Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components

Frontiers in Microbiology

Volumn 3, Issue JAN, 2012, Pages

  Hyldgaard, Morten ^a,b   Mygind, Tina ^b   Meyer, Rikke Louise ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b DANISCO A S   (Denmark)

Author keywords

Antimicrobial; Carvacrol; Mode of action; Phenylpropenes; Synergy; Terpenes; Terpenoids; Thymol

Indexed keywords

EID: 84866940077     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00012     Document Type: Article

References (192)

1. Ahmad, A., Khan, A., Akhtar, F., Yousuf, S.,Xess, I., Khan, L., and Manzoor, N. (2011). Fungicidal activity of thymol and carvacrol by disrupting ergos-terol biosynthesis and membrane integrity against Candida. Eur. J. Clin. Microbiol. Infect Dis. 30,41-50.
2. Ahmadifar, E., Falahatkar, B., and Akrami, R. (2011). Effects of dietary thymol-carvacrol on growth performance, hematological parameters and tissue composition of juvenile rainbowtrout, Oncorhynchus mykiss. J. Appl. Ichthyol. 27, 1057-1060.
3. Ahn, E. S. (2001). Observation of bactericidal effect of allyl isothiocyanate on Listeria monocytogenes. Food Sci. Biotechnol. 10,31-35.
4. Ahvenainen, R. (2003). Novel food Packaging Techniques. Cambridge: CRC Press, Woodhead Publishing Limited.
5. Ait-Ouazzou, A., Cherrat, L., Espina, L., Lorán, S., Rota, C., and 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.
6. Alessandrini, A., and Facci, P. (2005). AFM: a versatile tool in biophysics. Meas. Sci. Technol. 16, R65-R92.
7. Aligiannis, N., Kalpoutzakis, E., Mitaku, S., and Chinou, I. B. (2001). Composition and antimicrobial activity of the essential oils of two Origanum species. J. Agric. Food Chem. 49,4168-4170.
8. Alzoreky, N. S., and Nakahara, K. (2003). Antibacterial activity of extracts from some edible plants commonly consumed in Asia. Int. J. Food Microbiol. 80, 223-230.
9. Ankri, S., and Mirelman, D. (1999). Antimicrobial properties of allicin from garlic. Microbes Infect. 1, 125-129.
10. Babili, F. E., Bouajila, J., Souchard, J. P., Bertrand, C., Bellvert, F., Fouraste, I., Moulis, C., and Valentin, A. (2011). Oregano: chemical analysis and evaluation of its antimalarial, antioxi-dant, and cytotoxic activities. J. Food Sci. 76,512-518.
11. Bagamboula, C. F., Uyttendaele, M., and Debevere, J. (2004). Inhibitory effect of thyme and basil essential oils, carvacrol, thymol, estragol, linalool and p-cymene towards Shigella son-nei and S. flexneri. Food Microbiol. 21,33-42.
12. Bang, K. H., Lee, D. W., Park, H. M., and Rhee, Y. H. (2000). Inhibition of fungal cell wall synthesizing enzymes by trans-cinnamaldehyde. Biosci. Biotechnol Biochem. 64,1061-1063.
13. Baratta, M. T., Dorman, H. J. D., Deans, S. G., Figueiredo, A. C., Barroso, J. G., and Ruberto, G. (1998). Antimicrobial and antioxidant properties of some commercial essential oils. Flavour Fragr J. 13,235-244.
14. Bassolé, I. H. N., Lamien-Meda, A., Bay-ala, B., Tirogo, S., Franz, C., Novak, J., Nebié, R. C., and Dicko, M. H. (2010). Composition and antimicrobial activities of Lippia multi-flora Moldenke, Mentha xpiperita L. and Ocimum basilicum L. essential oils and their major monoterpene alcohols alone and in combination. Molecules 15, 7825-7839.
15. Ben Arfa, A., Combes, S., Preziosi-Belloy, L., Gontard, N., and Chalier, P. (2006). Antimicrobial activity of carvacrol related to its chemical structure. Lett. Appl. Microbiol. 43, 149-154.
16. Bennis, S., Chami, F., Chami, N., Bouchikhi, T., and Remmal, A. (2004). Surface alteration of Saccharomyces cerevisiae induced by thymol and eugenol. Lett. Appl. Microbiol. 38, 454-458.
