journal article·2023-01-16Open access

Pasteurization of Food and Beverages by High Pressure Processing (HPP) at Room Temperature: Inactivation of Staphylococcus aureus, Escherichia coli, Listeria monocytogenes, Salmonella, and Other Microbial Pathogens

Filipa Vinagre M. Silva, Evelyn Evelyn

Applied Sciences· Volume 13· Issue 2

Abstract

Vegetative pathogens actively grow in foods, metabolizing and dividing their cells. They have consequently become a focus of concern for the food industry, food regulators and food control agencies. Although much has been done by the food industry and food regulatory agencies, foodborne outbreaks are still reported globally, causing illnesses, hospitalizations, and in certain cases, deaths, together with product recalls and subsequent economic losses. Major bacterial infections from raw and processed foods are caused by Escherichia coli serotype O157:H7, Salmonella enteritidis, and Listeria monocytogenes. High pressure processing (HPP) (also referred to as high hydrostatic pressure, HHP) is a non-thermal pasteurization technology that relies on very high pressures (400–600 MPa) to inactivate pathogens, instead of heat, thus causing less negative impact in the food nutrients and quality. HPP can be used to preserve foods, instead of chemical food additives. In this study, a review of the effect of HPP treatments on major vegetative bacteria in specific foods was carried out. HPP at 600 MPa, commonly used by the food industry, can achieve the recommended 5–8-log reductions in E. coli, S. enteritidis, L. monocytogenes, and Vibrio. Staphylococcus aureus presented the highest resistance to HPP among the foodborne vegetative pathogens investigated, followed by E. coli. More susceptible L. monocytogenes and Salmonella spp. bacteria were reduced by 6 logs at pressures within 500–600 MPa. Vibrio spp. (e.g., raw oysters), Campylobacter jejuni, Yersinia enterocolitica, Citrobacter freundii and Aeromonas hydrophila generally required lower pressures (300–400 MPa) for inactivation. Bacterial species and strain, as well as the food itself, with a characteristic composition, affect the microbial inactivation. This review demonstrates that HPP is a safe pasteurization technology, which is able to achieve at least 5-log reduction in major food bacterial pathogens, without the application of heat.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Microbial Inactivation Methods · Listeria monocytogenes in Food Safety · Food Safety and Hygiene

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

LEAF—Linking Landscape, Environment, Agriculture and Food, Associated Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal

Department of Chemical Engineering, University of Riau, Pekanbaru 28293, Indonesia

Funding

Fundação para a Ciência e a Tecnologia · Linking Landscape, Environment, Agriculture and Food, Research Unit

References (100+)

