-lactone, but not when it was acidified with lactic or citric acid (Davey & Eyles, 1992). Mozzarella cheese has been reported to exhibit orange discoloration associated with Pseudomonas aureofaciens and Pseudomonas putida biovar II, orange-red discoloration related to Plantibacter flavus and Plantibacter agrosticola, orange-red-brown discoloration caused by Plantibacter brassicacearum, yellow-purple discoloration ascribed to Pantoea agglomerans and Pseudomonas gessardii, and greenish discoloration associated with strains of Ps. fluorescens, and fluorescent discoloration related to strains of Ps. fluorescens, Ps. putida and Pseudomonas palleroni (Cantoni et al., 2006). Fresh Ricotta cheeses showed red discoloration associated with the presence of Serratia marcescens, presumably coming from the milk of a cow with subclinical mastitis (Alberghini, Tallone, & Giaccone, 2010). Pink discoloration of ripe Continental-type cheeses was traced to the presence of the carotenoid-producing bacterium Thermus thermophilus, consistently isolated from hot water samples at the dairy plant (Quigley et al., 2016). As in the case of blue discoloration, contaminating Gram-negative bacteria

13

responsible for other colour defects in fresh cheeses can be easily eliminated by means of HPP treatments. Early blowing of cheese is caused by lactose-fermenting bacteria, mostly coliforms belonging different genera of the Enterobacteriaceae family, the growth and survival of which in cheese is ~ ez, Gaya, influenced by manufacture and ripening conditions (Nun & Medina, 1985). Gram-negative bacteria are more sensitive to high pressure than Gram-positive bacteria (Considine, Kelly, Fitzgerald, Hill, & Sleator, 2008; Hoover, Metrick, Papineau, Farkas, & Knorr, 1989) and HPP may be a useful tool for their control in cheese. The decrease in E. coli K-12 in model Cheddar cheese was 2.4 or 5.1 log units after HPP at 200 or 300 MPa for 20 min at 20  C, higher than in buffer or cheese slurry (O’Reilly et al., 2000a). In commercial La Serena cheese made from raw ewe milk and treated at 300 or 400 MPa for 10 min at 10  C, on day 2 after manufacture, coliform counts decreased by 4.1 or 5.5 log units, respectively, and did not s et al., 2006). Coliform counts were recover during ripening (Arque also lowered in pasteurised ovine milk Feta-type cheese by HPP treatment on day 15 of ripening, by approximately 1.0 and 1.5 log units at 200 and 500 MPa for 15 min at 20  C, respectively, compared with control cheese (Moschopoulou, Anisa, Katsaros, Taoukis, & Moatsou, 2010). In commercial Ibores cheese made from raw goat milk and treated on day 1 after manufacture at 400 or 600 MPa for 7 min, Enterobacteriaceae counts decreased by 1.4 or 2.6 log units, respectively, and did not recover afterwards (Delgado et al., 2012a). However, when commercial Ibores cheese was treated on day 60 after manufacture at 400 or 600 MPa for 7 min, Enterobacteriaceae counts only decreased by 0.5 or 1.1 log units, respectively (Delgado et al., 2013), which points to a higher resistance to high pressure of the strains that had withstood the acidic conditions of cheese during ripening. Coliform counts fell below detection level in commercial raw milk Arzúa-Ulloa cheese treated at 400 or 600 MPa for 5 min, on days 14 or 21 after manufacture, after all the HPP treatments while they attained in control cheese 6.1 log cfu g1 on day 14 and 5.8 log cfu g1 on day 21 (Calzada et al., 2015a). Coliforms responsible for the early blowing defect in many cheese types, particularly in those made from raw milk, can be easily controlled by means of HPP treatments. Butyric acid bacteria belonging to differences species of Clostridium, mainly Clostridium butyricum, Clostridium tyrobutyricum, Clostridium sporogenes and Clostridium beijerinckii, capable of fermenting lactic acid with production of butyric acid, acetic acid, carbon dioxide and hydrogen, are responsible for the late blowing ~ ez, defect in hard and semi-hard cheeses (Garde, Arias, Gaya, & Nun 2011). The high resistance to pressure of Clostridium spp. spores due to their particular cellular structures and biochemical composition (Black et al., 2007; Georget et al., 2015) constitutes a serious drawback for the application of HPP when aiming to prevent the late blowing defect in cheese. Pre-treatment at low (100 MPa) or high (500e600 MPa) pressures has been proven to induce the germination of Bacillus subtilis spores (Wuytack, Boven, & Michiels, 1998). Different metabolic pathways and physiological mechanisms are involved in the germination and inactivation of spores at low and high pressures (Black et al., 2007; Reineke, Mathys, Heinz, & Knorr, 2013). In miniature cheeses inoculated with B. cereus spores and treated at 300, 400 or 500 MPa at 30  C for 15 min, with or without a previous germination cycle at 60 MPa for 210 min at 30  C, the highest lethality (1.7 log units decrease) on day 1 was achieved by means of the germination cycle followed by HPP at 500 MPa for 15 min  pez et al., 2003). (Lo