17. Block, E. (1992). The organosulfur chemistry of the genus Allium - implications for the organic chemistry of sulfur. Angew. Chem. Int. Ed. Engl. 31,1135-1178.
18. Bouhdid, S., Abrini, J., Amensour, M., Zhiri, A., Espuny M. J., and Manresa, A. (2010). Functional and ultrastructural changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Cinnamomum verum essential oil. J. Appl. Microbiol. 109, 1139-1149.
19. Bouhdid, S., Abrini, J., Zhiri, A., Espuny, M. J., and Manresa, A. (2009). Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil. J. Appl. Microbiol. 106, 1558-1568.
20. Brasseur, R., Deleu, M., Mingeot-Leclercq, M. P., Francius, G., and Dufrene, Y. F. (2008). Probing peptide-membrane interactions using AFM. Surf. Interface Anal. 40, 151-156.
21. Breeuwer, P., Drocourt, J. L., Rom-bouts, F. M., and Abee, T. (1996). A novel method for continuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe 5 (and 6-)-carboxyfluoresceinsuccinimidyl ester. Appl. Environ. Microbiol. 62, 178-183.
22. Brenes, A., and Roura, E. (2010). Essential oils in poultry nutrition: main effects and modes of action. Anim. Feed Sci. Technol. 158,1-14.
23. Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods - a review. Int. J. Food Microbiol. 94,223-253.
24. Burt, S. A., and Reinders, R. D. (2003). Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett. Appl. Microbiol. 36, 162-167.
25. Burt, S. A., Van Der Zee, R., Koets, A. P., De Graaff, A. M., Van Knapen, E, Gaastra, W., Haagsman, H. P., and Veldhuizen, E. J. A. (2007). Car-vacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157:H7. Appl. Environ. Microbiol. 73, 4484-4490.
26. Caballero, B., Trugo, L. C., and Finglas, P. M. (2003). Encyclopedia of Food Sciences and Nutrition. Amsterdam: Academic Press.
27. Carson, C. F., Mee, B. J., and Riley, T. V. (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.
28. Carson, C. F., and Riley, T. V. (1995). Antimicrobial activity of the major components of the essential oil of Melaleuca alternifolia. J. Appl. Bac-teriol. 78, 264-269.
29. Cavallito, C. J., and Bailey, J. H. (1944). Allicin, the antibacterial principle of Allium sativum. I. Isolation, physical properties and antibacterial action. J. Am. Chem. Soc. 66, 1950-1951.
30. Cava-Roda, R., Taboada-Rodríguez, A., Valverde-Franco, M., and Marín-Iniesta, E (2010). Antimicrobial activity of vanillin and mixtures with cinnamon and clove essential oils in controlling Listeria monocyto-genes and Escherichia coli O157:H7 in milk. Food Bioprocess Technol. doi: 10.1007/s1 1947-010-0484-4
31. Cejpek, K., Valusek, J., and Velisek, J. (2000). Reactions of allyl isothio-cyanate with alanine, glycine, and several peptides in model systems. J. Agric. Food Chem. 48, 3560-3565.
32. Cerrutti,P.,andAlzamora,S.M. (1996). Inhibitory effects of vanillin on some food spoilage yeasts in laboratory media and fruit purées. Int. J. Food Microbiol. 29, 379-386.
33. Ceylan, E., and Fung, D. Y. C. (2004). Antimicrobial activity of spices. J. Rapid Methods Autom. Microbiol. 12, 1-55.
34. Chang, S. T., Chen, P. F., and Chang, S. C. (2001). Antibacterial activity of leaf essential oils and their constituents from Cinnamomum osmophloeum.J. Ethnopharmacol. 77,123-127.
35. Cimanga, K., Kambu, K., Tona, L., Apers, S., De Bruyne, T., Hermans, N., Totté, J., Pieters, L., and Vli-etinck, A. J. (2002). Correlation between chemical composition and antibacterial activity of essential oils of some aromatic medicinal plants growing in the Democratic Republic of Congo. J. Ethnopharmacol. 79, 213-220.
36. Claeson, P., Radstrom, P., Skold, O., Nilsson, A., and Hoglund, S. (1992). Bactericidal effect of the sesquiter-pene T-cadinol on Staphylococcus aureus. Phytother. Res. 6, 94-98.
