Trends in Food Science & Technology 88 (2019) 143–156

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Trends in Food Science & Technology

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Review Heat assisted HPP for the inactivation of bacteria, moulds and yeasts spores in foods: Log reductions and mathematical models T

∗∗ ∗ Evelyna, , Filipa V.M. Silvab,c, a Department of Chemical Engineering, University of Riau, Pekanbaru 28293, Indonesia b Department of Chemical and Materials Engineering, University of Auckland Private Bag 92019, Auckland 1142, New Zealand c LEAF, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal

ARTICLE INFO ABSTRACT

Keywords: Background: Food contamination by pathogenic and spoilage spore-formers is a concern. As opposed to ster- High pressure thermal processing ilization, spores can survive pasteurization processes. Pasteurization of foods require at least 5–6 log reduction of Spore-former the key pathogenic or spoilage microorganism. Traditional thermal processing at high temperature can achieve Pathogenic this reduction; however, it could diminish food quality. High pressure processing (HPP) is a non-thermal food Spoilage pasteurization technology used in the food industry, which is able to better retain the natural flavors and nu- Mathematical model trients of the foods. For the inactivation of specific spore-formers the combination of HPP with heat is required: high pressure thermal processing (HPTP) or HPP-thermal. Scope and approach: The up-to-date knowledge on the effect of HPP and HPTP on the spores of pathogenic and spoilage sporulating microorganisms in low- and high-acidic foods is provided, including the kinetic models used to describe their inactivation in specific foods. Key findings and conclusions: HPTP is required for the inactivation of bacterial spores in foods. Certain species of heat-resistant mould ascospores in high-acid fruit juices/purees have comparable resistance to bacterial spores, and also require HPTP. Due to the effects of food type on spore resistances, testing the most resistant spores in specific foods should be carried out before using it as a target/reference for designing new pasteurization processes. Yeasts spores are the least resistant, and susceptible to room temperature HPP. Most of the HPTP inactivation kinetics of bacterial and resistant mould spores showed non-linear trends, thus the resulting pas- teurization should be interpreted with more care.

1. HPP as an established technology for the pasteurization of non-thermal pasteurization of foods through the inactivation of pa- foods thogenic and spoilage microorganisms (usually by 5 or 6 log reduc- tions) followed by cold storage and distribution. The shelf-life of HPP- 1.1. HPP fundamentals processed foods is mainly influenced by the pressure level, holding time, storage conditions, and other factors such as packaging char- High pressure processing (HPP) is a non-thermal pasteurization acteristics. These foods typically have a shelf-life 3–10 times that of technology. It causes less adverse effects on food quality than conven- untreated foods (Hiperbaric, 2015). Juices, smoothies, jams and sauces tional thermal processes (Lee & Oey, 2018; Sánchez-Moreno & De made from fruits, yogurt, jelly, guacamole, dips, salsas, ready-to-eat Ancos, 2018). Industrial HPP typically operates at pressures of meals, meat and poultry products, and seafood are examples of com- 400–600 MPa, to treat liquid and solid foods for processing times be- mercially available HPP processed food products worldwide. These tween 5 and 10 min. According to Le Chatelier's principle, hydrostatic manufacturers are located mainly in Japan, the United States, and pressure reduces the volume of the pressurized material homo- Europe (Hogan, Kelly, & Sun, 2005; Houška & Pravda, 2018). geneously. As covalent bonds are not broken by pressure (Mozhaev, An example of the pressure–temperature (P-T) history of a HPTP Heremans, Frank, Masson, & Balny, 1994), the original food compo- process at 600 MPa and 70 °C for 5 min, showing the 3 phases of the nents remain unchanged with the process. The main goal of HPP is the process cycle (pressurization, constant pressure, and depressurization)

∗ Corresponding author. LEAF, Instituto Superior de Agronomia, Universidade de Lisboa, Portugal. ∗∗ Corresponding author. E-mail addresses: [email protected] (Evelyn), fi[email protected] (F.V.M. Silva). https://doi.org/10.1016/j.tifs.2019.03.016 Received 18 October 2018; Received in revised form 15 February 2019; Accepted 18 March 2019 Available online 21 March 2019 0924-2244/ © 2019 Elsevier Ltd. All rights reserved. Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Fig. 1. An example of the pressure and temperature (P–T) history of a HPTP process at 600 MPa and 70 °C for 5 min. is illustrated in Fig. 1. During the pressurization phase, the temperature pressure of HPTP synergistically enhance microbial spore inactivation increased adiabatically from 58.7 °C to 77.3 °C. The faster the pressur- (Evelyn & Silva, 2015b, 2015c, 2016a, 2016b; Daryaei, ization, the greater the temperature increase during this phase. During Balasubramaniam, & Legan, 2013; Evelyn, Kim, & Silva, 2016; Evelyn, the 5 min of constant-pressure treatment, a small decrease in the tem- Milani, & Silva, 2017; Silva, Tan, & Farid, 2012). Also, the resistance of perature was observed. Due to the temperature changes along the HPP spores varies significantly among species and is affected by the food process, the average temperature during the constant pressure phase of matrix. Until now, considerable efforts have been made to achieve the the HPP cycle is often considered as the processing temperature, and total inactivation of microbial spores by HPTP and the production of was therefore used in this review to compile the literature results of the shelf-stable sterilized food products of high quality, comparable to effect of HPTP on spore inactivation. canned foods. A lab-scale attempt of the pressure-enhanced sterilization of Clostridium botulinum spores in low-acid foods has been made by the Illinois Institute of Technology's Institute for Food Safety and Health 1.2. Effect of HPP on microbial spores in foods (IIT IFSH) and received FDA acceptance (IIT-IFSH, 2015). However, the operational challenges and costs of scale-up to an industrial level are Spores are highly resistant dormant structures formed from vege- some of the main factors holding back HPTP from commercial appli- tative cells which are different from their vegetative cell counterparts in cations. In the following sections, the effect of HPP alone and HPTP on chemical composition, morphological structure, and physiology the log reductions of spores in low-acid and high-acid foods was re- (Keynan, 1969). Spores develop when nutrients and moisture are lim- viewed. ited, enabling their survival for prolonged periods under various ex- treme environmental conditions. A spore may break its dormancy through germination induced by nutrients and non-nutrients agents and 2. HPP and HPTP inactivation of pathogenic bacterial spore- outgrowth back to its vegetative state when favorable conditions are formers in low-acid foods (pH > 4.6) reestablished (e.g., water and nutrients). Sub-lethal heating of spores has also been known to stimulate the spore germination. Food spoilage 2.1. Pathogenic bacterial spore-formers can occur due to the outgrowth of contaminating microbial spores in foods. When the microbe is a pathogen, foodborne illnesses and out- Bacterial spores are the most resistant, compared to mould and breaks can also result. Certain bacteria, moulds, and yeasts are able to yeast spores, and have the highest potential for outgrowth to toxin produce spores, although the spores made by fungi are biologically producing cells that cause foodborne illnesses and outbreaks. Thus, they different from those made by bacteria. Apart from their function for are frequently the target of food pasteurization and sterilization pro- survival, most fungi produce spores as part of their reproductive cycles. cesses (Evelyn & Silva, 2018a). The most dangerous spore-former in For the majority of microbial spores (Sarker, Akhtar, Torres, & low-acid foods is Clostridium botulinum (Carlin et al., 2000a; Gould, Paredes-Sabja, 2013; Wilson, Dabrowski, Stringer, Moezelaar, & 1999). It can produce potent and fatal neurointoxication (Brown, 2000) Brocklehurst, 2008) and enzymes (Hendrickx, Ludikhuyze, Van den and C. botulinum types A, B, E, and F have been implicated in human Broeck, & Weemaes, 1998; Sulaiman, Soo, Yoon, Farid, & Silva, 2015), foodborne botulism cases according to the U. S. Food and Drug Ad- non-thermal HPP treatment (room temperature) does not inactivate ministration (FDA, 2001). Incidents from ingestion of contaminated them. For example, Bacillus subtilis spores were found to survive pro- hot-smoked fish, canned tuna in oil, canned truffle cream, canned as- cessing conditions up to 1200 MPa at ambient temperature (Larson, paragus, pasteurized vegetables in oil, canned fish, and canned eggplant Hartzell, & Diehl, 1918). Therefore, in addition to cold-chain manage- have been reported (Aureli, Fenica, & Franciosa, 1999; Lindström, ment, heat-assisted HPP (HPTP – high pressure thermal processing) Kiviniemi, & Korkeala, 2006; Mongiardo et al., 1985; Pace, Krumbiegel, with temperatures higher than 50 °C are required for the inactivation of Angelotti, & Wisniewski, 1967; Peredkov, 2004; Przybylska, 2003; resistant spore-formers. Studies have shown that temperature and Therre, 1999).