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Information on the effectiveness of HPP against Clostridium spp. responsible for cheese late blowing defect is not abundant. HPP treatments (200e500 MPa for 10 min at 14  C) were applied on day 7 after manufacture to semi-hard cheeses made from raw ewe milk inoculated with two strains of C. tyrobutyricum at 5 log  mez-Torres, Delgado, Gaya, & Garde, 2016). cfu mL1 (Avila, Go Cheeses made from milk inoculated with C. tyrobutyricum spores, either untreated or HPP-treated at 200 MPa, showed visible late blowing defect, lower concentrations of lactic, citric and acetic acids, and higher levels of pyruvic, propionic and butyric acids. Those cheeses had higher levels of 1-butanol, methyl butanoate, ethyl butanoate and ethyl pentanoate than cheeses without added spores. However, cheeses with C. tyrobutyricum spores that had been HPP-treated at 300, 400 or 500 MPa did not show late blowing defect and their levels of organic acids and volatile compounds were similar to those of the respective HPP-treated cheeses made from milk not inoculated with spores. A decrease in C. tyrobutyricum spore counts observed after curd pressing seemed to indicate early spontaneous spore germination. HPP treatments of cheese at 300 MPa or higher pressures were able to inactivate the emerged C. tyrobutyricum vegetative cells and prevented the late blowing defect. 2.3.3. Dealing with eukaryotes Yeasts and moulds exert beneficial effects on the sensory characteristics of many cheese varieties. However, they may cause defects in most types of fresh cheeses and in semi-hard or hard bacterially ripened cheeses. In the case of yeasts, brown discoloration at the surface of raw ewe milk Portuguese cheese was associated with tyrosine metabolism by the yeast Yarrowia lipolytica (Carreira, Paloma, & Loureiro, 1998) a defect which has also appeared on the surface of mould-ripened cheeses (Williams & Withers, 2007). Moulds identified as Cladosporium cladosporioides, Cladosporium herbarum, Penicillium commune, Penicillium glabrum and Phoma sp. are responsible for the thread mould defect which may occur in vacuum-packaged Cheddar cheese (Hocking & Faedo, 1992) and they also cause discoloration defects in cheese, such as reported for Mozzarella contaminated with Phoma glomerata (Casalinuovo, Rodolfi, Rippa, Scognamiglio, & Musarella, 2015). Mould growth on the surface of many cheese varieties is deleterious for their external appearance but the main concern about mould growth is the possibility of mycotoxin production. Ochratoxin A and aflatoxin M1, the most hazardous mycotoxins found in cheese, are produced by some Aspergillus and Penicillium species either via direct contamination of cheese or indirect contamination of milk (Hymery et al., 2014). In addition, some cheese-related Penicillium spp. are capable of producing other mycotoxins such as PR toxin and roquefortine (Medina, Gaya, & ~ ez, 1985). Nun Vegetative cells of yeasts and moulds are more sensitive to high pressure than bacteria (Considine et al., 2008; Martínez-Rodríguez et al., 2012). However, ascospores of yeasts and moulds, particularly the older spores, are considerably more resistant than vegetative cells (Chapman et al., 2007). As in the case of bacterial endospores, sublethal HPP treatments may induce the germination of fungal ascospores. Influx of water through the HPP-damaged outer cell wall has been suggested as the mechanism inducing ascospore activation and germination (Dijksterhuis & Teunissen, 2004). In miniature Cheddar cheese made from milk intentionally contaminated with P. roqueforti, counts of the mould decreased by 6 log units after treatment at 400 MPa for 20 min at 20  C (O’Reilly et al., 2000a). In Irish blue-veined cheese treated at 400 or 600 MPa for 10 min at 20  C, P. roqueforti counts declined by 2.2 and 2.7 log units, respectively, on day 42 after manufacture (Voigt et al., 2010).

However, in ewe milk blue-veined cheese treated at 400 MPa for 5 min at 13  C, on days 21, 42 or 63 after manufacture, P. roqueforti counts respectively decreased by 5.3, 0.7 and 0.7 log units immediately after treatment, and fell below detection level after treatment at 600 MPa. Differences in lethality at 400 MPa were explained by the different physiological status of the mould at treatment (Calzada et al., 2013b). According to the authors, on day 21 there was profuse mycelial growth in cheese with low levels of spores, considered to be more baroresistant forms, while sporulation increased as ripening proceeded. In Brie cheese treated on days 14 or 21 of ripening at 400 MPa for 5 min at 14  C, counts of P. camemberti declined by 2.3e3.3 log units, and by more than 5 log units after treatment at 600 MPa (Calzada et al., 2014a). Counts of spoilage yeasts in fresh lactic curd cheese treated at 300, 400 and 600 MPa for 5 min on day 1 after manufacture were, respectively, approximately 2, 3 and 4 log units lower than in control cheese after 56 days of storage (Daryaei et al., 2008). In fresh rennet curd cheese, treated at 300 and 400 MPa for 5 min on day 1 after manufacture and stored at 4  C, counts of yeasts and moulds on day 7 were, respectively, 3.2 and 4.2 log units lower than in control cheese while on day 21 they were below detection level in control and 300 MPa cheeses and reached 4.8 log cfu g1 in 400 MPa cheese (Evert-Arriagada et al., 2012). In the same study, counts of yeasts and moulds on day 4 in cheeses treated at 400 MPa and stored at 8  C were respectively 3.7 and 4.1 log units lower than in control cheese, while their counts on day 11 were below detection level in control and 300 MPa cheeses and 3.0 log cfu g1 in 400 MPa cheese, a result that was partly explained by the authors as due to late microbial recovery in cheese treated at 400 MPa. Mites are considered to be involved in the ripening process of some cheese varieties such as Mimolette in France and Milbenkase in Germany (Melnyk, Smith, Scott-Dupree, Marcone, & Hill, 2010). Cheeses ripened with mites develop a nutty, fruity flavour and aroma, even though the mechanisms responsible for their effect on cheese sensory characteristics remain unknown. The main cheeserelated mite species are Acarus siro, Acarus farris, Acarus immobilis, Tyrophagus putrescentiae, Tyrophagus longior, Tyrophagus neiswanderi, Tyrophagus palmarum and Tyrolichus casei (Melnyk et al., 2010). Mites infest and grow in cheeses under favourable ripening and storage conditions, i.e., temperature above 4  C and relative humidity above 60%. Populations may attain 260 mites nchez-Ramos & Castan ~ era, 2009). They cm2 at the cheese rind (Sa are responsible not only for the characteristic external appearance defects in cheese, which bring about important economic losses, but also for respiratory disorders in workers of cheese plants (Molina, Aiache, Tourreau, & Jeanneret, 1974). There is no available information on the effect of HPP on cheese mites. However, HPP treatments were investigated for the control of codling moth in apple and western cherry fruit fly in cherries, with 100% lethality for codling moth eggs, more baroresistant than larvae, at 207 MPa for 5 min and for western cherry fruit fly eggs, more baroresistant than instars, at 172 MPa for 5 min (Neven, Follett, & Raghubeer, 2007). From the results of their study on arthropods other than mites such as fruit moths and flies, HPP treatment may be suggested as a useful tool for the control of cheese mites. 3. The HPP of cheese: shadows As in the case of HPP treatments of other foodstuffs, different studies on cheese HPP have pointed out some setbacks for the optimal application of this technology. They may be related to the survival of undesirable microorganisms in cheese or to changes in cheese external or sensory characteristics.

