Abstract
Consumer demand for improved quality and fresh-like food products has led to the development of new nonthermal preservation methods. High pressure processing (HPP) is currently the novel nonthermal technology best established in the food processing industry. However, many potential HPP applications would require long treatment times to ensure an adequate inactivation level of pathogens and spoilage microorganisms. High hydrostatic pressure and the addition of essential oils (EOs) have similar effects on microbial structures and thus they may act synergistically on the inactivation of microorganisms. Therefore, the combination of high hydrostatic pressure with EOs is a promising alternative to expand the HPP food industry. In this work, findings on this scarcely investigated hurdle option have been reviewed with a focus on the mechanisms involved. The main mechanisms involved are as follows: (1) membrane permeability induced by HPP and EOs facilitating the uptake of EOs by bacterial cells; (2) generation of reactive oxygen species via the Fenton reaction; (3) impairment of the proton motive force and electron flow; and (4) disruption of the protein–lipid interaction at the cell membrane altering numerous cellular functions. The effectiveness of a specific EO in enhancing the microbial inactivation level achieved by HPP treatments depends on the microbial ecology of the food product, the molecular mechanisms of the microbial inactivation by HPP, and the mode of action of the EO being used.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Adegoke GO, Iwahashi H, Komatsu Y (1997) Inhibition of Saccharomyces cerevisiae by combination of hydrostatic pressure and monoterpenes. J Food Sci 62(2):404–405
Aertsen A, De Spiegeleer P, Vanoirbeek K, Lavilla M, Michiels CW (2005) Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 71:2226–2231
Aertsen A, Vanoirbeek K, De Spiegeleer P, Sermon J, Hauben K, Farewell A, Nystrom T, Mivhiels CW (2004) Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 70:2660–2666
Ait-Ouazzou A, Cherrat L, Espina L, Lorán S, Rota C, Pagán R (2011) The antimicrobial activity of hydrophobic essential oil constituents acting alone or in combined processes of food preservation. Innov Food Sci Emerg Technol 12:320–329
Angioni A, Barra A, Coroneo V, Dessi S, Cabras P (2006) Chemical composition, seasonal variability, and antifungal activity of Lavandula stoechas L. ssp stoechas essential oils from stem/leaves and flowers. J Agric Food Chem 54:4364–4370
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475
Benito A, Ventoura G, Casadei M, Robinson T, Mackey B (1999) Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat, and other stresses. Appl Environ Microbiol 65:1564–1569
Bors WASM (1987) Radical scavenging by flavonoids antioxidants. Free Radic Res Commun 2:289–294
Boyle W (1955) Spices and essential oils as preservatives. Am Perfumer Essent Oil Rev 66:25–28
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253
Carson CF, Mee BJ, Riley TV (2002) Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob Agents Chemother 46:1914–1920
Casadei MA, Manas P, Niven G, Needs E, Mackey BM (2002) Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Appl Environ Microbiol 68:5965–5972
Cebrián G, Michiels CW, Mañas P, Condón S (2010) Biological approach to modeling of Staphylococcus aureus high-hydrostatic-pressure inactivation kinetics. Appl Environ Microbiol 76:6982–6990
Chaibi A, Ababouch LH, Belasri K, Boucetta S, Busta FF (1997) Inhibition of germination and vegetative growth of Bacillus cereus T and Clostridium botulinum 62A spores by essential oils. Food Microbiol 14:161–174
Cheftel JC (1995) High pressure, microbial inactivation and food preservation. Comptes Rendus de l’Academie d’Agriculture de France 81(1):13–38
Cheftel JC (1995) Review: high-pressure, microbial inactivation and food preservation. Food Sci Technol Int 1:75–90
Chung YK, Vurma M, Turek EJ, Chism GW, Yousef AE (2005) Inactivation of barotolerant Listeria monocytogenes in sausage by combination of high-pressure processing and food-grade additives. J Food Prot 68:744–750
Chung YK, Yousef AE (2008) Inactivation of barotolerant strains of Listeria monocytogenes and Escherichia coli O157:H7 by ultra high pressure and tert-butylhydroquinone combination. J Microbiol 46:289–294
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
Cox SD, Mann CM, Markham JL, Bell HC, Gustafson JE, Warmington JR, Wyllie SG (2000) The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 88:170–175
Delaquis PJ, Stanich K, Girard B, Mazza G (2002) Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils. Int J Food Microbiol 74:101–109
Denyer SP, Hugo WB (1991) Biocide-induced damage to the bacterial cytoplasmic membrane. The society for applied bacteriology, technical series. Oxford Blackwell Scientific Publication, Oxford, UK
Evrendilek GA, Balasubramaniam VM (2011) Inactivation of Listeria monocytogenes and Listeria innocua in yogurt drink applying combination of high pressure processing and mint essential oils. Food Control 22:1435–1441
Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966
Gustafson JE, Liew YC, Chew S, Markham J, Bell HC, Wyllie SG, Warmington JR (1998) Effects of tea tree oil on Escherichia coli. Lett Appl Microbiol 26:194–198.