144 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Clostridium perfringens and Bacillus cereus are two other pathogenic and temperatures of 60 °C–85 °C or higher are required for the in- spore-formers in low-acid foods. Food outbreaks in ready-to-eat and activation of pathogenic Bacillus spores. Similar to Ju, Gao, Yao, and partially cooked meat and poultry products due to improper handling Qian (2008) (540 MPa, 71 °C, and 17 min), Van Opstal, Bagamboula, and preparation of large quantities of the foods have often been re- Vanmuysen, Wuytack, and Michiels (2004) reported > 5 log spore in- ported in association with C. perfringens enterotoxin (Evelyn & Silva, activation for four strains of B. cereus in milk after 500 MPa, 60 °C, and 2015a, 2016a; Labbé & Juneja, 2013; Silva & Gibbs, 2009). Symptoms 15 min. Evelyn and Silva (2015b, 2016b) obtained 3.0–4.6 log reduc- are typically reported after 8–24 h of food ingestion. A large numbers of tions of two strains of B. cereus spores in skim milk and beef slurry after vegetative cells present in the temperature-abused foods is followed by 600 MPa, 70 °C, and 15 min. Scurrah, Robertson, Craven, Pearce, and sporulation in the human gastrointestinal tract, resulting in diarrhea Szabo (2006) and Robertson, Carrol, and Pierce (2008) obtained (Labbé & Juneja, 2013). The United Kingdom and several other coun- 3.8–4.5 log reductions of five B. cereus strains in skim milk after tries such as Australia and Japan have listed this bacterium as the 600 MPa, initial temperature of 72–75 °C, and 1 min, except for strain leading cause of foodborne disease outbreaks (Grass, Gould, & Mahon, FRR B2603 with 6 log. Scurrah et al. (2006) also demonstrated differ- 2013). Outbreaks in spinach and a fried bean curd dish were also re- ences in the resistance of nine strains of B. licheniformis (1.6–4.3 log) ported with this species (Miwa et al., 1999). Similar to C. perfringens, B. and six strains of B. pumilus (1.8–4.7 log) spores in skim milk after the cereus is often detected in meat and in dishes containing meat, resulting same treatment of 600 MPa, initial temperature of 72 °C, and 1 min. A in food poisoning. Diarrhea and emetic syndromes are two types of wide range of inactivation of six strains of B. licheniformis (< 2.0–5.0 diseases caused by B. cereus (Schoeni & Lee Wong, 2005). Other food log) and six strains of B. pumilus in skim milk was observed by commodities commonly containing B. cereus are rice, cereals, and Robertson, Carroll, and Pearce (2008). These results suggest that spe- spices. Some strains of this species have frequently been isolated from cies and strain, play a significant role in Bacillus spore resistance to low-acid chilled foods, generally dairy-based, (Carlin et al., 2000b; HPTP. Thus, investigating the most resistant spores for each spe- Dufrenne, Bijwaard, Te Giffel, Beumer, & Notermans, 1995; Silva & cies–food combination is necessary to ensure food safety and quality. Gibbs, 2010; Silva, Gibbs, Nunez, Almonacid, & Simpson, 2014) due For B. cereus, seven log reductions were achieved after 600 MPa–85 °C-4 their ability to grow at low temperatures (T < 8 °C) (Choma et al., min treatment in cooked rice (Daryaei et al., 2013). A treatment of 2000; Dufrenne et al., 1995; García Armesto & Sutherland, 1997). 600 MPa–initial temperature of 80 °C and 16 min caused > 7.0 log re- The following spore-forming bacteria have also been reported in ductions for B. licheniformis in mashed carrot (Margosch, Gänzle, low-acid foods and cause diseases and typical foodborne infection Ehrmann, & Vogel, 2004b), suggesting that HPP at higher temperature symptoms in humans: Bacillus licheniformis, Bacillus pumilus, Bacillus resulted in more lethal effect to the Bacillus spores. According to thuringiensis, Bacillus anthracis, Clostridium baratii and Clostridium bu- Reineke et al. (2012), above a threshold pressure which is 600 MPa for tyricum in infants, and Clostridium difficile (Aureli et al., 1986; Barash, Bacillus spores, the process temperature dominates the inactivation Tang, & Arnon, 2005; CDC, 2000; Hormazabal & Granum, 2007; rate. Jackson, Goodbrand, Ahmed, & Kasatiya, 1995; Pavic et al., 2005; Rupnik & Songer, 2010; Salkinoja-Salonen et al., 1999). Among them, 3. HPP and HPTP inactivation of spoilage bacterial spore-formers B. licheniformis and B. pumilus are the two most common species found in low-acid (pH > 4.6) and high-acid (pH < 4.6) foods in low-acid manufactured foods (Oomes et al., 2007). 3.1. Spoilage bacterial spore-formers 2.2. Log reductions of Clostridium spores Spoilage spore-formers from the Bacillus and Clostridium genera Table 1 shows the spore log reductions obtained for pathogenic commonly found in low-acid foods (pH > 4.6) are B. subtilis, Clostridium spores in low-acid food products after high pressure in the Geobacillus stearothermophilus, Bacillus coagulans, Bacillus sphaericus, range of 345–900 MPa, combined with temperatures of 60 °C–110 °C. Bacillus circulans, Bacillus sporothermodurans, Bacillus mycoides, Bacillus Regarding C. botulinum, HPTP at 900 MPa–110 °C–0.8 min and HPTP at megaterium, Bacillus macerans, Clostridium sporogenes, Clostridium tyr- 827 MPa–84 °C–15 min were not sufficient to inactivate a few strains of obutyricum, Clostridium beijerinckii, Clostridium frigidicarnis, Clostridium these species (≤2.0 log) (Ramaswamy, Shao, Bussey, & Austin, 2013; esterheticum, Clostridium laramie, and Clostridium gasigenes (Adam, Flint, Reddy, Tetzloff, Solomon, & Larkin, 2006), indicating high resistance to & Brightwell, 2010; Cosentino, Mulargia, Pisano, Tuveri, & Palmas, the HPTP treatments. With respect to C. perfringens, the same low in- 1997; Garde, Ávila, Gómez, & Nuñez, 2013; Ledenbach & Marshall, activation (≤2.0 log) was obtained with two strains processed at 2009; Oomes et al., 2007; Scheldeman, Herman, Foster, & Heyndrickx, 600 MPa–75 °C–15 min (Evelyn & Silva, 2016a). Some Clostridium 2006). Meat and dairy products have been associated with these spore- strains showed ≥5.0 log reductions after HPTP treatments formers. With respect to C. sporogenes spores, their high pressure- (600–900 MPa, 80–110 °C, 0.8–16 min). Other results showed modest thermal resistance and similar physiological properties to C. botulinum Clostridium spore reductions in foods (2.0–4.1 log) after high pressures have made this microbial species an important surrogate organism for at 600–900 MPa combined with temperatures of 75–110 °C or initial HPTP inactivation studies (Koutchma, Guo, Patazc;a, & Parisi, 2005; temperature of 80 °C for 0.8–16 min (Margosch, Ehrmann, Gänzle, & Ramaswamy & Shao, 2010; Ramaswamy, Shao, & Zhu, 2010; Shao, Vogel, 2004a; Ramaswamy et al., 2013; Reddy, Solomon, Tetzloff,& Zhu, Ramaswamy, & Marcotte, 2010; Zhu, Naim, Marcotte, Rhodehamel, 2003). Kalchayanand, Dunne, Sikes, and Ray (2003) ob- Ramaswamy, & Shao, 2008). tained almost no spore reductions of C. perfringens in roast beef (0.4 log) Spoilage problems, along with the subsequent major economic after 345 MPa–60 °C–5 min. Overall, bacterial spores from the genus losses can occur in high-acid and acidified foods (pH < 4.6) due to Clostridium, have the highest degree of resistance to high pressure with contamination with the spore-forming bacterium Alicyclobacillus acid- thermal processing (HPTP). oterrestris (Cerny, Duong, Hennlich, & Miller, 2000; Jay, 2000; Silva & Evelyn, 2018). The optimum pH for A. acidoterrestris growth is between 2.3. Log reductions of Bacillus spores 3.5 and 4.5 (Pinhatti, Variane, Eguchi, & Manilla, 1997) and the op- timum growth temperature is between 35 and 53 °C (Deinhard, Blanz, Room temperature HPP at 400–600 MPa for 10–15 min resulted Poralla, & Altan, 1987; Sinigaglia et al., 2003). Aseptically packaged in < 1.0 log reduction of B. cereus spores (Lopez-Pedemonte, Roig- apple juice, canned diced tomatoes, carbonated fruit juice drinks, fruit Sagués, Trujillo, Capellas, & Guamis, 2003; McClements, Patterson, & pulps, isotonic water, lemonade, and shelf-stable ice tea containing Linton, 2001; Shigehisa, Ohmori, Saito, Taji, & Hayashi, 1991), there- berry juice are among the foods linked to A. acidoterrestris spore spoi- fore most studies used HPTP (Table 1). Generally, at least 500–600 MPa lage (Cerny et al., 1984; Duong & Jensen, 2000; Pettipher &