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3.1. Recovery of HPP-injured cells Microorganisms present in cheese subjected to HPP may die or remain alive as sublethally injured cells, depending on the severity of treatment parameters together with the substrate characteristics and the physiological status of microorganisms at treatment. Two types of cell injury, I1 and I2, were described for pathogens after HPP of milk (Bozoglu, Alpas, & Kaletunç, 2004), depending on the cell ability (I1) or inability (I2) to form colonies on non-selective media. Only after full injury recovery would cells be able to form colonies on selective media. The detection of sublethally injured cells will sometimes require a resuscitation step in mild culture media under favourable incubation conditions or the use of cultureindependent methods (Jany & Barbier, 2008). The recovery of microorganisms after HPP treatment and their detection in HPPtreated cheese during storage is of particular concern in the case of pathogens. Two S. enterica strains were able to recover in model starter-free cheese treated at 400 MPa for 10 min, with increases of 3e5 log units from day 0, immediately after treatment, to day 15 of storage at 8  C, but they were not able to recover in cheese made with starter culture. Values of pH decreased during the 15-day storage period from 4.89 to 4.79 in cheese made with starter culture and from 6.56 to 6.46 in starter-free cheese (De Lamo-Castellví et al., 2007). No recovery of three Y. enterocolitica strains of different serotype, a E. coli O59:H21 strain and a E. coli O157:H7 strain occurred during storage at 8  C of model cheeses made with starter culture and treated at 300e500 MPa for 10 min (De Lamo-Castellví et al., 2005, 2006). L. monocytogenes and S. aureus did not recover after HPP treatment of model semi-hard cheeses at 300 MPa for 10 min or 500 MPa for 5 min, on days 2 or 50 after manufacture, during further ripening s et al., 2005a,b). This was also the case at 12  C until day 60 (Arque for E. coli O157:H7 in model cheeses HPP-treated and ripened under the same conditions (Rodríguez et al., 2005). Cheese pH values during ripening ranged from 5.07 to 5.22 in control cheese, from 5.10 to 5.34 in 300 MPa cheeses and from 5.09 to 5.28 in 500 MPa s et al., 2005a,b; Rodríguez et al., 2005). cheeses (Arque In contrast, two L. monocytogenes strains, inoculated at 6 log cfu g1 in starter-free fresh cheese which was HPP-treated at 400e600 MPa, recovered during storage at 4  C (Evert-Arriagada et al., 2018). Counts of L. monocytogenes CECT 4031 increased from 3.0 log cfu g1 immediately after treatment at 400 MPa for 5 min to 4.7 log cfu g1 on day 15, and from counts below detection level in cheeses treated at 500 or 600 MPa for 5 min to 1.7 and 0.8 log cfu g1, respectively, on day 15. Counts of L. monocytogenes Scott A, which was more resistant to pressure than strain CECT 4031, increased from 5.4 to 2.4 log cfu g1 immediately after treatment at 500 or 600 MPa to 6.3 and 3.4 log cfu g1, respectively, after 15 days at 4  C (Evert-Arriagada et al., 2018). Values of pH close to neutrality as in starter-free cheeses are more favourable for the recovery of cells injured by HPP treatment than the low pH values found in most cheese varieties. Counts of B. cereus in model cheeses made with starter culture, with a pH value close to 5.0, treated at 300 MPa for 15 min, 400 MPa for 15 min or 60 MPa for 210 min, all at 30  C, increased from 5.8, 5.8 and 4.8 log cfu g1 on day 1 after treatment to 6.3, 6.1 and 5.0  pezlog cfu g1, respectively, on day 15 of storage at 8  C (Lo Pedemonte et al., 2003). In commercial starter-free fresh cheeses treated at 400 MPa, counts of aerobic mesophiles increased from 3.4 log cfu g1 on day 1 after treatment to 6.2 log cfu g1 on day 21 while counts of psychrotrophic bacteria and moulds þ yeasts, which were below detection level on day 1 after treatment, reached 6.1 and 4.8 log cfu g1, respectively, on day 21 (Evert-Arriagada et al., 2012).

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Recovery of injured cells after HPP treatments is a problem that cannot be solved exclusively by the use of higher pressure levels, which might be deleterious for cheese characteristics. As discussed later in this review, combined strategies seem a more convenient tool for preventing their recovery. 3.2. Changes in external appearance and colour The external appearance of cheese is the first quality parameter that the consumer perceives. HPP treatment of some cheese types may alter the colour and general aspect of their rind, and even modify their shape. No changes in the external aspect of Irish blueveined cheese samples were reported after treatment at 400 or 600 MPa for 10 min (Voigt et al., 2010). However, ewe milk blueveined cheeses treated at 400 or 600 MPa for 5 min on days 21, 42 or 63 after manufacture suffered subsiding, which was more influenced by cheese age at treatment than by pressure level (Calzada et al., 2013b). Cheese height at the centre of the flat surface (93 mm in control cheese on day 21) decreased on average 14 and 12 mm in cheeses treated at 400 and 600 MPa, respectively, while it decreased 18, 10 and 12 mm in cheeses treated on days 21, 42 or 63 after manufacture, respectively. HPP-treated cheeses gradually recovered their shape after treatment, with average decreases in height of 15 and 11 mm on days 90 and 360 after manufacture (Calzada et al., 2013b). The rind of Brie cheese was considerably altered by HPP treatment at 400 or 600 MPa for 5 min on days 14 or 21 (Calzada et al., 2014d). On day 30 after manufacture, values of L*, a* and b* colour parameters were 91.34, 0.12 and 6.80 in control cheese, respectively, while L* ranged from 77.10 to 80.42 (less bright), a* from 1.63 to 3.44 (more reddish), and b* from 18.44 to 21.26 (more yellowish) in HPP-treated cheeses. Impregnation of the mould mycelium at the rind of HPP-treated cheeses by water and fat from the interior resulted in loss of its typical white mossy aspect, which might diminish consumer acceptance. On day 60 after manufacture, values of L*, a* and b* were 85.74, 0.44 and 8.44 in control cheese, respectively, while L* ranged from 77.38 to 81.95, a* from 1.27 to 1.91, and b* from 22.50 to 25.35 in HPP-treated cheeses. Changes in a* and b* colour parameters during storage were related to growth of red and yellow-pigmented microorganisms (Calzada et al., 2014d). Colour parameters at the cheese interior also vary with HPP treatments. Changes in colour at the interior of HPP-treated cheeses have been attributed to a higher degree of casein hydration, as shown by the increased amount of non-expressible serum, to a more dense and compact protein network with different size and shape of pores, and to smaller fat globules more uniform in size and shape, which alter its light-absorbing and light-scattering properties (Capellas et al., 2001; Koca, Balasubramaniam, & Harper, 2011; ~ ez, 2013; Sheehan et al., 2005). HPP Picon, Alonso, van Wely, & Nun treatments alter colour parameters at the interior of cheeses made from either cow, goat or ewe milk. In reduced-fat mozzarella cheese HPP-treated on day 1 at 400 MPa for 5 min, L* decreased from 86.0 to 67.9, a* decreased from 8.9 to 9.9, and b* decreased from 27.1 to 23.8 immediately after treatment, although the three parameters reached similar values after 75 days of storage (Sheenan et al., 2005). In Cheddar cheese treated at 400 MPa for 10 min, L* did not vary, a* declined from 7.2 to 7.9, and b* increased from 31 to 32 with respect to control cheese on day 40 of ripening (Rynne et al., 2008). Whitebrined cheese made from cow milk and treated at 400 MPa for 5 min had similar L* values, lower a* values, and higher b* values than control cheese (Koca et al., 2011). Starter-free fresh cheese treated at 500 MPa for 5 min on day 1 showed after treatment lower L* value (94.4 versus 95.3), similar a* value (0.76

