Abstract
In food processing, high hydrostatic pressure (HHP) can inactivate microbes, and the inactivation is either lethal or sublethal, depending on the intensity of HHP-induced stress. Inactivation of bacteria is a key to ensure food safety by HHP food processing. This manuscript reviews HHP-induced injury of bacteria such as Escherichia coli, Listeria monocytogenes, and (vegetative) Bacillus subtilis. The stress in the sublethal inactivation depends on HHP level, holding time, bacterial species/strain, and other environmental factors. The sublethal inactivation induces injury of bacteria, and the injured bacteria may recover under suitable conditions. The recovery behavior depends on nutrients surrounding the bacteria and the storage temperature. In the detection of HHP-injured bacteria, detection media and incubation temperature play important roles. Mechanisms involved in HHP-injured bacteria can be discussed from several viewpoints including membrane damage, reactive oxygen species, HHP resistance, ribosomes, metabolome, and colony-forming behavior. HHP-induced injury of molds, yeasts, parasites, and viruses has not been sufficiently studied.
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References
Hayashi R (1987) Possibility to apply high pressure to cooking, processing, pasteurization, and preservation. Shokuhin to Kaihatsu [Food Process Ingred] 22(7):55–62 (in Japanese)
Kimura K, Ida M, Yosida Y et al (1994) Comparison of keeping quality between pressure-processed jam and heat-processed jam: changes in flavor components, hue, and nutrients during storage. Biosci Biotechnol Biochem 58(8):386–1391
Balasubramaniam VM, Barbosa-Cánovas GV, Lelieved HLM (2016) High Pressure Processing of Foods. Springer, New York
Yamamoto K (2017a) Food processing by high hydrostatic pressure. Biosci Biotechnol Biochem 81(4):672–679
Rendueles E, Omer MK, Alvseike O et al (2011) Microbiological food safety assessment of high hydrostatic pressure processing: a review. Lebenson Wiss Technol 44(5):1251–1260
Schottroff F, Fröhling A, Zunabovic-Pichler M et al (2018) Sublethal injury and viable but non-culturable (VBNC) state in microorganisms during preservation of food and biological materials by non-thermal processes. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02773
Syed QA, Buffa M, Guamis B et al (2016) Factors affecting bacterial inactivation during high hydrostatic pressure processing of foods: A review. Crit Rev Food Sci Nutr 56(3):474–483
Wu VCH (2008) A review of microbial injury and recovery methods in food. Food Microbiol 25(6):735–744
Hoover DG, Metrick C, Papineau AM et al (1989) Biological effects on high hydrostatic pressure on food microorganisms. Food Technol 43:99–107
Mackey BM, Mañas P (2008) Inactivation of Escherichia coli by high pressure. In: Michiels C, Aertsen A, Bartlett D, Yayanos Y (eds) High Pressure Microbiology. ASM Press, Washington DC, pp 53–85
Needs EC, Capellas M, Bland AP et al (2000) Comparison of heat and pressure treatments of skim milk, fortified with whey protein concentrate, for set yogurt preparation: effects on milk proteins and gel structure. J Dairy Res 67(3):329–348
Aertsen A, Meersman F, Hendrickx MEG et al (2009) Biotechnology under high pressure: applications and implications. Trends Biotechnol 27(7):434–441
Meersman F, Smeller L, Heremans K (2006) Protein stability and dynamics in the pressure–temperature plane. Biochim Biophys Acta 1764(3):346–354