Show source-provided references
1. Simpson, R. (2009). Principles of thermal processing: Pasteurization. Engineering Aspects of Thermal Food Processing, CRC Press.10.1201/9781420058598 ↗
2. Batt, C.A., and Tortorello, M.L. (2014). Thermal processes: Pasteurization. Encyclopedia of Food Microbiology, Elsevier.
3. Rai, V.R., and Bai, J.A. (2017). Inactivation of pathogenic microorganisms in foods by high-pressure processing. In Food Safety and Protection, CRC Press.10.1201/9781315153414 ↗
4. Houška, M., and Silva, F.V.M. (2018). High pressure processing effect on microorganisms in fruit and vegetable products. High Pressure Processing of Fruit and Vegetable Juices, CRC Press.10.1201/9781315121123 ↗
5. EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), Koutsoumanis, K., Alvarez-Ordóñez, A., Bolton, D., Bover-Cid, S., Chemaly, M., Davies, R., De Cesare, A., Herman, L., and Hilbert, F. (2022). The efficacy and safety of high-pressure processing of food. EFSA J., 20, 7128.10.2903/j.efsa.2022.7128 ↗
6. Strawberry puree processed by thermal, high pressure, or power ultrasound: Process energy requirements and quality modeling during storage10.1177/1082013216685485 ↗
7. Houška, M., and Silva, F.V.M. (2018). High pressure processing effect on nutrients and their stability. High Pressure Processing of Fruit and Vegetable Juices, CRC Press.
8. Nonthermal pasteurization of beer by high pressure processing: Modelling the inactivation of Saccharomyces cerevisiae ascospores in different alcohol beers10.1080/08957959.2016.1190354 ↗
9. SO2, high pressure processing and pulsed electric field treatments of red wine: Effect on sensory, Brettanomyces inactivation and other quality parameters during one year storage10.1016/j.ifset.2018.06.016 ↗
10. Houška, M., and Silva, F.V.M. (2018). Sensory properties of high pressure treated fruit and vegetable juices. High Pressure Processing of Fruit and Vegetable Juices, CRC Press.10.1201/9781315121123 ↗
11. Houška, M., and Silva, F.V.M. (2018). Health active components in fruit/vegetable juices treated by high pressure. High Pressure Processing of Fruit and Vegetable Juices, CRC Press.10.1201/9781315121123 ↗
12. Houška, M., Silva, F.V.M., Buckow, R., Terefe, N.S., and Tonello, C. (2022). High pressure processing applications in plant foods. Foods, 11.10.3390/foods11020223 ↗
13. Kinetics of flavour and aroma changes in thermally processed cupuaçu (Theobroma grandiflorum) pulp10.1002/(SICI)1097-0010(20000501)80:6<783::AID-JSFA622>3.0.CO;2-R ↗
14. High pressure processing inactivation of Brettanomyces bruxellensis in seven different table wines10.1016/j.foodcont.2017.05.028 ↗
15. High pressure inactivation of Brettanomyces bruxellensis in red wine10.1016/j.fm.2016.11.020 ↗
16. Houska, M., and Silva, F.V.M. (2018). High Pressure Processing of Fruit and Vegetable Products, CRC Press Taylor and Francis Group.10.1201/9781315121123 ↗
17. (2022, November 24). HPP Technology Applications. Available online: https://www.hiperbaric.com/en/hpp-technology/hpp-applications/.
18. Pasteurization of beer by non-thermal technologies10.3389/frfst.2021.798676 ↗
19. Dynamic structural changes in microbial membranes in response to high hydrostatic pressure analyzed using time-resolved fluorescence anisotropy measurement10.1016/j.bpc.2013.05.005 ↗
20. Bacteria, mould and yeast spore inactivation studies by scanning electron microscope observations10.1016/j.ijfoodmicro.2017.10.008 ↗
21. Silva, F.V.M., and van Wyk, S. (2021). Emerging non-thermal technologies as alternative to SO2 for the production of wine. Foods, 10.10.3390/foods10092175 ↗
22. Recent advances in the use of high pressure as an effective processing technique in the food industry10.1007/s11947-007-0007-0 ↗
23. High pressure thermal processing for the inactivation of Clostridium perfringens spores in beef slurry10.1016/j.ifset.2015.12.021 ↗
24. Modeling the inactivation of psychrotrophic Bacillus cereus spores in beef slurry by 600MPa HPP combined with 38–70 °C: Comparing with thermal processing and estimating the energy requirements10.1016/j.fbp.2016.05.003 ↗