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versus 0.66), and higher b* value (11.4 versus 10.5) than control cheese (Evert-Arriagada et al., 2014). Arzúa-Ulloa cheese made from raw cow milk and treated at 400 or 600 MPa for 5 min on days 14 or 21 after manufacture had L* values on day 21 ranging from 85.3 to 86.6, a* values from 1.3 to 1.7, and b* values from 18.2 to 18.8, close to the values of control cheese, which were 85.1, 2.0 and 19.0, respectively (Calzada et al., 2015b).  fresh cheese at 500 MPa for 5 After treatment of goat milk Mato or 30 min at 10  C (Capellas et al., 2001), L* respectively declined from 89.2 to 88.4 or 87.7, a* increased from 0.81 to 0.57 or 0.76, and b* increased from 7.8 to 8.3 or 8.7. In goat milk Garrotxa semihard cheese treated at 400 MPa for 5 min, L* declined from 93.6 to 92.5, a* declined from 0.84 to 0.94, and b* increased from 8.6 to 9.6 with respect to control cheese on day 3 after manufacture (Saldo, Sendra, & Guamis, 2002). Pressure level influenced the colour of Ibores cheese made from raw goat milk and HPP-treated on day 1 that on day 2 showed L*, a* and b* values of 96.8, 1.76 and 2.05 after treatment at 400 MPa, 98.1, 0.43 and 0.33 values after treatment at 600 MPa, and 97.6, 0.03 and 1.80 values if untreated (Delgado et al., 2012a). Ewe milk cheese treated at 300 MPa for 10 min on days 1 or 15 after manufacture showed on day 15 L* values of 89.8e90.5, a* values of 0.55e0.58, and b* values of 10.9e11.4 while the respective values of control cheese were 92.2, 0.50 and 9.6 (Juan et al., 2008). nico cheese made from a mixture of ewe and cow milk and In Hispa treated at 400 MPa for 5 min, L* declined from 80.5 to 78.9, a* declined from 1.08 to 1.31, and b* increased from 14.2 to 14.7  with respect to control cheese on day 15 after manufacture (Avila, ~ ez, 2008). Torta del Casar cheeses made from raw ewe Garde, & Nun milk and HPP-treated on day 60 at 200 or 600 MPa for 5 or 20 min showed on day 120 after manufacture L* values ranging from 96.4 to 100.4, a* values from 0.8 to 1.6 and b* values from 1.9 to 6.4 while the respective values of control cheese were 98.7, 0.5 and 2.8, with low statistical significance of HPP treatment (Delgado et al., 2015). Semi-hard cheeses made from raw ewe milk and HPP-treated at 200, 300, 400 and 500 MPa for 10 min on day 7 after manufacture showed on day 60 similar L* values (80.0e82.9 versus 81.1), lower a* values (2.2 to 3.0 versus 1.9) and, only in the case of cheeses treated at 400 or 500 MPa, higher b* values  (17.8e19.1 versus 16.3) than control cheese (Avila et al., 2017a). 3.3. Altered sensory properties The effect of HPP treatment on the biochemical events occurring during ripening induces changes in cheese flavour, aroma and odour, which can be correlated with the levels of sapid and aromatic compounds, and in cheese texture, closely related with the extent of casein network breakdown. Since not all the studies on the HPP of cheese oriented to mastering its ripening process included sensory analysis, information on the subject is still lacking. HPP treatments alter sensory characteristics of cheeses made from either cow, goat or ewe milk. Edam cheese HPP-treated at 200 or 400 MPa for 30 min did not exhibit the characteristic eyes of this variety and had a more flexible consistency than control cheese (Iwanczak & Wisniewska, 2005). Cheddar cheese treated at 400 MPa for 10 min on day 1 had similar odour attributes than control cheese but the scores of flavour attributes such as pungent, onion-like, salty, acidic and bitter as well as flavour strength were lower than those of control cheese after ripening for 90 or 180 days (Rynne et al., 2008). Commercial Arzúa-Ulloa raw milk cheese treated at 400 or 600 MPa on days 21 or 35 of ripening showed no differences in flavour preference, flavour intensity or umami scores with respect to control cheese, although bitter scores were higher in HPPtreated cheeses from day 60 onwards (Calzada et al., 2015a).

There were no differences in odour preference, odour intensity or odour attributes such as acid, putrid or rancid between control and HPP-treated Arzúa-Ulloa cheeses, in spite of the lower contents of short-chain FFA and the higher levels of sulphur compounds in all the HPP-treated cheeses, and the higher levels of aldehydes and ketones and the lower levels of alcohols in 600 MPa cheeses (Calzada et al., 2015b). Commercial Brie cheese HPP-treated at 400 or 600 MPa for 5 min on days 14 or 21 showed flavour preference scores similar to those for control cheese until day 30, but from day 30 to day 60 the flavour preference for HPP cheeses hardly varied while that for control cheese suffered a drastic decline, with differences persisting until day 120 (Calzada et al., 2014a). Odour preference scores of HPP-treated and control cheeses were similar from day 21 to day 60, but on day 90 they ranged from 5.7 to 6.1 in HPP-treated cheeses and were 4.0 in control cheese and on day 120 they ranged from 4.3 to 4.9 in HPP-treated cheeses and were 1.4 in control cheese. Unpleasant odour characteristics of control cheeses on day 120 were related to the sharp increase in the levels of volatile compounds such as sulphur compounds, pyrazines and amines (Calzada et al., 2014d). Garrotxa cheese made from pasteurised goat milk and treated at 400 MPa for 5 min showed bitter and acidic flavour notes, and a less crumbly and more elastic texture than control cheese (Saldo et al., 2000). Commercial Ibores cheese made from raw goat milk and treated at 400 and 600 MPa on days 1, 30 or 50 of ripening showed lower odour intensity than control cheese on day 60 if HPP-treated on day 1, but odour intensity at day 60 did not vary if the cheeses were HPP-treated on days 30 or 50 (Delgado et al., 2012a). However, flavour intensity and the taste attributes salty, sharp and abnormal taste did not vary with any of the HPP treatments applied (Delgado et al., 2012a). Cheese made from pasteurised ewe milk and treated at 300 MPa for 10 min on day 1 had inferior taste quality, aroma quality and odour quality scores on day 90 when compared with control cheese and with cheese treated at 300 MPa on day 15. The lower quality scores of cheese treated on day 1 were attributed to its lower FFA levels and its higher pH value, which might negate the flavour efnico cheese made from a fect of FFAs (Juan et al., 2008). Hispa mixture of ewe and cow milk and treated at 400 MPa for 5 min on day 15 showed taste preference and taste intensity scores similar to those for control cheese, higher scores for “milky” odour and aroma attributes and lower scores for odour preference, odour intensity, and “buttery” odour, “caramel” odour and “yogurt-like” odour and aroma attributes. Differences in sensory properties were attributed to the lower FFA concentration and the different volatile profile of  HPP-treated cheese (Avila et al., 2006a, 2007). Cheeses made from raw ewe milk and HPP-treated at 200e500 MPa for 10 min on day 7 after manufacture had sensory properties similar to those of control cheese when treated at 200e400 MPa but treatment at 500 MPa affected some flavour characteristics, with a positive effect on aroma preference and a negative effect on taste intensity. Differences in sensory properties were associated with the higher FAA concentration of 200e400 MPa cheeses and the volatile profile of all the HPP-treated cheeses, which varied with the pressure level  applied (Avila et al., 2017a). Commercial La Serena cheese made from raw ewe milk and HPP-treated on days 2 or 50 after manufacture, at 300 or 400 MPa for 10 min, showed lower taste preference and taste intensity than control cheese on day 60 while sour taste increased with HPP at 400 MPa on day 2 and was not affected by the other treatments, bitter taste slightly increased with all treatments excepting 400 MPa on day 50, and texture preference declined with HPP treatments at 300 or 400 MPa on day 2 and was not affected by HPP treatments on day 50 (Garde et al., 2007). Odour characteristics of