Moussa M, Perrier-Cornet J-M, Gervais P (2007) Damage in Escherichia coli cells treated with a combination of high hydrostatic pressure and subzero temperature. Appl Environ Microbiol 73(20):6508–6518
Takahashi S, Sugimoto N (2013) Effect of pressure on the stability of G-quadruplex DNA: thermodynamics under crowding conditions. Angew Chem Int Ed 52:13774–13778
Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222(3):599–620
Lullien-Pellerin V, Balny C (2002) High-pressure as a tool to study some proteins’ properties: conformational modification, activity and oligomeric dissociation. Innov Food Sci Emerg Technol 3(3):209–221
Matsuki H, Goto M, Tada K et al (2013) Thermotropic and barotropic phase behavior of phosphatidylcholine bilayers. Int J Mol Sci 14(2):2282–2302
Aertsen A, De Spiegeleer P, Vanoirbeek K et al (2005) Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 71(5):2226–2231
Hite BH (1899) The effect of pressure in the preservation of milk. West Virg Agric Exp Sta Bull 58:15–35
Daryaei H, Yousef AE, Balasubramaniam VM (2016) Microbiological aspects of high-pressure processing of food: inactivation of microbial vegetative cells and spores. In: Balasubramaniam VM, Barbosa-Cánovas GV, Lelieved HLM (eds) High Pressure Processing of Foods. Springer, New York, pp 271–294
Reitermayer D, Kafka TA, Lenz CA et al (2018) Interrelation between Tween and the membrane properties and high pressure tolerance of Lactobacillus plantarum. BMC Microbiol 18:72. https://doi.org/10.1186/s12866-018-1203-y
Ludwig H, Schreck C (1997) The inactivation of vegetative bacteria by pressure. In: Heremans K (ed) High pressure research in the biosciences and biotechnology. Leuven University Press, Leuven, pp 221–224
Cebrián G, Mañas P, Condón S (2016) Comparative resistance of bacterial foodborne pathogens to non-thermal technologies for food preservation. Front Microbiol 7(734):1–17
Mackey BM, Forestiére K, Isaacs N (1995) Factors affecting the resistance of Listeria monocytogenes to high hydrostatic pressure. Food Biotechnol 9(1–2):1–11
Alpas H, Kalchayanand N, Bozoglu F et al (1999) Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Appl Environ Microbiol 65(9):4248–4251
Black EP, Huppertz THM, Kelly AL et al (2007) Baroprotection of vegetative bacteria by milk constituents: a study of Listeria innocua. Int Dairy J 17(2):104–110
Koseki S, Mizuno Y, Yamamoto K (2008) Use of mild-heat treatment following high-pressure processing to prevent recovery of pressure-injured Listeria monocytogenes in milk. Food Microbiol 25:288–293
Kimura K, Morimatsu K, Inaoka T et al (2017) Injury and recovery of Escherichia coli ATCC25922 cells treated by high hydrostatic pressure at 400–600 MPa. J Biosci Bioeng 123(6):698–706
Yamamoto K (2017b) “Koatsu shokuhin kakou niokeru shokuhin anzensei kakuho” (Food safety assurance in high pressure food processing). Food Packag 58(9):530–537 (in Japanese)
Davis C (2014) Enumeration of probiotic strains: review of culture-dependent and alternative techniques to quantify viable bacteria. J Microbiol Methods 103:9–17
Wilkinson MG (2018) Flow cytometry as a potential method of measuring bacterial viability in probiotic products: a review. Trends Food Sci Technol 78:1–10
Kell DB, Kaprelyants AS, Weichart DH et al (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 73:169–187
Oliver JD (2005). The viable but nonculturable state in bacteria. J Microbiol 43 (S): 93–100.