25. Alicyclobacillus acidoterrestris spore inactivation by high pressure combined with mild heat: Modelling the effect of temperature and soluble solids10.1016/j.foodcont.2016.08.034 ↗
26. Heat assisted HPP for the inactivation of bacteria, molds and yeast spores in foods: Log reductions and mathematical models10.1016/j.tifs.2019.03.016 ↗
27. Microbiological food safety assessment of high hydrostatic pressure processing: A review10.1016/j.lwt.2010.11.001 ↗
28. Modeling the protective effect of aw and fat content on the high pressure resistance of Listeria monocytogenes in dry-cured ham10.1016/j.foodres.2015.05.052 ↗
29. Modelling the impact of water activity and fat content of dry-cured ham on the reduction of Salmonella enterica by high pressure processing10.1016/j.meatsci.2016.09.014 ↗
30. Centers for Disease Control and Prevention (CDC) (2022, November 24). Foodborne Germs and Illnesses, Available online: http://www.cdc.gov/foodsafety/foodborne-germs.html.
31. Centers for Disease Control and Prevention (CDC) (2019). Surveillance for Foodborne Disease Outbreaks, United States, 2017, Annual Report, U.S. Department of Health and Human Services, CDC.
32. Centers for Disease Control and Prevention (CDC) (2022, November 24). Salmonella (Non-Typhoidal). Available online: https://www.who.int/en/news-room/fact-sheets/detail/salmonella-(non-typhoidal).
33. European Food Safety Authority, and European Centre for Disease Prevention and Control (2018). Multi-country outbreak of Listeria monocytogenes serogroup IVb, multi-locus sequence type 6, infections linked to frozen corn and possibly to other frozen vegetables—First update. EFSA Support. Publ., 15, 1448E.10.2903/sp.efsa.2018.EN-1448 ↗
34. Heating milk for microbial destruction: A historical outline and update10.4315/0362-028X-41.2.122 ↗
35. Inactivation of Mycobacterium paratuberculosis in cows’ milk at pasteurization temperatures10.1128/aem.62.2.631-636.1996 ↗
36. Mycobacterium paratuberculosis and milk
37. Coxiella burnetii and milk pasteurization: An early application of the precautionary principle?10.1017/S0950268806005978 ↗
38. Psychrotrophy and foodborne Salmonella10.1016/0168-1605(91)90004-9 ↗
39. Penfield, M.P., Campbell, A.M., and Penfield, M.P. (1990). Experimental Food Science, Academic Press.10.1016/B978-0-12-157920-3.50013-2 ↗
40. (2022, November 24). Implementation of the FDA Food Safety Modernization Act (FSMA, P.L. 111–353), Available online: https://www.govinfo.gov/content/pkg/PLAW-111publ353/pdf/PLAW-111publ353.pdf.
41. Houška, M., and Silva, F.V.M. (2018). Regulatory aspects of high pressure processed foods in North America, Europe, Asia, New Zealand and Australia. High Pressure Processing of Fruit and Vegetable Juices, CRC Press.
42. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk10.1016/0168-1605(88)90057-8 ↗
43. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: Estimation of enterotoxin A in the incriminated milk and powdered skim milk10.1017/S0950268802007951 ↗
44. Outbreak of staphylococcal food intoxication after consumption of pasteurized milk products, June 2007, Austria. Wien10.1007/s00508-008-1132-0 ↗
45. First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 200910.2807/ese.15.13.19528-en ↗
46. Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation10.1111/j.1574-6976.2011.00311.x ↗
47. Effects of high hydrostatic pressure on characteristics of pork slurries and inactivation of microorganisms associated with meat and meat products10.1016/0168-1605(91)90071-V ↗
48. Inactivation and recovery of bacterial strains, individually and mixed, in milk after high pressure processing10.1016/j.idairyj.2021.105147 ↗
49. Use of hydrostatic pressure for inactivation of microbial contaminants in cheese10.1128/AEM.66.11.4890-4896.2000 ↗
50. Bacillus cereus spores and Staphylococus aureus sub. aureus vegetative cells inactivation in human milk by high-pressure processing10.1016/j.foodcont.2020.107212 ↗