37. Cosentino, S., Tuberoso, C. I. G., Pisano, B., Satta, M., Mascia, V., Arzedi, E., and Palmas, E (1999). In-vitro antimicrobial activity and chemical composition of Sardinian Thymus essential oils. Lett. Appl. Microbiol. 29, 130-135.
38. Cotter, P. D., Hill, C., and Ross, R. P. (2005). Food microbiology: bac-teriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3, 777-788.
39. Cox, S. D., Mann, C. M., Markham, J. L., Bell, H. C., Gustafson, J. E., Warm-ington, J.R.,Wyllie,S.G. (2000). The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J. Appl. Microbiol. 88, 170-175.
40. Cristani, M., D'Arrigo, M., Mandalari, G., Castelli, F., Sarpietro, M. G., Micieli, D., Venuti, V., Bisignano, G., Saija, A., and Trombetta, D. (2007). Interaction of four monoter-penes contained in essential oils with model membranes: implications for their antibacterial activity. J. Agric. Food Chem. 55, 6300-6308.
41. Davidson, P. M., and Parish, M. E. (1989). methods for testing the efficacy of food antimicrobials. Food Technol. 43, 148-155.
42. De, M., De, A. K., and Banerjee, A. B. (1999). Antimicrobial screening of some Indian spices. Phytother. Res. 13, 616-618.
43. De Oliveira, T. L. C., De Araújo Soares, R., Ramos, E. M., Das Graças Cardoso, M., Alves, E., and Piccoli, R. H. (2011). Antimicrobial activity of Satureja montana L. essential oil against Clostridium perfringens type A inoculated in mortadella-type sausages formulated with different levels of sodium nitrite. Int. J. Food Microbiol. 144, 546-555.
44. De Souza, E. L., De Barros, J. C., De Oliveira, C. E. V., and Da Conceição, M. L. (2010). Influence of Origanum vulgare L. essential oil on entero-toxin production, membrane permeability and surface characteristics of Staphylococcus aureus. Int. J. Food Microbiol. 137,308-311.
45. De Souza, E. L., Stamford, T. L. M., Lima, E. D. O., Barbosa Filho, J. M., and Marques, M. O. M. (2008). Interference of heating on the antimicrobial activity and chemical composition of Origanum vulgare L. (Lamiaceae) essential oil. Ciênc. Tecnol. Aliment. 28,418-422.
46. Deans, S. G., and Ritchie, G. (1987). Antibacterial properties of plant essential oils. Int. J. Food Microbiol. 5, 165-180.
47. Delaquis, P. (1995). Antimicrobial properties of isothiocyanates in food preservation. Food Technol. 49, 73.
48. Delaquis, P. (1997). Antimicrobial activity of gaseous allyl isothiocyanate. J. Food Prot. 60, 943.
49. Delaquis, P. J., Stanich, K., Girard, B., and 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.
50. Demuner, A. J., Barbosa, L. C. A., Maga-lhaes, C. G., Da Silva, C. J., Maltha, C. R. A., and Pinheiro, A. L. (2011). Seasonal variation in the chemical composition and antimicrobial activity of volatile oils of three species of Leptospermum (Myrtaceae) grown in Brazil. Molecules 16, 1181-1191.
51. Di Pasqua, R., Betts, G., Hoskins, N., Edwards, M., Ercolini, D., and Mau-riello, G. (2007). Membrane toxicity of antimicrobial compounds from essential oils. J. Agric. Food Chem. 55, 4863-4870.
52. Di Pasqua, R., Hoskins, N., Betts, G., and Mauriello, G. (2006). Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J. Agric. Food Chem. 54, 2745-2749.
53. Di Pasqua, R., Mamone, G., Ferranti, P., Ercolini, D., and Mauriello, G. (2010). Changes in the proteome of Salmonella enterica serovar Thompson as stress adaptation to sub-lethal concentrations of thymol. Proteomics 10,1040-1049.
54. Djenane, D., Yangüela, J., Montañés, L., Djerbal, M., and Roncalés, P. (2011). Antimicrobial activity of Pistacia lentiscus and Satureja montana essential oils against Listeria monocytogenes CECT 935 using laboratory media: efficacy and syner-gistic potential in minced beef. Food Control 22, 1046-1053.