145 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 1 Inactivation of pathogenic Clostridium and Bacillus spores in low-acid foods by HPTP and HPP alone.

Spores Strains Food products pH Pressure Processing Holding Log reduction Reference (MPa) temp. (°C)a time (min)

Clostridium botulinum Proteolytic type B PA9508B Milk > 4.6 900 110 0.8 1.8 Ramaswamy et al. (2013) type A HO9504A 3.5 type A CK2-A 5.0

Proteolytic type A 62-A Crabmeat blend > 4.6 827 86 15 2.7 Reddy et al. (2003) BS-A 3.0

Non proteolytic type B 2B Crabmeat blend 7.2–7.4 827 84 15 < 1.0 Reddy et al. (2006) 17B 1.6 KAP9-B 2.0 KAP8-B > 5.5

Proteolytic type B TMW 2.357 Mashed carrot 5.2 600 80b 16 1.2 Margosch et al. (2004a) type A TMW 2.356 2.6 type B TMW 2.359 2.6 type F TMW 2.358 4.1 type A ATCC 19397 > 5.5 Non proteolytic type B ATCC 25765 > 5.5

Clostridium perfringens NZRM 2621 (ATCC 12917) Beef slurry 6.5 600 75 15 1.5 Evelyn and Silva (2016a) NZRM 898 (ATCC 14809) 2.0

1027 Roast beef > 4.6 345 60 5 0.4 Kalchayanand et al. (2003)

Bacillus cereus ATCC 9818 Cooked rice 6.0 600 85 4 7.0 Daryaei et al. (2013)

NZ 6 Skim milk > 4.6 600 85 1 3.8 Robertson et al. (2008) NZ 5 3.9 NZ 4 (NCTC 8035) 4.2 NZ 3 4.4 NZ 7 4.5

NZ 4 (NCTC 8035) Skim milk > 4.6 600 72b 1 4.1 Scurrah et al. (2006) NZ 6 4.3 NZ 3/NZ 5/NZ 7 4.4 FRR B2603 6.1

NZRM 984 (ATCC 11778) Skim milk > 4.6 600 70 15 3.0 Evelyn and Silva (2015b) ICMP 12442 (ATCC 9139) 3.5

ICMP 12442 (ATCC 9139) Beef slurry 6.5 600 70 15 4.6 Evelyn and Silva (2016b)

As 1.1846 Milk buffer 7.0 540 71 17 6.0 Ju et al. (2008)

LMG 6910 (ATCC 7004) Milk 6.7 500 60 15 5.4 Van Opstal et al. (2004) INRAAV P21S 5.6 INRAAV Z4222 5.6 INRAAV TZ415 6.6

nr Pork slurry > 4.6 600 Room T 10 < 1.0 Shigehisa et al. (1991)

NCFB 578 Milk > 4.6 400 Room T 15 < 0.5 McClements et al. (2001)

NCFB 1031 < 0.5

ATCC 9139 Cheese 5.5 400 Room T 15 < 0.5 Lopez-Pedemonte et al. (2003)

Bacillus licheniformis NZ 23/NZ 24 Skim milk > 4.6 600 85 1 < 2.0 Robertson et al. (2008) NZ 25 2.0 NZ 22 3.0 NZ 21 (NCTC 6346) 3.2

TMW 2.492 Mashed carrot 5.2 600 80b 16 > 7.0 Margosch et al. (2004b)

(continued on next page)

146 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 1 (continued)

Spores Strains Food products pH Pressure Processing Holding Log reduction Reference (MPa) temp. (°C)a time (min)

NZ 23/Werribee 260 Skim milk > 4.6 600 72b 1 1.6 Scurrah et al. (2006) NZ 24/NZ 25 2.0 FRR B2653 (ATCC 9789) 2.6 NZ 22 2.7 NZ 21(NCTC 6346) 3.4 Werribee 229 3.6 Werribee 207 4.3

Bacillus pumilus NZ 31/NZ 33 Skim milk > 4.6 600 85 1 < 2.0 Robertson et al. (2008) NZ 27/NZ 32 (NCTC 10327) < 3.0 NZ 29 4.0 NZ 28 < 5.0

NZ 33 Skim milk > 4.6 600 72b 1 1.8 Scurrah et al. (2006) NZ 32 (NCTC 10327) 2.9 NZ 27 3.5 NZ 31 3.7 NZ 29 4.3 NZ 28 4.7

a Processing temperature was the average temperature during the constant pressure phase of the HPP cycle. b Initial temperature before compression; Room T = Room temperature HPP, T less or equal to 45 °C.