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60-day cheeses were not affected by HPP treatments on day 2, but aroma preference and aroma intensity scores were lower than those of control cheese. Differences in the sensory properties of La Serena cheese were related to the higher levels of 2-alcohols and branched-chain aldehydes and the lower levels of aldehydes, 2methyl ketones, dihydroxy-ketones, alcohols, unsaturated alcohols and esters in cheeses HPP-treated on day 2 with respect to s et al., 2007). control cheese (Arque Commercial Torta del Casar cheese made from raw ewe milk and treated at 600 MPa on days 21 or 35 showed flavour intensity lower than that of control cheese and cheeses treated at 400 MPa on days 180e240, and lower flavour preference on days 120e240. Acid, salty, sweet and umami scores were similar for control and HPPtreated cheeses, but bitter scores were lower in 600 MPa cheeses than in control cheese from day 120 onwards (Calzada et al., 2014b). Odour preference scores of control and HPP-treated cheeses did not differ significantly on day 60 but scores on day 240 were 0.9 for control cheese, 5.0e5.8 for 400 MPa cheeses and 5.1e6.2 for 600 MPa cheeses, most probably as a consequence of the increase in volatile sulphur compounds (Calzada et al., 2014c). Commercial blue-veined cheese made from pasteurised ewe milk and HPP-treated at 400 or 600 MPa for 5 min on days 21, 42 and 63 showed minor differences in sensory characteristics with respect to control cheese, with the only exception of cheese treated at 600 MPa on day 21 that had lower flavour intensity and flavour preference scores than control cheese, which were related to the higher levels of hydrophobic peptides in 600 MPa cheese. In contrast, flavour attributes “acid”, “bitter”, “salty”, “sweet”, and “umami” attained similar scores in control and HPP-treated cheeses (Calzada et al., 2013b). The low flavour preference scores of cheese treated at 600 MPa on day 21 were also attributed to its reduced levels of some groups of volatile compounds which were related to the low counts of P. roqueforti and other microorganisms during ripening and storage (Calzada et al., 2013c). 4. The HPP of cheese: prospects In light of the results obtained so far on the HPP treatment of cheese, new strategies can be envisaged to overcome some process limitations and take profit of new business opportunities. The proportion of installed HPP equipment in the dairy industry remains low when compared with other sectors of the food industry and this trend persisted during the last two years (Fig. 8). Even though cheese is by itself a safe and stable product, HPP can be a useful tool to improve the properties of some cheese types. Practical examples are the use of HPP by Italian companies to treat buffalo mozzarella cheese for export to Japan and by Spanish companies to extend the shelf life of fresh cheeses through the inactivation of lactic acid bacteria, moulds and yeasts (Jung & Tonello-Samson, 2018). 4.1. Overcoming limitations Combined strategies appear as a promising approach to optimise the effects of HPP on cheese properties. Among them, the combination of HPP with antimicrobials such as bacteriocins and, in the case of particular cheese types, the combination with mild heat treatments stand out. HPP treatments have been applied together with bacteriocins on two main purposes, the improvement of microbiological safety, by acting on bacterial pathogens, and the acceleration of ripening, by acting on starter LAB. The combination of HPP treatments at 300 or 500 MPa for 5 min on day 2 after manufacture with each of seven bacteriocinproducing (BP) strains of LAB to eliminate L. monocytogenes Scott A in model semi-hard cheese made from raw milk inoculated with