Hauben KJ, Bartlett DH, Soontjens CC, Cornelis K, Wuytack EY, Michiels CW (1997) Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl Environ Microbiol 63:945–950
Helander IM, Alakomi HL, Latva-Kala K, Matilla-Sandholm T, Pol I, Smid EJ, Gorris LGM, von Wright A (1998) Characterization of the action of selected essential oil components on gram-negative bacteria. J Agric Food Chem 46:3590–3595
Hite BH (1899) The effects of pressure in the preservation of milk. Bull West Va University Agric Experiment Station Morgant 58:15–35
Juven BJ, Kanner J, Schved F, Weisslowicz H (1994) Factors that interact with the antibacterial action of thyme essential oil and its active constituents. J Appl Bacteriol 76:626–631
Kalchayanand N, Dunne CP, Sikes A, Ray B (2003) Inactivation of bacterial spores by combined action of hydrostatic pressure and bacteriocins in roast beef. J Food Saf 23:219–231
Kalchayanand N, Sikes A, Dunne CP, Ray B (1998) Interaction of hydrostatic pressure, time and temperature of pressurization and pediocin AcH on inactivation of foodborne bacteria. J Food Prot 61:425–431
Karatzas AK, Bennik MHJ, Smid EJ, Kets EPW (2000) Combined action of S-carvone and mild heat treatment on Listeria monocytogenes Scott A. J Appl Microbiol 89:296–301
Karatzas AK, Kets EPW, Smid EJ, Bennik MHJ (2001) The combined action of carvacrol and high hydrostatic pressure on Listeria monocytogenes Scott A. J Appl Microbiol 90:463–469
Kitching JA (1957) Effects of high hydrostatic pressures on the activity of flagellates and ciliates. J Exp Biol 34:494–510
Klotz B, Mañas P, Mackey BM (2010) The relationship between membrane damage, release of protein and loss of viability in Escherichia coli exposed to high hydrostatic pressure. Int J Food Microbiol 137:214–220
Klotz B, Pyle DL, Mackey BM (2007) New mathematical modeling approach for predicting microbial inactivation by high hydrostatic pressure. Appl Environ Microbiol 73(8):2468–2478
Koseki S, Yamamoto K (2007) Modelling the bacterial survival/death interface induced by high pressure processing. Int J Food Microbiol 116(1):136–143
Lado BH, Yousef AE (2002) Alternative food-preservation technologies: efficacy and mechanisms. Microb Infect 4:433–440
Lambert RJW, Skandamis PN, Coote PJ, Nychas GJE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol 91:453–462
Lee J, Kaletunç G (2010) Inactivation of Salmonella Enteritidis strains by combination of high hydrostatic pressure and nisin. Int J Food Microbiol 140:49–56
Leistner L (1992) Food preservation by combined methods. Food Res Int 25:151–158
Lisbalchin M, Deans SG (1997) Bioactivity of selected plant essential oils against Listeria monocytogenes. J Appl Microbiol 82:759–762
Mackey BM, Forestiere K, Isaacs N (1995) Factors affecting the resistance of Listeria monocytogenes to high hydrostatic pressure. Food Biotechnol 9:1–11
Malone AS, Chung YK, Yousef AE (2006) Genes of Escherichia coli O157:H7 that are involved in high-pressure resistance. Appl Environ Microbiol 72:2661–2671
Malone AS, Chung YK, Yousef AE (2008) Proposed mechanism of inactivating Escherichia coli O157:H7 by ultra-high pressure in combination with tert-butylhydroquinone. J Appl Microbiol 105:2046–2057
Mañas P, Mackey BM (2004) Morphological and physiological changes induced by high hydrostatic pressure in exponential- and stationary-phase cells of Escherichia coli: relationship with cell death. Appl Environ Microbiol 70:1545–1554
Mañas P, Pagán R (2005) Microbial inactivation by new technologies of food preservation. J Appl Microbiol 98:1387–1399
Mejlholm O, Dalgaard P (2002) Antimicrobial effect of essential oils on the seafood spoilage micro-organism Photobacterium phosphoreum in liquid media and fish products. Lett Appl Microbiol 34:27–31