Earnshaw RG, Appleyard J, Hurst RM (1995) Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. Int J Food Microbiol 28(2):197–219
Tsuchido T, Kanda K, Shibasaki I (1975) Enhancement of sporicidal activity of an amphoteric surfactant by heating. J Ferment Technol 53(12):862–868
Nakamura M, Saito K, Katayama T et al (2004) Radiation-heat synergism for inactivation of Alicyclobacillus acidoterrestris spores in citrus juice. J Food Prot 67(11):2538–2543
Koseki S, Yamamoto K (2006) Recovery of Escherichia coli ATCC25922 in phosphate buffered saline after treatment with high hydrostatic pressure. Int J Food Microbiol 110:108–111
Morimatsu K, Inaoka T, Nakaura Y et al (2019) Injury and recovery of Escherichia coli cells in phosphate-buffered saline after high hydrostatic pressure treatment. Food Sci Technol Res 25(3):479–484
Gounot A-M (1986) Psychrophilic and psychrotrophie microorganisms. Experientia 42:1192–1197
Nakaura Y, Morimatsu K, Inaoka T et al (2019) Listeria monocytogenes cells injured by high hydrostatic pressure and their recovery in nutrient-rich or -free medium during cold storage. High Pressure Res 39(2):324–333
Nasiłowska J, Sokołowska B, Fonberg-Broczek M (2018) Long-term storage of vegetable juices treated by high hydrostatic pressure: assurance of the microbial safety. BioMed Res Int. https://doi.org/10.1155/2018/7389381
Ray B (1979) Methods to detect stressed microorganisms. J Food Prot 42(4):346–355
Hartsell SE (1951) The longevity and behavior of pathogenic bacteria in frozen foods: the influence of plating media. Am J Public Health Nations Health 41(9):1072–1077
Nakane M, Fuchu H, Nakaura Y et al (2019) Effect of plating and incubation conditions on the detection of lactic acid bacteria after high hydrostatic pressure treatment. High Press Res 39(2):334–343
Chuang S, Sheen S, Sommers CH et al (2020) Survival evaluation of Salmonella and Listeria monocytogenes on selective and nonselective media in ground chicken meat subjected to high hydrostatic pressure and carvacrol. J Food Prot 83(1):37–44
Mañas P, Pagán R (2005) Microbial inactivation by new technologies of food preservation. J Appl Microbiol 98(6):1387–1399
Calabrese JP, Bissonnette GK (1990) Improved membrane filtration method incorporating catalase and sodium pyruvate for detection of chlorine-stressed coliform bacteria. Appl Environ Microbiol 56(11):3558–3564
Czechowicz S, Santos O, Zottola E (1996) Recovery of thermally-stressed Escherichia coli O157:H7 by media supplemented with pyruvate. Int J Food Microbiol 33(2–3):275–284
McDonald LC, Hackney CR, Ray B (1983) Enhanced recovery of injured Escherichia coli by compounds that degrade hydrogen peroxide or block its formation. Appl Environ Microbiol 45(2):360–365
Mizunoe Y, Wai SN, Takade A et al (1999) Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H2O2-degrading compounds. Arch Microbiol 172:63–67
Morishige Y, Fujimori K, Amano F (2013) Differential resuscitative effect of pyruvate and its analogues on VBNC (viable but non-culturable) Salmonella. Microbes Environ 28(2):180–186
Inaoka T, Kimura K, Morimatsu K et al (2017) Characterization of high hydrostatic pressure-injured Bacillus subtilis cells. Biosci Biotechnol Biochem 81(6):1235–1240
Welch TJ, Farewell A, Neidhardt FC et al (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175(22):7170–7177
Aertsen A, Vanoirbeek K, De Spiegeleer P et al (2004) Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 70(5):2660–2666
Nguyen HTM, Akanuma G, Tu HTM et al (2020) Ribosome reconstruction during recovery from high hydrostatic pressure-induced injury in Bacillus subtilis. Appl Environ Microbiol 86(1):e01640-e1719. https://doi.org/10.1128/AEM.01640-19
Zundel MA, Basturea GN, Deutscher MP (2009) Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15(5):977–983
Kaplan R, Apirion D (1975) The fate of ribosomes in Escherichia coli cells starved for a carbon source. J Biol Chem 250(5):1854–1863
Davis BD, Luger SM, Tai PC (1986) Role of ribosome degradation in the death of starved Escherichia coli cells. J Bacteriol 166(2):439–445
Kimura K, Inaoka T, Yamamoto K (2018) Metabolome analysis of Escherichia coli ATCC25922 cells treated with high hydrostatic pressure at 400 and 600 MPa. J Biosci Bioeng 126(5):611–616
Pandya Y, Jewett FF Jr, Hoover DG (1995) Concurrent effects of high hydrostatic pressure, acidity and heat on the destruction and injury of yeasts. J Food Prot 58(3):301–304
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Yamamoto, K., Zhang, X., Inaoka, T. et al. Bacterial Injury Induced by High Hydrostatic Pressure. Food Eng Rev 13, 442–453 (2021). https://doi.org/10.1007/s12393-020-09271-8
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DOI: https://doi.org/10.1007/s12393-020-09271-8
Keywords
- High hydrostatic pressure
- Bacteria
- Injury
- Recovery
- Mechanism
- Detection