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s the pathogen at 4.8 log cfu mL1 showed to be synergistic (Arque et al., 2005b). Counts of L. monocytogenes on day 3 were 7.0 log cfu g1 in control cheese, 6.1e6.7 log cfu g1 in cheeses with BP-LAB, 6.1 log cfu g1 in 300 MPa cheese without BP-LAB, 3.8e5.4 log cfu g1 in 300 MPa cheeses with BP-LAB, 2.0 log cfu g1 in 500 MPa cheese without BP-LAB and 0.5e1.8 log cfu g1 in 500 MPa cheeses s et al., 2005b). The effect was less marked in with BP-LAB (Arque cheese made from raw milk inoculated with S. aureus at 4.9 log cfu mL1 and HPP-treated under the same conditions, with counts of the pathogen on day 3 of 6.5 log cfu g1 in control cheese, 6.0e6.3 log cfu g1 in cheeses with BP-LAB, 6.0 log cfu g1 in 300 MPa cheese without BP-LAB, 5.4e5.8 log cfu g1 in 300 MPa cheeses with BP-LAB, 4.0 log cfu g1 in 500 MPa cheese without BP-LAB and s et al., 2.5e3.1 log cfu g1 in 500 MPa cheeses with BP-LAB (Arque 2005a). In the case of E. coli O157:H7 inoculated at 4.9 log cfu mL1 in raw milk, from which model semi-hard cheese was manufactured and HPP-treated as described above, counts on day 3 were 6.8 log cfu g1 in control cheese, 6.1e6.4 log cfu g1 in cheeses with BPLAB, 5.5 log cfu g1 in 300 MPa cheese without BP-LAB, 3.4e4.8 log cfu g1 in 300 MPa cheeses with BP-LAB, 3.1 log cfu g1 in 500 MPa cheese without BP-LAB and 0.1e1.9 log cfu g1 in 500 MPa cheeses with BP-LAB (Rodríguez et al., 2005). These results were unexpected, since bacteriocins do not inhibit Gram-negative bacteria, and were explained as due to sublethal damage in the outer membrane that increased cell sensitivity to bacteriocins, as previously reported for the inactivation of E. coli O157:H7 suspended in peptone solution with added pediocin AcH and HPP-treated at 345 MPa (Kalchayanand, Sikes, Dunne, & Ray, 1998) and the inactivation of E. coli NCTC 9001 suspended in culture medium with added nisin and HPP-treated at 150e200 MPa (ter Steeg, Hellermons, & Kok, 1999). In the case of spore-forming bacteria, more resistant to HPP treatments than vegetative forms, combined strategies seem of particular interest. To this aim, HPP was combined with nisin addition for the inactivation of B. subtilis spores. However, cheese made from milk inoculated with B. subtilis spores at 5 log cfu mL1 and HPP-treated on day 1 at 500 MPa for 5 min had a spore count of 2.0 log cfu g1, cheese with nisin added at 7 ppm and HPP-treated or not a spore count of 0.9 log cfu g1, and control cheese a spore count of 2.9 log cfu g1 (Capellas et al., 2000). In model cheese made from milk inoculated with B. subtilis spores to reach 6 log cfu g1 in cheese, treatment at 300 or 400 MPa with or without 0.05 mg L1 nisin added to milk had no effect on spore counts while addition of 1.56 mg L1 nisin to milk lowered spore counts with respect to control cheese by 0.7 log units in cheese treated at 300 MPa, by 0.8 log units in cheese treated at 400 MPa, and by 0.2 pez-Pedemonte et al., 2003). log units in untreated cheese (Lo Germination and inactivation of B. subtilis spores suspended in milk HPP-treated at 500 MPa for 5 min at 40  C were enhanced by nisin addition at 500 IU mL1 in comparison with just the HPP treatment, germination by 2.2 log units and inactivation by 3.2 log units, and furthermore when nisin addition was combined with a double HPP cycle, germination by 3.8 log units and inactivation by 5.9 log units (Black et al., 2008). C. tyrobutyricum can be inactivated in cheese by HPP treatments, although the decrease in spore counts of 60-day cheese even if treated at 500 MPa only attained 0.6e0.8 log units, depending on  the strain, with respect to control cheese (Avila et al., 2016). On the other hand, antimicrobial compounds such as reuterin, nisin, lysozyme and sodium nitrite were active against C. tyrobutyricum, C butyricum, C. beijerinckii and C. sporogenes strains isolated from cheeses with late blowing defect, although spores were more  mezresistant to antimicrobials than vegetative cells (Avila, Go ndez, & Garde, 2014). It seems feasible to combine Torres, Herna

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Total installed HPP equipment by sectors (%) 2

3

6

1

23

7

Juices & Beverages Fruits & Vegetables Tolling Meat Products

19

Seafood R&D

21

RTE Foods Dairy Products Pet Food

18

Installed HPP equipment in 2017-2018 by sectors (%) 4

1

2

0 3

9

34

Juices & Beverages Fruits & Vegatables Tolling Meat Products Seafood R&D RTE Foods

Dairy Products 25

Pet Food 22

Fig. 8. Distribution (%) of total installed HPP equipment and HPP equipment installed in years 2017e2018 by food industry sectors (clockwise, starting with Juices & Beverages). Adapted from Hiperbaric (2019).

HPP of cheese with addition or in situ production of antimicrobials   ~ ez, 2011; Avila, in milk or cheese (Garde, Avila, Arias, Gaya, & Nun  mez-Torres, Delgado, Gaya, & Garde, 2017b) to achieve a more Go effective inactivation of Clostridium spp. spores. Combination of HPP with mild heat treatment has been suggested for the inactivation of pathogens and spoilage microorganisms in foods (Kalchayanand et al., 1998; Koseki et al., 2008; ter Steeg, Hellemons, & Kok, 1999). However, the temperatures, up to 35e50  C, used in those studies, which were carried out in culture media or in milk, preclude industrial application to most cheese types. Only stretched-curd cheeses or those cheese types including a curd heating step in their manufacturing process seem adequate for the use of mild temperatures in combination with HPP for cheese treatment. Cheese ripening may be accelerated by combining HPP treatnico cheeses made with a BP-LAB ments and bacteriocins. Hispa strain producing nisin Z and lacticin 481 and non-HPP-treated, made with the BP-LAB and HPP-treated at 400 MPa for 5 min, made without the BP-LAB and non-HPP-treated, and made without the BP-LAB and HPP-treated had on day 50 levels of hydrophobic peptides of 103.9, 129.5, 50.2 and 64.0 area units mg1, respectively,

levels of hydrophilic peptides of 197.0, 206.3, 70.6 and 86.5 area units mg1, respectively, FAA concentrations of 7.31, 7.21, 2.69 and 4.73 mg g 1, respectively, and taste intensity scores of 6.3, 6.5, 6.0  and 5.9, respectively (Avila et al., 2006b). Levels of most volatile compounds were considerably higher in cheeses made with the BP LAB, independently of the HPP treatment (Avila et al., 2006a). 4.2. Seizing opportunities Costs of HPP treatment have considerably decreased as larger vessels, of up to 525-L capacity, allowing for better volumetric efficiency and providing higher throughputs are nowadays available. Investment costs of $0.031 L-1 and processing costs of $0.107 L-1 were estimated for fluid products at a production rate of 16,500,000 L year1 (Sampedro, McAloon, Yee, Fan, & Geveke, 2014). In the case of solid products, processing costs as low as V0.064 kg1 can be attained by means of 525-L vessels (Jung & Tonello-Samson, 2018). Despite these facts, cheese plants may be doubtful about the cost effectiveness of installing HPP equipment at their facilities to be used exclusively for the treatment of their products. Production of many cheese types, particularly those made