Monzote L, Montalvo AM, Almanonni S, Scull R, Miranda M, Abreu J (2006) Activity of the essential oil from Chenopodium ambrosioides grown in cuba against Leishmania amazonensis. Chemotherapy 52:130–136
Mújica-Paz H, Valdez-Fragoso A, Tonello Samson C, Welti-Chanes J, Torres JA (2011) High-pressure processing technologies for the pasteurization and sterilization of foods. Food Bioprocess Technol 4(6):969–985. doi:10.1007/s11947-011-0543-5
O’Byrne CP, Booth IR (2002) Osmoregulation and its importance to food-borne microorganisms. Int J Food Microbiol 74:203–216
Ogawa T, Matsuzaki H, Isshiki K (1998) Bacterial control by hydrostatic pressure treatment with addition of allyl isothiocyanate. Nippon Shokuhin Kagaku Kogaku Kaishi 45(6):349–356
Pagán R, Mackey B (2000) Relationship between membrane damage and cell death in pressure-treated Escherichia coli cells: differences between exponential- and stationary-phase cells and variation among strains. Appl Environ Microbiol 66:2829–2834
Palhano FL, Vilches TTB, Santos RB, Orlando MTD, Ventura JA, Fernandes PMB (2004) Inactivation of Colletotrichum gloeosporioides spores by high hydrostatic pressure combined with citral or lemongrass essential oil. Int J Food Microbiol 95:61–66
Patterson MF (2005) A review: microbiology of pressure-treated foods. J Appl Microbiol 98:1400–1409
Patterson MF, Quinn M, Simpson R, Gilmour A (1995) Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate buffered saline and foods. J Food Prot 58:524–529
Phillips CA, Duggan J (2002) The effect of temperature and citric acid, alone, and in combination with nisin, on the growth of Arcobacter butzleri in culture. Food Control 13:463–468
Raso J, Barbosa-Cánovas GV, Swanson BG (1998) Sporulation temperature affects initiation of germination and inactivation by high hydrostatic pressure of Bacillus cereus. J Appl Microbiol 85:17–24
Rasooli I, Rezaei MB, Allameh A (2006) Ultrastructural studies on antimicrobial efficacy of thyme essential oils on Listeria monocytogenes. Int J Infect Dis 10:236–241
Rastogi NK, Raghavarao KSMS, Balasubramaniam VM, Niranjan K, Knorr D (2007) Opportunities and challenges in high pressure processing of foods. Crit Rev Food Sci Nutr 47(1):69–112
San Martin MF, Barbosa-Cánovas GV, Swanson BG (2002) Food processing by high hydrostatic pressure. Crit Rev Food Sci Nutr 42(6):627–645
Saucedo-Reyes D, Marco-Celdrán A, Pina-Pérez MC, Rodrigo D, Martínez-López A (2009) Modeling survival of high hydrostatic pressure treated stationary- and exponential-phase Listeria innocua cells. Innov Food Sci Emerg Technol 10:135–141
Shahidi F, Zhong Y (2010) Novel antioxidants in food quality preservation and health promotion. Eur J Lipid Sci Technol 112:930–940
Sikkema J, Debont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269:8022–8028
Sikkema J, Debont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222
Skandamis PN, Nychas GJE (2000) Development and evaluation of a model predicting the survival of Escherichia coli O157:H7 NCTC 12900 in homemade eggplant salad at various temperatures, pHs, and oregano essential oil concentrations. Appl Environ Microbiol 66:1646–1653
Skandamis PN, Nychas GJE (2001) Effect of oregano essential oil on microbiological and physico-chemical attributes of minced meat stored in air and modified atmospheres. J Appl Microbiol 91:1011–1022
Smid EJ, Gorris LGM (1999) Natural antimicrobials for food preservation. In: Rahman MS (ed) Handbook of food preservation. Marcel Dekker Inc., New York, NY, pp 285–308