Osmundson, 2000; Walls & Chuyate, 1998). of temperature before compression (Scurrah et al., 2006). The variation Although not a common problem, the growth of spoilage spore- of results of the different strains within the same species is in agreement forming Bacillus and Clostridium have been reported in tomato, pear, with the previous results obtained with pathogenic spores. B. circulans peach, mango, mandarin, and orange fruit pulps and drinks, with pH appeared to be the least resistant species presenting 4.2–5.2 log re- values between 3.7 and 4.5. These organisms include B. coagulans, B. ductions for the same treatment (Scurrah et al., 2006). Surprisingly, the licheniformis, B. subtilis, Bacillus macerans, B. megaterium, Bacillus poly- high temperature (116 °C) used by Wang et al. (2009) combined with myxa, C. butyricum, C. tyrobutyricum, and Clostridium pasteurianum similar pressures attempted in most studies (600 MPa) for 15 min re- (Azizi & Ranganna, 1993; De-Jong, 1989; Everis & Betts, 2001; Gibriel sulted in only 4.6 log reductions of B. coagulans spores in milk, con- & Abd-El Al, 1973; Ikeyami, Okaya, Samayama, Mori, & Oku, 1970; tradicting the expected inactivation at such high temperature. Other Jacobsen & Jensen, 1975; Montville & Sapers, 1981; Nakajyo & Ishizu, authors attempted a higher pressure (827 MPa) combined with 75 °C 1985; Rodriguez, Cousin, & Nelson, 1993; Sandoval, Barreiro, & with B. subtilis and obtained only 3.2 log after 5 min (Balasubramanian Mendoza, 1992; Shridhar & Shankhapal, 1986; Vaughn, Irving, & & Balasubramaniam, 2010). The increase of temperature and/or the Mercer, 1952). Food acidification by citric or ascorbic acids is usually pressure had little effect on the spores in both studies. The variety of employed to inhibit the growth of these spore-forming bacteria. results registered, suggest that the most resistant strain for a specific food should be targeted when designing new HPTP processes.

3.2. Clostridium and Bacillus log reductions in low-acid foods 3.3. Bacteria log reductions in high-acid foods Table 2 shows the inactivation of spoilage Clostridium and Bacillus spore-formers after high pressures (600–900 MPa) combined with Table 3 shows the log reductions of A. acidoterrestris, B. subtilis, B. temperatures (75 °C–116 °C) for 1–15 min. Numerous investigators re- coagulans, and B. licheniformis bacterial spores achieved in suspended ported only 3.0 or less log reductions of C. sporogenes spores in low-acid fruit juices, purees, pulp, and concentrates after high pressures foods after high pressure thermal treatment at 900 MPa and 100 °C for (200– 827 MPa) combined with moderate temperatures (45–90 °C). 2 min, indicating the high resistance of these spores (Ramaswamy et al., Tomato juice was HPTP treated at a higher temperature of 105 °C. A. 2010; Ramaswamy & Shao, 2010; Shao et al., 2010; Zhu et al., 2008). acidoterrestris in fruit juice concentrates showed pressure and heat re- Careful consideration should be taken when using C. sporogenes as sistance, resulting in lower log reductions due to the high sugar content. surrogate species for HPTP C. botulinum inactivation, as the spore in- For instance, no inactivation occurred at 70 °Brix content, while a 5.0 activation is dependent on the C. botulinum strain and food product log reduction was achieved in a 35 °Brix apple juice concentrate pro- (Bull, Olivier, van Diepenbeek, Kormelink, & Chapman, 2009). cessed at 621 MPa–90 °C for 10 min (Lee, Chung, & Kang, 2006). With respect to Bacillus spores, milder processing conditions Sokolowska et al. (2013) also obtained similar behaviour with a dif- (≤827 MPa and ≤90 °C) were applied for HPTP inactivation studies, ferent strain, showing no effect on microbes for a 200 MPa-50 °C-10 min except Wang et al. (2009) who applied 600 MPa and 116 °C for 15 min process applied to apple juice concentrates (35.7 °Brix) vs. 2.0 log re- (Table 3). G. stearothermophilus (ATCC 7953) is the most resistant, with duction in 11.2 °Brix apple juice. As discussed previously, the tem- only 2 log reductions in soymilk after a 620 MPa-90 °C-7 min treatment perature plays an important role in bacterial spore inactivation, when (Estrada-Girón, Guerrero-Beltran, Swanson, & Barbosa-Canovas, 2007). the temperatures used were elevated. For example, HPTP of A. acid- High resistance was also observed for four strains of B. sphaericus spores oterrestris strain ATCC 49025 strain in apple juice at 621 MPa–90 °C–1 in skim milk with 0.4–1.2 log reduction after a 1 min treatment at min resulted in 6.0 log reductions (Lee, Dougherty, & Kang, 2002), 600 MPa and 85 °C or initial temperature before HPP of 72 °C compared to only 1.2 log reductions for A. acidoterrestris strain NZRM (Robertson et al., 2008; Scurrah et al., 2006). The same treatment 4098 in apple juice after 600 MPa–45 °C–10 min (Uchida & Silva, caused decimal log reductions of 1.4–3.4 log for five strains of B. subtilis 2017). Regarding B. coagulans, the use of 105 °C at 600 MPa resulted in in skim milk (Robertson et al., 2008; Scurrah et al., 2006). A wider 3.2 log reductions of 185 A strain after 0.5 min processing, indicating a range of spore inactivations (0.5–5.4 log) were obtained for three high resistance of these spores in tomato juice (Daryaei & strains of B. coagulans, also in skim milk, after 600 MPa-1 min and 72 °C Balasubramaniam, 2013; Zimmermann, Schaffner, & Aragão, 2013). B.

147 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 2 Inactivation of spoilage Clostridium and Bacillus spores in low-acid foods by HPTP.

Species Strains Food products pH Pressure Processing Holding Log Reference (MPa) temp. (°C)a Time (min) reduction

Clostridium PA 3679 (ATCC 7955) Milk > 4.6 900 100 2 1.1 Shao et al. (2010) sporogenes ATCC 11437 Milk > 4.6 900 100 2 2.7 Ramaswamy et al. (2010)

ATCC 7955 Salmon slurry 6.3 900 100 2 3.0 Ramaswamy and Shao (2010)

PA 3679 Ground beef > 4.6 900 100 2 3.0 Zhu et al. (2008)

Geobacillus ATCC 7953 Soymilk 6.5 620 90 7 2.0 Estrada-Girón et al. (2007) stearothermophilus

ATCC 7953 Cocoa mass (10% > 4.6 600 90 15 0.0 Ananta, Heinz, Schlüter, and Knorr water) (2001) Cocoa mass (30% > 4.6 600 90 15 4.5 water) Mashed broccoli > 4.6 600 90 15 4.5

Bacillus NZ 12 (ATCC 4525)/NZ Skim milk > 4.6 600 85 1 < 1.0 Robertson et al. (2008) sphaericus 14/NZ 15 NZ 13 1.0

NZ 14 Skim milk > 4.6 600 72b 1 0.4 Scurrah et al. (2006) NZ 12 (ATCC 4525) 0.6 NZ 15 0.9 NZ 13 1.2