~ez et al. / International Dairy Journal 100 (2020) 104558 M. Nun

from ewe and goat milk, suffers seasonal variations because of the seasonal production of milk by small ruminants. Arresting or accelerating the ripening process may be of interest for those cheese types to overcome seasonal fluctuations of production. This would result in periods of the year with low or zero workload, which could be filled by processing other foodstuffs of noncoincident seasonality. Also, a considerable proportion of recently installed HPP equipment (Fig. 8) works under a tolling service regime that would permit HPP treatment of cheeses with seasonal variations in production. An alternative procedure to circumvent the seasonal production of cheeses including ewe and/or goat milk in their composition is the HPP treatment of curd made from raw milk in the period of maximum milk production followed by frozen storage of the curd until needed. To this aim, curd made from raw ewe milk in spring months was HPP-treated at 400 or 500 MPa for 10 min at 12  C, frozen for 120 days and used for the manufacture of Hisp anico cheese by mixing them (20:80) with curd recently made from n, Gaya, Fern pasteurised cow milk (Alonso, Pico andez-García, & ~ ez, 2011). The microbiological quality of experimental cheeses Nun was similar to that of control cheese made from a mixture of pasteurised cow and ewe milk. On day 1 after manufacture, aminopeptidase activity in cheeses including curd treated at 400 or 500 MPa was 155% and 87%, respectively, higher than in control cheese and esterase activity 81% and 44% higher, respectively. On day 60 in cheeses including curd treated at 400 or 500 MPa relative to control cheese, hydrophilic peptides were 24% and 21% higher, hydrophobic peptides 27% and 20% higher and FAAs 61% and 69% higher. Compared with control cheese, FFAs were 8% higher in cheeses made with curd treated at 400 MPa and 23% lower in cheeses made with curd treated at 500 MPa. Differences in the volatile fraction of experimental and control cheeses were partly attributed to the production of volatile compounds by wild LAB strains that had survived the HPP treatment of curd. The texture of experimental cheeses was less firm and elastic than that of control cheese. There were no significant differences in flavour intensity, flavour preference, umami taste or bitter taste scores between experimental and control cheeses throughout ripening (Alonso et al., 2011). In a similar study, experimental cheeses were manufactured using curd made from raw goat milk in spring months, which was HPP-treated at 400 MPa for 10 min at 14  C, frozen for 120 days and mixed (30:70) with curd recently made from pasteurised cow milk ~ ez, 2013). The microbiological quality of (Picon, Alonso, Gaya, & Nun experimental cheese was similar to that of control cheese made from a mixture of pasteurised cow and goat milk. On day 1 after manufacture, aminopeptidase activity was similar in cheese made with curd treated at 400 MPa and in control cheese but esterase activity was 3.9-fold higher in experimental cheese, probably coming from the HPP-treated goat milk curd. On day 60, hydrophilic and hydrophobic peptides were similar in experimental and control cheeses while FAAs were 22% higher in experimental cheese. Regarding lipolysis, short chain-FFAs and medium chainFFAs were similar in experimental and control cheeses but long chain-FFAs were 11% lower in experimental cheese. Volatile compounds 1-methoxy-2-propanol, cyclohexanol and 2,3-butanedone were at levels 3.1-, 3.3- and 2-3-fold higher, respectively, in experimental cheese than in control cheese on day 60. Experimental cheese had a less firm and elastic texture than control cheese. Flavour intensity and acidic, bitter, salty and umami taste scores were similar for experimental and control cheeses on day 60 while flavour preference score was higher for experimental cheese than for control cheese (Picon et al., 2013). Reduction of the allergenicity caused by bovine milk proteins offers another opportunity for the application of HPP treatment to

19

cheese. Caseins, including aS1-, aS2-, b- and k-casein, are known to contain different allergens of molecular mass ranging from 19.0 to 25.2 kDa while whey proteins, including a-lactalbumin, b-lactoglobulin, bovine serum albumin, immunoglobulins and lactoferrin, contain allergens of molecular mass ranging from 14.2 to 160 kDa (Villa, Costa, Oliveira, & Mafra, 2018). The practical totality of caseins is retained in the curd while most of whey proteins are drained off with the whey in conventional cheese making, although whey proteins are incorporated into the curd when procedures such as milk ultrafiltration are included in the manufacturing process. Bovine milk allergy is common in early childhood and, if persisting in adults, precludes consumption of cheese and cheesecontaining foods. HPP treatments alter the tertiary and quaternary structure of milk proteins, with unfolding phenomena which may cause the exposure of hidden epitopes, thus increasing allergenicity, and aggregation phenomena, which may increase reactivity by revealing determinants absent in monomers (Huang, Hsu, Yang, & Wang, 2014). Thus, b-lactoglobulin antigenicity increased when suspended in solutions that were HPP-treated at 200e600 MPa (Kleber, Maier, & Hinrichs, 2007). On the other hand, the Ig-E binding capacity of the enzymatic hydrolysis products of b-lactoglobulin decreased by up to 76% when the hydrolysis with chymotrypsin was combined with HPP at 400 MPa for 20 min at   n, Belloque, Alonso, Martín-Alvarez, pez37e45  C (Chico & Lo ~ o, 2008). Fandin Similar results of decreased Ig-E binding capacity were obtained for different milk proteins when trypsin and chymotrypsin hydrolysis was combined with HPP treatment at 500 MPa for 30 min at 40  C (Beran et al., 2009). The combination of high pressure treatments with enzymatic hydrolysis of whey proteins can be used for the preparation of hypoallergenic foods with improved nutritional and sensory properties (Barba, Terefe, Buckow, Knorr, & Orlien, 2015). However, to our knowledge there is no information available on the effect of HPP treatments on the allergenicity of proteins and their hydrolysis products in cheese generated during ripening by the enzymatic activity of coagulant enzymes and starter culture proteinases. 5. Conclusions From the results reported in the papers considered in this review, HPP appears as a reliable tool for the assurance of cheese microbiological quality and the prevention of defects of microbiological origin. Process parameters commonly used in the food industry suffice to guarantee the elimination of undesirable microorganisms and, by the use of combined strategies, even of fastidious bacteria such as spore-formers. HPP treatment of cheese aiming to satisfy microbiological quality objectives has concomitant effects on the biochemical, textural and sensory properties of cheese, a fact that should be carefully taken into account. Different cheese types show different responses to HPP and, consequently, treatment conditions must be selected on a case by case basis. Mild or severe HPP parameters may serve to accelerate or arrest the biochemical processes occurring during cheese ripening, which can be useful to overcome seasonal shortages or surpluses of production. Although some cheese types, particularly mould-ripened varieties, cannot be subjected to HPP treatment because of alterations in their visual appearance, many fresh, soft and semi-hard cheese varieties can considerably benefit from HPP if aiming for the extension of their shelf life. Modern equipment with vessels of larger capacity has made HPP treatments more affordable for the dairy industry. Even with the increase in the available information on the subject, cheese HPP still offers attractive research and business opportunities.