Somolinos M, García D, Pagán R, Mackey B (2008) Relationship between sublethal injury and microbial inactivation by the combination of high hydrostatic pressure and citral or tert-butyl hydroquinone. Appl Environ Microbiol 74:7570–7577
Tassou CC, Drosinos EH, Nychas GJE (1995) Effects of essential oil from mint (Mentha-piperita) on Salmonella Enteritidis and Listeria monocytogenes in model food systems at 4 degrees and 10 degrees. J Appl Bacteriol 78:593–600
Tay A, Shellhammer TH, Yousef AE, Chism GW (2003) Pressure death and tailing behavior of Listeria monocytogenes strains having different barotolerances. J Food Prot 66:2057–2061
Torres JA, Sanz PD, Otero L, Pérez Lamela C, Saldaña MDA (2009) Engineering principles to improve food quality and safety by high pressure processing. In: Ortega-Rivas E (ed) Processing effects on safety and quality of foods. Contemporary food engineering. CRC Taylor & Francis, Inc., Boca Raton, FL, pp 379–414
Torres JA, Velazquez G (2005) Commercial opportunities and research challenges in the high pressure processing of foods. J Food Eng 67(1–2):95–112
Tribst AAL, Franchi MA, Cristianini M (2008) Ultra-high pressure homogenization treatment combined with lysozyme for controlling Lactobacillus brevis contamination in model system. Innov Food Sci Emerg Technol 9:265–271
Tsigarida E, Skandamis P, Nychas GJE (2000) Behaviour of Listeria monocytogenes and autochthonous flora on meat stored under aerobic, vacuum and modified atmosphere packaging conditions with or without the presence of oregano essential oil at 5 degrees C. J Appl Microbiol 89:901–909
Ulmer HM, Gaenzle MG, Vogel RF (2000) Effects of high pressure on survival and metabolic activity of Lactobacillus plantarum TW1.460. Appl Environ Microbiol 66:3966–3973
Ultee A, Kets EPW, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65:4606–4610
Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411
Vanlint D, Mitchell R, Bailey E, Meersman F, McMillan PF, Michiels CW, Aertsen A (2011) Rapid acquisition of gigapascal-high-pressure resistance by Escherichia coli. MBio 2(1):e00130–00110. doi:10.1128/mBio.00130-10
Vasseur C, Baverel L, Hebraud M, Labadie J (1999) Effect of osmotic, alkaline, acid or thermal stresses on the growth and inhibition of Listeria monocytogenes. J Appl Microbiol 86:469–476
Vurma M, Chung YK, Shellhammer TH, Turek EJ, Yousef AE (2006) Use of phenolic compounds for sensitizing Listeria monocytogenes to high-pressure processing. Int J Food Microbiol 106:263–269
Welch TJ, Farewell A, Neidhardt FC, Bartlett DH (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175:7170–7177
Wendakoon CN, Sakaguchi M (1993) Combined effect of sodium chloride and clove on growth and biogenic amine formation of Enterobacter aerogenes in mackerel muscle extract. J Food Prot 56:410–413
Wouters PC, Glaasker E, Smelt JPPM (1998) Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum. Appl Environ Microbiol 64:509–514
Yayanos AA, Pollard EC (1969) A study of the effects of hydrostatic pressure on macromolecular synthesis in Escherichia coli. Biophys J 9:1464–1482
Yin MC, Cheng WS (2003) Antioxidant and antimicrobial effects of four garlic-derived organosulfur compounds in ground beef. Meat Sci 63:23–28
Zobell CE, Cobert AB (1963) Filament formation by Escherichia coli at increased hydrostatic pressures. J Bacteriol 87:710–719
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gayán, E., Torres, J.A. & Paredes-Sabja, D. Hurdle Approach to Increase the Microbial Inactivation by High Pressure Processing: Effect of Essential Oils. Food Eng Rev 4, 141–148 (2012). https://doi.org/10.1007/s12393-012-9055-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12393-012-9055-y