Bacillus ATCC 6633 Mince crabmeat 7.3 827 75 5 3.2 Balasubramanian and subtilis Balasubramaniam (2010)

NZ 8 (NCTC 3610) Skim milk > 4.6 600 85 1 1.4 Robertson et al. (2008) NZ 1/NZ 9/NZ 10/NZ 11 3.2–3.3

NZ 8 (NCTC 3610) Skim milk > 4.6 600 72b 1 1.4 Scurrah et al. (2006) NZ 10 2.1 NZ 9 3.2 NZ 1 3.3 NZ 11 3.4

Bacillus coagulans IFFI 10144 Milk > 4.6 600 116 15 4.6 Wang et al. (2009)

FRR B2723 Skim milk > 4.6 600 72b 1 0.5 Scurrah et al. (2006) FRR B2735 (ATCC 15949) 3.7 FRR B2626 5.4

Bacillus circulans Werribee R236 Skim milk > 4.6 600 72b 1 4.2 Scurrah et al. (2006) Werribee 67 5.0 Werribee 233 5.2

a Processing temperature was the average temperature during the constant pressure phase of the HPP cycle. b Initial temperature before compression. subtilis in tomato puree was subjected to higher pressure (827 MPa) Saccharomyces cerevisiae and Zygosaccharomyces bailii are two yeast combined with 75 °C during 5 min, and < 5.0 log reduction was ob- spore-formers that have been responsible for spoilage of high-acid and tained (Balasubramanian & Balasubramaniam, 2010). acidified foods (Silva & Evelyn, 2018). Although low-acid foods are less susceptible to fungal spoilage than fi 4. HPP and HPTP inactivation of mould and yeast spores in low- high-acid and acidi ed foods since they are usually kept at refrigerator acid (pH > 4.6) and high-acid (pH < 4.6) foods temperatures, spoilage by mould and yeast spore-formers have also been recorded. The spoilage thought to be due to post-processing 4.1. Mould and yeast spore-formers contaminations during bottling or packaging (Jodral et al., 1993) or the presence of heat-resistant of mould/yeast spores (Garnier, Valence, & High-acid and acidified foods are prone to mould and yeast spore- Mounier, 2017). Examples of important mould spore-formers and as- fi formers contamination. The growth of moulds could result in the in- sociated foods are B. nivea, N. scheri, Eupenicillium brefeldianum and crease of the food pH above 4.6, thus increasing the potential for C. Hamigera avellanea, all in cream cheese (Pitt & Hocking, 2009). B. nivea, fi botulinum growth and risk (Breidt & Costilow, 2004). Typical mould N. scheri, and Talaromyces macrosporus isolated from heat-treated milk, spore-formers associated with spoilage of these foods during distribu- have also been found (Pitt & Hocking, 2009). Aspergillus and Penicillium tion at room temperature or at refrigerated conditions are Byssochlamys are also typical spoilage moulds in dairy products (Garnier et al., 2017). nivea, Byssochlamys fulva, Neosartorya fischeri, Talaromyces avellanus, Certain species of Aspergillus have been found as contaminants in tree Talaromyces flavus, Eurotium repens, Eupenicillium javanicum, and Peni- nuts, peanuts, other oilseeds (including corn and cottonseed), and milk cillium expansum (Silva & Evelyn, 2018; Silva & Gibbs, 2004, 2009). (FDA, 2012). With respect to yeast, important spore-formers in low-acid

148 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 3 Inactivation of Alicyclobacillus acidoterrestris and other spoilage bacterial spores in high-acid fruit juice, purees, and concentrates by HPTP.

Bacteria Strain Fruit products pH Soluble Pressure Processing Holding Log Reference solids (MPa) temp. (°C)a time (min) reduction (°Brix)

Alicyclobacillus ATCC 49025, Apple juice 3.7 11–13 621 90 1 6.0 Lee et al. (2002) acidoterrestrisb NFPA1013

NFPA1013, Apple juice conc. 3.9 17.5 621 90 5 5.8 Lee et al. (2006) NFPA1101 Apple juice conc. 3.9 35 621 90 10 5.0 Apple juice conc. 3.9 70 621 90 10 0.0

Alicyclobacillus NZRM 4098 Orange juice 3.8 9.2 600 65 10 2.6 Silva et al. (2012) acidoterrestris

NZRM 4447 Apple juice 3.4 10.6 600 45 10 1.2 Uchida and Silva (2017) (ATCC 49025) Lime juice conc. 2.5 20.2 600 45 10 0.5 Blackcurrant juice 3.1 30.3 600 45 10 0.2 conc.

TO-117/02 Apple juice 3.4 11.2 200 50 10 2.0 Sokolowska et al. (2013) Concentrate 3.3 23.6 200 50 10 1.2 Concentrate 3.2 35.7 200 50 10 0.0 TO-29/4/02 Apple juice 3.4 11.2 200 50 10 2.6 Concentrate 3.3 23.6 200 50 10 1.4 Concentrate 3.2 35.7 200 50 10 0.5

Bacillus subtilis ATCC 6633 Tomato puree 4.1 nr 827 75 5 4.5 Balasubramanian and Balasubramaniam (2010)

Bacillus coagulans 185A Tomato juice 4.2 6.0 600 105 0.5 3.2 Daryaei and Balasubramaniam (2013)

ATCC 7050 Tomato pulp 4.3 4.0 600 60 10 5.0 Zimmermann et al. (2013)