51. The combined effect of high hydrostatic pressure and mild heat on inactivation of pathogens in milk and poultry10.4315/0362-028X-61.4.432 ↗
52. Sensitivity of Staphylococcus aureus and Lactobacillus helveticus in ovine milk subjected to high hydrostatic pressure10.3168/jds.S0022-0302(99)75332-4 ↗
53. Comparison of nonthermal decontamination methods to improve the safety for raw beef consumption10.4315/JFP-21-243 ↗
54. Jarzynka, S., Strom, K., Barbarska, O., Pawlikowska, E., Minkiewicz-Zochniak, A., Rosiak, E., Oledzka, G., and Wesolowska, A. (2021). Combination of high-pressure processing and freeze-drying as the most effective techniques in maintaining biological values and microbiological safety of donor milk. Int. J. Environ. Res. Public Health, 18.10.3390/ijerph18042147 ↗
55. The combined effect of high hydrostatic pressure, heat and bacteriocins on inactivation of foodborne pathogens in milk and orange juice10.1023/A:1008936607413 ↗
56. New mild technologies in meat processing: High pressure as a model technology10.1016/S0309-1740(02)00122-5 ↗
57. Centers for Disease Control and Prevention (CDC) (2022, November 24). Reports of Selected E. coli Outbreak Investigations, Available online: http://www.cdc.gov/ecoli/outbreaks.html.
58. Survival of Escherichia coli O157:H7 in mayonnaise and mayonnaise-based sauces at room and refrigerated temperatures10.4315/0362-028X-57.7.629 ↗
59. Growth and survival of Escherichia coli O157:H7 under acidic conditions10.1128/aem.61.1.382-385.1995 ↗
60. Acid adaptation and temperature effect on the survival of E. coli O157:H7 in acidic fruit juice and lactic fermented milk product10.1016/S0168-1605(01)00538-4 ↗
61. Centers for Disease Control and Prevention (CDC) (1996). Outbreak of Escherichia coli O157:H7 infections associated with drinking unpasteurized commercial apple juice--British Columbia, California, Colorado, and Washington, October 1996. MMWR Morb. Mortal. Wkly. Rep., 45, 975.
62. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice10.7326/0003-4819-130-3-199902020-00005 ↗
63. Escherichia coli O157:H7 acid tolerance and survival in apple cider10.4315/0362-028X-57.6.460 ↗
64. Survival of Escherichia coli O157:H7 and Salmonella spp. in acidic condiments10.4315/0362-028X-60.7.751 ↗
65. Verotoxin producing Escherichia coli O157 infections associated with the consumption of yoghurt10.1017/S0950268800056880 ↗
66. Food borne pathogen Escherichia coli O157: H7 History, sources of transmission, symptoms, detection and prevention
67. Centers for Disease Control and Prevention (CDC) (2022, November 24). E. coli (Escherichia coli): General Information, Available online: http://www.cdc.gov/ecoli/general/.
68. Effect of high pressure processing on the safety, shelf life and quality of raw milk10.1016/j.ifset.2019.01.009 ↗
69. The use of high-pressure processing (HPP) to improve the safety and quality of raw coconut (Cocos nucifera L) water10.1016/j.ijfoodmicro.2020.108697 ↗
70. Modeling the inactivation of Escherichia coli O157:H7 and uropathogenic E. coli in ground beef by high pressure processing and citral10.1016/j.foodcont.2016.09.017 ↗
71. Populations of aerobic mesophils and inoculated E. coli during storage of fresh goat’s milk cheese treated with high pressure10.4315/0362-028X-59.6.582 ↗
72. Inactivation of Escherichia coli O157:H7 in orange juice using a combination of high pressure and mild heat10.4315/0362-028X-62.3.277 ↗
73. High pressure destruction kinetics of spoilage and pathogenic microorganisms in mango juice10.1111/j.1745-4549.2011.00559.x ↗
74. Inactivation and injury of pressure-resistant strains of Escherichia coli O157 and Listeria monocytogenes in fruit juices10.1046/j.1365-2672.2001.01402.x ↗
75. Vicario, T. (2015). Listeria monocytogenes and ready-to-eat-meat-based food products: Incidence and control. Listeria Monocytogenes Incidence, Growth Behavior, and Control, Nova Science Publishers Inc.