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Acknowledgements ~ ez and J. Calzada wish to acknowledge courage Authors M. Nun and companionship from Ana del Olmo during the preparation of this review. References Alberghini, L., Tallone, G., & Giaccone, V. (2010). A new discoloration of Ricotta cheese. Italian Journal of Food Safety, 8, 7e10. ~es, R., Carneiro, L., Santos, I., Silva, J., Ferreira, V., et al. (2013). Almeida, G., Magalha Foci of contamination of Listeria monocytogenes in different cheese processing plants. International Journal of Food Microbiology, 167, 303e309. n, A., Gaya, P., Ferna ndez-García, E., & Nun ~ ez, M. (2011). MicrobioAlonso, R., Pico logical, chemical, and sensory characteristics of Hisp anico cheese manufactured using frozen high pressure treated curds made from raw ovine milk. International Dairy Journal, 21, 484e492. Andreani, N. A., Carraro, L., Martino, M. E., Fondi, M., Fasolato, L., Miotto, G., et al. (2015). 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~ez et al. / International Dairy Journal 100 (2020) 104558 M. Nun Costabel, L. M., Bergamini, C., Vaudagna, S. R., Cuatrin, A. L., Audero, G., & Hynes, E. (2016). Effect of high-pressure treatment on hard cheese proteolysis. Journal of Dairy Science, 99, 4220e4232. Costard, S., Espejo, L., Groenendaal, H., & Zagmutt, F. J. (2017). Outbreak-related disease burden associated with consumption of unpasteurized cow's milk and cheese, United States, 2009e2014. Emerging Infectious Diseases, 23, 957e964. Daryaei, H., Coventry, M. J., Versteeg, C., & Sherkat, F. (2006). Effects of highpressure treatment on shelf life and quality of fresh lactic curd cheese. Australian Journal of Dairy Technology, 61, 186e188. Daryaei, H., Coventry, M. J., Versteeg, C., & Sherkat, F. (2008). Effect of high pressure treatment on starter bacteria and spoilage yeasts in fresh lactic curd cheese of bovine milk. Innovative Food Science & Emerging Technologies, 9, 201e205. Daryaei, H., Coventry, M. J., Versteeg, C., & Sherkat, F. (2010). Effect of high pressure treatment on glycolytic enzymes of Lactococcus lactis subsp. lactis, Streptococcus thermophilus and Lactobacillus acidophilus. Innovative Food Science & Emerging Technologies, 11, 245e249. Davey, J. A., & Eyles, M. J. (1992). Discoloration of cottage cheese caused by Rahnella aquatilis in the presence of glucono-d-lactone. Australian Journal of Dairy Technology, 47, 62e63 & 82. pez-Pedemonte, T., Hern De Lamo-Castellví, S., Capellas, M., Lo andez-Herrero, M. M., s, A. X. (2005). Behavior of Yersinia enterocolitica Guamis, B., & Roig-Sague strains inoculated in model cheese treated with high hydrostatic pressure. Journal of Food Protection, 68, 528e533. s, A. X., Lo  pez-Pedemonte, T., De Lamo-Castellví, S., Capellas, M., Roig-Sague ndez-Herrero, M. M., & Guamis, B. (2006). Fate of Escherichia coli strains Herna inoculated in model cheese elaborated with or without starter and treated by high hydrostatic pressure. Journal of Food Protection, 69, 2856e2864. s, A. X., Lo pez-Pedemonte, T., Herna ndezDe Lamo-Castellví, S., Roig-Sague Herrero, M. M., Guamis, B., & Capellas, M. (2007). Response of two Salmonella enterica strains inoculated in model cheese treated with high hydrostatic pressure. Journal of Dairy Science, 90, 99e109. Delgado-Martínez, F. J., Carrapiso, A. I., Contador, R., & Ramírez, R. (2019). Volatile compounds and sensory changes after high pressure processing of mature “Torta del Casar” (raw Ewe's milk cheese) during refrigerated storage. Innovative Food Science & Emerging Technologies, 52, 34e41. Delgado, F. J., Delgado, J., Gonz alez-Crespo, J., Cava, R., & Ramírez, R. (2013). Highpressure processing of a raw milk cheese improved its food safety maintaining the sensory quality. Food Science and Technology International, 19, 493e501. lez-Crespo, J., Cava, R., & Ramírez, R. (2011). Changes in the Delgado, F. J., Gonza volatile profile of a raw goat milk cheese treated by hydrostatic high pressure at different stages of maturation. International Dairy Journal, 21, 135e141. lez-Crespo, J., Cava, R., & Ramírez, R. (2012a). Changes in Delgado, F. J., Gonza microbiology, proteolysis, texture and sensory characteristics of raw goat milk cheeses treated by high-pressure at different stages of maturation. Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology, 48, 268e275. lez-Crespo, J., Cava, R., & Ramírez, R. (2012b). High-pressure Delgado, F. J., Gonza treatment applied throughout ripening of a goat cheese caused minimal changes on free fatty acids content and oxidation in mature cheese. Dairy Science & Technology, 92, 237e248. Delgado, F. J., Rodríguez-Pinilla, J., M arquez, G., Roa, I., & Ramírez, R. (2015). Physicochemical, proteolysis and texture changes during the storage of a mature soft cheese treated by high-pressure hydrostatic. European Food Research and Technology, 240, 1167e1176. ~ ez, M. (2018). The blue discoloration of fresh cheeses: del Olmo, A., Calzada, J., & Nun A worldwide defect associated to specific bacterial contamination. Food Control, 86, 359e366. Dijksterhuis, J., & Teunissen, P. G. M. (2004). Dormant ascospores of Talaromyces macrosporus are activated to germinate after treatment with ultra high pressure. Journal of Applied Microbiology, 96, 162e169. Dupont, K., Janzen, T., Vogensen, F. K., Josephsen, J., & Stuer-Lauridsen, B. (2004). Identification of Lactococcus lactis genes required for bacteriophage adsorption. Applied and Environmental Microbiology, 70, 5825e5832. Dur~ aes-Carvalho, R., Souza, A. R., Martins, L. M., Sprogis, A. C. S., Bispo, J. A. C., Bonafe, C. F. S., et al. (2012). Effect of high hydrostatic pressure on Aeromonas hydrophila AH 191 growth in milk. Journal of Food Science, 77, M417eM424. ndez-Herrero, M. M., & Roig-Xague s, A. X. (2018). Espinosa-Pesqueira, D., Herna High hydrostatic pressure as a tool to reduce formation of biogenic amines in artisanal Spanish cheeses. Foods, 7. article 137. Evelyn, & Silva, F. V. M. (2015). High pressure processing of milk: Modeling the inactivation of psychrotrophic Bacillus cereus spores at 38e70  C. Journal of Food Engineering, 165, 141e148. n, J. J., Juan, B., & Evert-Arriagada, K., Hern andez-Herrero, M. M., Gallardo-Chaco Trujillo, A. J. (2013). Effect of high pressure processing on volatile compound profile of a starter-free fresh cheese. Innovative Food Science & Emerging Technologies, 19, 73e78. Evert-Arriagada, K., Hern andez-Herrero, M. M., Guamis, B., & Trujillo, A. J. (2014). Commercial application of high-pressure processing for increasing starter-free fresh cheese shelf-life. Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology, 55, 498e505. Evert-Arriagada, K., Hern andez-Herrero, M. M., Juan, B., Guamis, B., & Trujillo, A. J. (2012). Effect of high pressure on fresh cheese shelf-life. Journal of Food Engineering, 110, 248e253.

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