a Processing temperature was the average temperature during the constant pressure phase of the HPP cycle. b Cocktail of strains; nr – not reported. foods are S. cerevisiae and Pichia membranefaciens in cheese and milk treatment (Evelyn, Kim, & Silva, 2016). This is in agreement with Ba- (Fleet, 1990), and Rhodotorula mucilaginosa in butter and margarine cillus spores, where temperature played a significant role in the in- (Fleet & Mian, 1987). Aspergillus, Penicillium, and Eurotium moulds as activation above 600 MPa. More research is needed, since specific well as Pichia, Rhodotorula, and Saccharomyces yeasts are also common strains of B. nivea were comparable to spores of psychrotrophic B. cereus spore-formers isolated from spoiled fresh and refrigerated meats and strains in terms of resistance. Room temperature (Room-T) HPP only poultry (Dave & Ghaly, 2011). had an effect in a specific group of less resistant mould spores. Room temperature HPP at 600 MPa for 15 min achieved only 1.1 log reduc- 4.2. Log reductions of moulds and yeasts tion of Talaromyces avellaneus (Voldřich, Dobiáš, Tichá, Čeřovský, & Krátká, 2004); non-thermal HPP (≤45 °C) combined with 350–500 MPa In general, heat-resistant mould spores require the combination of for 15 min achieved a higher E. repens (4.2 log) and P. expansum (6.0 high pressure and thermal processing (HPTP) for their inactivation in log) spore reduction (Merkulow, Eicher, & Ludwig, 2000). high-acid foods. Some strains of B. nivea mould spores even posed si- Although contamination and spoilage of low-acid foods with mould milar degrees of HPTP resistance to those of bacterial spores. On the spore-formers is possible, HPP or HPTP inactivation studies with mould contrary, yeast spores exhibited the least resistance to HPP, thus re- spores are rare. Certain fruits such as mango, avocado, watermelon, quiring only HPP at room temperature for their inactivation. Table 4 melon, banana, etc., can have low acidity and deserve special attention presents the HPTP inactivation of resistant mould spores in high-acid due to safety issues, as pathogens can grow. Chapman et al. (2007) juices, purees, and concentrates. HPTP at 700 MPa–70 °C–15 min had obtained B. nivea spores inactivation between 3 log reduction to no no effect on B. nivea suspended in 63 °Brix bilberry jam (Butz, inactivation in mango puree (pH 5) after 600 MPa-room T-10 min, Funtenberger, Haberditzl, & Tauscher, 1996). Similarly, the protective without any heating. Similarly, these authors also showed that three effect of high sugar content was observed for B. nivea in 41 and 50 °Brix strains of B. fulva in mango puree at pH 5 were reduced by 2.8–3.6 log juice concentrates after 5 min at 689 MPa-60 °C (Palou et al., 2000). after the same treatment. Merkulow et al. (2000) obtained only 2 log Similar to bacteria, these results show the important role of high sugar reductions for E. repens spores after 500 MPa–room T–15 min and < 6 content in foods to the resistance of moulds to HPTP. B. nivea seemed to log reductions for P. expansum spores after 350 MPa–room T–15 min, be the most resistant among all the moulds, and comparable to bacterial both in broccoli juice (pH 6.6). resistance, with log reductions between 1.5 and 3.2 after 600–700 MPa Yeast ascospores presented lower resistances than bacterial and combined with 70–75 °C for 15 min (Butz et al., 1996; Evelyn & Silva, mould spores and were much easier to inactivate. Thus, only ambient 2015c; Ferreira, Rosenthal, Calado, Saraiva, & Mendo, 2009). Evelyn HPP was applied (Table 4). For example, at 500 MPa, 6 log reduction of and Silva (2018b) confirmed the higher resistance of B. nivea spores S. cerevisiae in apple and orange juices were obtained after 0.4–1.1 min, over psychrotrophic B. cereus spores, i.e., 2.2 log for B. nivea vs. 4.9 log depending on the strain (Parish, 1998; Zook, Parish, Braddock, & for B. cereus after HPTP (600 MPa, 70–75 °C, and 20 min). Ferreira et al. Balaban, 1999). A lower pressure (300 MPa) for 15 min resulted in 0.5, (2009) obtained a 6 log reduction when using a higher temperature 1.5, and 2 log reductions of Z. bailii spores in grape juice, orange/apple/ (90 °C) at 600 MPa HPP instead of 70 °C –600 MPa for 15 min. N. fischeri pineapple, and cranberry juices, respectively (Raso, Calderón, Góngora, in apple juice resulted 3.7 log reductions after 75°C-600 MPa–15 min Barbosa-Cánovas, & Swanson, 1998).

149 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 4 Inactivation of 4–5 week old moulds and yeast spores in high-acid fruit juices, purees, and concentrates by HPTP and HPP alone.

Strain Fruit products Pressure Processing Holding time Log reduction Reference (MPa) temp. (min) pH Brix (°C)a

Moulds:

Byssochlamys nivea nr Pineapple nectar 3.7 12 600 90 15 6.0 Ferreira et al. (2009) 600 70 15 1.5 Pineapple juice 3.7 13 600 90 5 6.0 600 70 15 2.0

DSM 1824 Grape juice < 4.6 nr 700 70 15 3.2 Butz et al. (1996)

JCM Strawberry puree 3.4 8.1 600 75 15 1.8 Evelyn and Silva (2015c) 12806 (CBS 696.95)

nr Apple juice 3.8 41 689 60 5 0.0 Palou et al., 2000 concentrate Cranberry juice 2.6 50 689 60 5 0.0 concentrate

DSM 1824 Bilberry jam < 4.6 63 700 70 15 0.0 Butz et al. (1996)

Neosartorya fischeri JCM 1740 Apple juice 3.7 10.6 600 75 15 3.7 Evelyn et al. (2016)

Talaromyces avellaneus nr Apple juice 3.5 10.8 600 Room T 15 1.1 Voldřich et al. (2004)

Eurotium repens DSMZ Apple juice 3.3 nr 500 Room T 15 4.2 Merkulow et al. (2000) 62631

Penicillium expansum DSMZ Apple juice 3.3 nr 350 Room T 15 6.0 1994 (CECT 2279)

Yeasts:

Zygosaccharomyces bailii ATCC Grape juice 3.0 nr 300 Room T 15 0.5 Raso, Calderón, Góngora, 36947 Barbosa‐Cánovas, and Swanson (1998) Orange juice 3.9 nr 300 Room T 15 1.5 Apple juice 4.1 nr 300 Room T 15 1.5 Pineapple juice 3.4 nr 300 Room T 15 1.5 Cranberry juice 3.5 nr 300 Room T 15 2.0

Saccharomyces cerevisiae YM-147 Orange juice 3.9 nr 500 Room T 1.1 6.0 Zook et al. (1999) Apple juice 3.8 nr 500 Room T 0.9 6.0 nr Orange juice 3.7 11 500 Room T 0.4 6.0 Parish (1998) Pichia anomala nr Sucrose solution 4.2 20 400 Room T 2.0 2.0 Hocking, Begum, and Stewart (2004)

Processing temperature was the average temperature during the constant pressure phase of the HPP cycle. a Room T = Room temperature HPP, T less or equal to 45 °C; .nr – not reported.

5. Models and kinetics of HPP and HPTP inactivation of HPTP treatment for a specific time t (min). Based on this, some authors pathogenic and spoilage spores in foods used the first-order biphasic model when two fractions of micro- organisms are assumed to be inactivated independently, according to

5.1. Mathematical and kinetic models for spore inactivation first-order kinetics (Eq. (1)). Thus, two D-values (D1 and D2)(Cerf, 1977; Xiong, Xie, Edmondson, & Sheard, 1999) are obtained, D1 cor- Simple first-order kinetic and Weibull models are common primary responding to the less resistant and D2 the most resistant microbial models used to describe microbial log survivors in foods after HPP and fractions. HPTP (Bigelow, 1921; Peleg & Cole, 1998). The main kinetic parameter The Weibull model is based on the principle of heterogeneity in the of the first-order model is the decimal reduction time or DP,T-value, resistance distributed among individual cells within a population (vi- which is the time (min) at a certain pressure and/or temperature ne- talistic approach) (Pin & Baranyi, 2006) (Eq. (2)): cessary to reduce microbial population by 90% (calculated from the N reciprocal of the slope of Eq. (1)): log =−btn N0 (2) N t log =− Two parameters obtained from this primary model are b(scale N0 DPT (1) factor) and n (survival curve shape factor), where b is a rate parameter where N0 is the initial or untreated cell population in the food (cfu/g or which is related to the rate at which the microorganism is inactivated, cfu.mL), and N is the number of survivors after being exposed to HPP or and n describes the degree of curvilinearity, with n < 1 and n >1

150 vlnadFVM Silva F.V.M. and Evelyn Table 5 Modelling the pathogenic and spoilage bacterial spore inactivation in foods after HPTP.