76. Human listeriosis in England, 2001–2007: Association with neighbourhood deprivation10.2807/ese.15.27.19609-en ↗
77. CDC (2022, November 24). Listeriosis: Diagnosis, Available online: http://www.cdc.gov/listeria/diagnosis.html.
78. CDC (2022, November 24). Listeria Outbreaks, Available online: http://www.cdc.gov/listeria/outbreaks/.
79. EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards) (2018). Scientific Opinion on the Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J., 16, 5134.10.2903/j.efsa.2018.5134 ↗
80. EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), Koutsoumanis, K., Alvarez-Ordóñez, A., Bolton, D., Bover-Cid, S., Chemaly, M., Davies, R., De Cesare, A., Herman, L., and Hilbert, F. (2020). The public health risk posed by Listeria monocytogenes in frozen fruit and vegetables, including herbs, blanched during processing. EFSA J., 18, 6092.10.2903/j.efsa.2020.6092 ↗
81. Effects of high pressure processing and hot water pasteurization of cooked sausages on inactivation of inoculated Listeria monocytogenes, natural populations of lactic acid bacteria, Pseudomonas spp., and coliforms and their recovery during storage at 4 and 10 °C10.4315/0362-028X.JFP-18-024 ↗
82. Efficiency of high pressure treatment for destruction of Listeria monocytogenes in goat cheese from raw milk
83. Effects of combined application of high-pressure processing and active coatings on phenolic compounds and microbiological and physicochemical quality of apple cubes10.1002/jsfa.11065 ↗
84. Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods10.4315/0362-028X-58.5.524 ↗
85. Centers for Disease Control and Prevention (CDC) (2022, November 24). Reports of Selected Salmonella Outbreak Investigations, Available online: https://www.cdc.gov/salmonella/outbreaks.html.
86. The role of hens’ eggs in outbreaks of salmonellosis in north Spain10.1016/0168-1605(89)90072-X ↗
87. Summer meeting 2007–the problems with fresh produce: An overview10.1111/j.1365-2672.2008.03746.x ↗
88. Salmonellosis outbreaks in the United States due to fresh produce: Sources and potential intervention measures10.1089/fpd.2008.0232 ↗
89. Baron, S. (1996). Salmonella. Medical Microbiology, University of Texas Medical Branch.
90. Behravesh, C.B., Lynch, M., and Schlundt, J. (2008). Salmonellosis, Control of Communicable Diseases Manual, United Book Press.
91. Effect of high pressure processing on the survival of Salmonella Enteritidis and shelf-life of chicken fillets10.1016/j.fm.2017.08.019 ↗
92. Application of high pressure processing for prevention of greenish-gray yolks and improvement of safety and shelf-life of hard-cooked peeled eggs10.1016/j.ifset.2017.09.016 ↗
93. Destruction of Salmonella Enteritidis inoculated in liquid whole egg by high hydrostatic pressure: Comparative study in selective and non-selective media10.1006/fmic.1998.0248 ↗
94. Effect of hydrostatic pressure pulsing on the inactivation of Salmonella Enteritidis in liquid whole egg10.1089/fpd.2007.0055 ↗
95. Effects of high hydrostatic pressure on heat resistant and heat sensitive strains of Salmonella10.1111/j.1365-2621.1989.tb05156.x ↗
96. Reduction of Salmonella spp. populations in Italian salami during production process and high pressure processing treatment: Validation of processes to export to the U.S10.1016/j.meatsci.2019.06.005 ↗
97. High pressure processing at ultra-low temperatures: Inactivation of foodborne bacterial pathogens and quality changes in frozen fish fillets10.1016/j.ifset.2021.102811 ↗
98. Jay, J.M. (2000). High-temperature food preservation and characteristics of thermophilic microorganisms. Modern Food Microbiology, Springer.10.1007/978-1-4615-4427-2_17 ↗
99. Centers for Disease Control and Prevention (CDC) (2022, November 24). Vibrio Species Causing Vibriosis: Symptoms and Outbreaks, Available online: https://www.cdc.gov/vibrio/outbreaks.html.
100. Emergence of a new Vibrio parahaemolyticus serotype in raw oysters: A prevention quandary10.1001/jama.284.12.1541 ↗