Food products pH Pressure Processing Model Model parametersb Reference (MPa) temp. (°C)a

Clostridium perfringens NZRM 2621 Beef slurry 6.5 600 75 Weibull b = 0.20; n = 0.74 Evelyn and Silva (2016a) (ATCC 12917) NZRM 898 b = 0.68; n = 0.39 (ATCC 14809) Bacillus cereus NZRM 984 Skim milk > 4.6 600 70 Weibull b = 0.55; n = 0.59 Evelyn and Silva (2015b) (ATCC 11778) ICMP 12442 b = 0.67; n = 0.57 (ATCC 9139) ICMP 12442 Beef slurry 6.5 600 70 Weibull b = 2.13; n = 0.28 Evelyn and Silva (2016b) (ATCC 9139) As 1.1846 Milk buffer 7.0 400–600 60–80 Second degree Y = 5.42 + 1.54P+0.30T + 0.25t−0.11P2+ 0.17T2-0.23t2-0.23 Pt Ju et al. (2008) polynomial (RSM) Clostridium sporogenes PA 3679 (ATCC Milk > 4.6 900 100 First order D-value (min): 1.2 zT-value: Shao et al. (2010) 7955) 90 7.0 18.9 °C

151 80 13.7 PA 3679 Ground beef > 4.6 900 100 First order D-value (min): 0.7 zT-value: Zhu et al. (2008) 90 2.3 19.8 °C 80 6.9 ATCC 11437 Milk > 4.6 900 100 First order D-value (min): 0.6 zT-value: Ramaswamy et al. (2010) 90 3.7 19.6 °C 80 6.6 ATCC 7955 Salmon slurry 6.3 900 100 First order D-value (min): 0.6 zT-value: Ramaswamy and Shao 90 2.8 16.4 °C (2010) 80 9.4 Geobacillus stearothermophilus ATCC 7953 Soymilk 6.5 620 90 First order D-value (min): 3.5 zT-value: Estrada-Girón et al. (2007) 80 6.2 41.5 °C 70 10.6 Trends inFoodScience&Technology88(2019)143–156 As 1.1923 Milk buffer 7.0 432–768 63–97 Second degree Y = 5.28 + 1.576P+0.15T + 0.312t−0.14P2+0.199T2-0.138t2 Gao, Ju, and Jiang (2006b) polynomial (RSM) Bacillus subtilis ATCC 6633 Citrate phosphate 3–7 690–827 60–75 Second order Y = −15.2 + 0.04P+1t-1.74 pH + 0.026t2−0.0007PT-0.0009 Pt+0.0011PpH−0.0163 Tt+0.024TpH Balasubramanian and buffer polynomial Balasubramaniam (2010) As 1.1731 Milk buffer 7.0 332–668 63–97 Second degree Y = 4.12 + 1.56P+0.347T + 0.248t+0.266P2+0.339 PT Gao et al. (2006a) polynomial (RSM) Bacillus coagulans IFFI 10144 Milk > 4.6 600 116 Weibull b = −2.79; n = 0.18 Wang et al. (2009) 185A Tomato juice 4.2 600 95 Weibull b = 1.93; n = 0.68 Daryei and Balasubramanian 2013 ATCC 7050 Tomato pulp (4.0 4.3 600 60 First order D-value (min)c: (1) 1.6 Zimmermann et al. (2013) °Bx) biphasic (2) 5.6 Alicyclobacillus acidoterrestris (continued on next page) Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

corresponding to concave-upwards (tailings) and convex or concave- downwards (shoulders) survival curves, respectively. When n = 1, the Weibull model becomes the same as a simple first-order kinetic model. The secondary model is an extension of the primary model, in which the parameters of the primary model (e.g. D-value and inactivation rates, k) relate to the environmental variables/conditions such as

pressure or temperature. With respect to the first-order kinetics, the zT- Silva et al. (2012) Uchida and Silva (2017) Reference value (°C) is the temperature increase under constant pressure, which results in a 10-fold decrease in the D-value. This is equal to the re- ciprocal of the slope of the log D-values plotted against temperature (Eq. (3)):

TTref − zT = logD− logDref (3) are the log reductions and variables pressure,

pH where DTref is the D-value at a reference temperature Tref (°C), and T is , t the temperature of the isothermal treatment (°C). Likewise, a zP-value T , -value: T , can be used to relate the inactivation D-value to the HPTP pressure for a 34.4 °C P

, fixed temperature or room temperature HPP, and is equal to the re- Y ciprocal of the slope of the log D-values plotted against pressure (Eq. (4)):

PPref − zP = logD− logDref (4) ), respectively;

(2) The Weibull model can also relate the inactivation rate parameter (b-value) to environmental variables, particularly temperature and can be used to predict the parameter values outside the range of the vari- 8.6 19.9 46.1 ables tested (Evelyn & Silva, 2015a, 2015b, 2015c, 2016a, 2016b, 2017; Evelyn et al., 2016). The polynomial model or response surface model (RSM) is another secondary model that has been developed to predict the effect of mul- tiple environmental factors on the inactivation parameters (Ross & Dalgaard, 2004). Second-order polynomial equations are generally b -values were calculated from the inactivation rates published. used, involving first-order, second-order (quadratic), and interaction D terms, as shown in Eq. (5) (Pérez-Rodríguez & Valero, 2013):

n n n 2 Y=+ B0 ∑∑ BXii + BXii i + ∑ BXXij i j +ε i==11i j ≠1 (5) -values. The -value (min): -value (min): 3.4 z D Model parameters D D are the Weibull scale and shape factors (Eq.

n where Y is the predicted response (microbial log survivors); B0, Bi, Bii, and Bij are the estimated regression coefficients; Xi and Xj are the en- and

b vironmental factors (such as pressure, temperature, and pressure- ), respectively. holding in HPTP); and ε is the error term. By graphically translating (5) RSM, food operators can find the operating conditions that minimize Model First order the response Y.

a 5.2. Bacterial spores

Most of the studies carried out with pathogenic Clostridium and Processing temp. (°C) Bacillus demonstrated non-linearity for the log survivors vs. time in low- acid foods after HPTP (Table 5). Thus, the Weibull model was one of the models used (Eq. (2)). For 600 MPa processed at 70 °C–75 °C, the

(MPa) Weibull shape factors (n) for C. perfringens and B. cereus spores were between 0.28 and 0.74, indicating that the log survival curves have upward concavity (n < 1) with more pronounced tailings, as proces- 3.4 6002.5 600 45 45 3.1 600 45 3.8 600 65 First order sing times increase (Evelyn & Silva, 2015b; 2016a; 2016b). Response surface methodology has often been used to investigate the effects of

rst-order kinetic parameters (Eqs.(1), (3) and (4)); pressure, temperature, and time on spore inactivation, and to predict fi the processing conditions to achieve a desired log reduction of spores (Eq. (5)). For example, the optimum process parameters of 540 MPa–71 °C–16.8 min for a six-log cycle reduction of B. cereus spores ) Food products pH Pressure Apple juice (10.6 °Bx) Lime juice conc. (20.2 °Bx) Blackcurrant juice conc. (30.3 °Bx) °Bx) in milk buffer were predicted (Ju et al., 2008).

value are the Several authors reported first-order kinetics (Eqs. (1), (3) and (4)) z- rst-order biphasic model assumes two rates of inactivation corresponding to two

continued for HPTP of all strains of C. sporogenes, one strain of G. stear- fi ( and othermophilus spores in meat/milk and two strains of A. acidoterrestris in T (ATCC 49025) D Processing temperature was the average temperature during constant pressure phase of the HPP cycle. The fruit juices/concentrates. For C. sporogenes, HPTP at 900 MPa–90 °C, a b c NZRM 4447 NZRM 4098 Orange juice (9.2 Table 5 – – temperature, holding-time, and acidity of the RSM polynomial equation (Eq. D90°C-values = 2.3 7.0 min and zT-values = 16.4 19.8 °C were

152 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156

Table 6 Modelling the inactivation of mould and yeast spores in high-acid fruit juices and purees after HPTP and HPP alone.

Fruit products Pressure Processing Model Model parametersb Reference

pH Brix (MPa) temp. (°C)a

Moulds: Byssochlamys nivea JCM 12806 (CBS 696.95) Strawberry puree 3.4 8.1 600 75 Weibull b = 0.29; n = 0.66 Evelyn and Silva (2015c)

Neosartorya fischeri JCM 1740 (ATCC 1020) Apple juice 3.7 10.6 600 75 Weibull b = 1.44; n = 0.35 Evelyn et al. (2016)

Eurotium repens DSMZ 62631 Apple juice 3.3 12.4 500 Room T First order D-value (min): Merkulow et al. (2000) biphasic (1) 2.0; (2) 9.0

Penicillium expansum DSMZ 1994 (CECT 2279) Apple juice 3.3 12.4 350 Room T First order D-value (min): Merkulow et al. (2000) biphasic (1) < 1.0; (2) no inactivation

Yeasts: Saccharomyces cerevisiae YM-147 Orange juice 3.9 nr 500 Room T First order D-value (min): 0.18 Zook et al. (1999)

zp-value: 117 MPa

Apple juice 3.8 nr 500 Room T First order D-value (min): 0.15 zp-value:115 MPa

nr Orange juice 3.7 11 500 Room T First order D-value (min): 0.067 Parish (1998)

zp-value =123 MPa

a Processing temperature was the average temperature during the constant pressure phase of the HPP cycle. b DT and z-value are the first-order kinetic parameters (Eqs. (1), (3) and (4)); b and n are the Weibull scale and shape factors (Eq. (2)), respectively; The first-order biphasic model assumes two rates of inactivation corresponding to two D-values and the D-values were calculated from the inactivation rates published; Room T = Room temperature HPP, T less or equal to 45 °C; nr – not reported.

estimated, and for G. stearothermophilus HPTP at 620 MPa-90 °C, D90°C- 5.3. Mould and yeast spores values = 3.5 min and zT-values = 41.5 °C were obtained (Estrada-Girón et al., 2007; Ramaswamy et al., 2010; Ramaswamy & Shao, 2010; Shao Similar to bacteria, HPTP inactivation of heat-resistant mould et al., 2010; Zhu et al., 2008). Silva et al. (2012) and Uchida and Silva spores also showed non-linearity (Weibull and first-order biphasic (2017) also used first-order kinetics to model the survival lines of A. models adjusted to spore log survival data). For example, the in- acidoterrestris in juices, in spite of a slight non-linearity being recorded. activation of B. nivea and N. fischeri in high-acid juices/purees exhibited

At 600 MPa, the D65°C-value in orange juice was 3.4 min and zT- an upward concavity (n between 0.35 and 0.66) and was best described value = 34.4 °C, and for apple juice with another strain the D45°C- by the Weibull model (Eq. (2), Table 6). The first-order biphasic or value = 8.6 min. The D600 MPa, 45°C-value increased from 8.6 min in 10.6 linear model (Eq. (1)) was fitted to other mould spore inactivations at °Brix apple juice to 20 min in 20 °Brix lime juice concentrate, and to room temperature. For example, the first-order biphasic model was 46 min in 30 °Brix blackcurrant juice concentrate. used in high-acid juices: D-values of 2 and 9 min for E. repens at For non-linear inactivation of spoilage bacterial spores, authors used 500 MPa and D-values of < 1.0 followed by no inactivation for P. ex- the Weibull model (as reported for the pathogenic bacterial spores) to pansum at 350 MPa. In broccoli juice at higher pH, both models have describe the relation between the log survivors vs. time of B. coagulans been used. A D-value of 16 min for E. repens at 500 MPa and D-values spores in milk for 600 MPa-116 °C and tomato juice for 600 MPa and of < 1.0 followed by no inactivation for P. expansum at 350 MPa were 95 °C processes (Daryaei & Balasubramaniam, 2013; Wang et al., 2009). obtained (Merkulow et al., 2000). With respect to yeast spores, first- Other studies used the first-order biphasic model to describe the non- order kinetics (Eqs. (1), (3) and (4)) has often been used to describe linear survival curves. For instance, the D1-and D2-values of 1.6 and HPP inactivation (Table 6). The first-order kinetic parameters reported 5.6 min, respectively, was fitted to describe the inactivation of B. coa- for room-T HPP inactivation of S. cerevisiae yeast spores in acidic fruit gulans spores in tomato pulp after 600 MPa and 60 °C (Zimmermann juices are as follows: the D500 MPa-values ranged between 0.07 and et al., 2013). In three studies, a second order polynomial was generated 0.18 min with very similar zP-values i.e. 117–123 MPa (Parish, 1998; using response surface methodology (RSM). The combined effect of Zook et al., 1999). HPTP pressure, temperature and processing time on spore inactivation was investigated and the following optimum HPTP microbial in- 6. Conclusions and final remarks activation conditions were predicted in milk buffer: 576 MPa–87 °C–13 min for B. subtilis, and 625 MPa–86 °C–14 min for G. In general, among all microorganisms, bacterial spores have the stearothermophilus (Gao, Ju, & Jiang, 2006a; 2006b). HPTP inactivation highest resistance to HPP, requiring combinations of high pressure and of B. subtilis spores suspended in citrate phosphate buffer has also been temperatures (HPTP) for their inactivation in foods. Likewise, HPTP is fitted with a second-order polynomial equation (Balasubramanian & also required for the inactivation of resistant mould spores often present Balasubramaniam, 2010). in high-acid foods, in which similar HPTP resistance to bacterial spores To summarize, most studies of HPTP inactivation of spoilage spores was shown for certain species. The type of food affects spore resistance. in foods/beverages exhibited non-linearity. The tails in the survival For a specific food, the most resistant spores should be tested and used curves pose a challenge to HPP processors, thus severe processing as a target/reference to design successful pasteurization processes and conditions (higher temperature and/or pressure) might be more effec- produce safe pasteurized foods. tive. Subsequently, there is a need to design commercial HPP units Based on literature, for low-acid (pH > 4.6) foods such as milk, which can handle these conditions. meat and vegetables, C. botulinum proteolytic type B spores with

153 Evelyn and F.V.M. Silva Trends in Food Science & Technology 88 (2019) 143–156 minimum HPTP treatment conditions of > 900 MPa and > 110 °C CDC (Centers for Disease Control) (2000). Human ingestion of Bacillus Anthracis-con- for > 5 min can be used as process reference/objective. taminated meat — Minnesota, August 2000. Morbidity and Mortality Weekly Report fi (MMWR), 49(36). Regarding high-acid and acidi ed foods (juices/purees), the fol- Cerf, O. (1977). Tailing of survival curves of bacterial spores. Journal of Applied lowing microbial spore targets and minimum HPTP treatment condi- Bacteriology, 42,1–19. tions are recommended, depending on the most critical organism for a Cerny, G., Duong, H. A., Hennlich, W., & Miller, S. (2000). Alicyclobacillus acidoterrestris. fi Influence of oxygen content on growth in fruit juices. Food Australia, 52(7), 289–291. speci c food: Chapman, B., Winley, E., Fong, A. S. W., Hocking, A. D., Stewart, C. M., & Buckle, K. A. (2007). 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