55. Domadia, P., Swarup, S., Bhunia, A., Sivaraman, J., and Dasgupta, D. (2007). Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde. Biochem. Pharmacol. 74,831-840.
56. Donsi, E, Annunziata, M., Sessa, M., and Ferrari, G. (2011). Nanoencapsula-tion of essential oils to enhance their antimicrobial activity in foods. Food Sci. Technol. 44, 1908-1914.
57. Dorman, H. J. D., and Deans, S. G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J. Appl. Microbiol. 88, 308-316.
58. Dufrêne, Y. E (2008). Towards nanomi-crobiology using atomic force microscopy. Nat. Rev. Microbiol. 6, 674-680.
59. Eliopoulos, G. M., Moellering, R. C. J., and Pillai, S. K. (1996). "Antimicrobial combinations," in Antibiotics in Laboratory Medicine, 5th Edn, ed. V. Lorian (Philadelphia: Williams & Wilkins), 365-440.
60. Espina, L., Somolinos, M., Lorán, S., Conchello, P., García, D., and Pagán, R. (2011). Chemical composition of commercial citrus fruit essential oils andevaluation of their antimicrobial activity acting alone or in combined processes. Food Control 22, 896-902.
61. Essam, E. (2001). Insecticidal activity of essential oils: octopaminergic sites of action. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130, 325-337.
62. Fantner, G. E., Barbero, R. J., Gray, D. S., and Belcher, A. M. (2010). Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat. Nanotechnol. 5,280-285.
63. Feldberg, R. S., Chang, S. C., Kotik, A. N., Nadler, M., Neuwirth, Z., Sundstrom, D. C., and Thompson, N. H. (1988). In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Chemother. 32, 1763-1768.
64. Feron, V. J., Til, H. P., De Vrijer, F., Woutersen, R. A., Cassee, E R., and Van Bladeren,P.J. (1991). Aldehydes: occurrence, carcinogenic potential, mechanism of action and risk assessment. MU tat. Res. 259, 363-385.
65. Fisher, K., and Phillips, C. (2008). Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends Food Sci. Technol. 19, 156-164.
66. Fisher, K., and Phillips, C. (2009). The mechanism of action of a citrus oil blend against Enterococcus faecium and Enterococcus faecalis. J. Appl. Microbiol. 106,1343-1349.
67. Fisher, K., and Phillips, C. A. (2006). The effect of lemon, orange and berg-amot essential oils and their components on the survival of Campylobac-ter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J. Appl. Microbiol. 101,1232-1240.
68. Fitzgerald, D. J., Stratford, M., Gas-son, M. J., and Narbad, A. (2005). Structure-function analysis of the vanillin molecule and its antifungal properties. J. Agric. Food Chem. 53, 1769-1775.
69. Fitzgerald, D. J., Stratford, M., Gasson, M. J., Ueckert, J., Bos, A., and Narbad, A. (2004). Mode of antimicrobial of vanillin against Escherichia coli, Lactobacillus plantarum and Lis-teria innocua. J. Appl. Microbiol. 97, 104-113.
70. Fitzgerald, D. J., Stratford, M., and Narbad, A. (2003). Analysis of the inhibition of food spoilage yeasts by vanillin. Int. J. Food Microbiol. 86, 113-122.
71. Focke, M., Feld, A., and Lichtenthaler, H. K. (1990). Allicin, a naturally occurring antibiotic from garlic, specifically inhibits acetyl-CoA synthetase. FEBSLett. 261, 106-108.
72. Fraenkel, G. S. (1959). The raison d'être of secondary plant substances. Science 129,1466-1470.
73. Gabel, C. V., and Berg, H. C. (2003). The speed of the flagellar rotary motor of Escherichia coli varies linearly with protonmotive force. Proc. Natl. Acad. Sci. U.S.A. 100,8748-8751.
74. Gao, C., Tian, C., Lu, Y., Xu, J., Luo, J., and Guo, X. (2011). Essential oil composition and antimicrobial activity of Sphallerocarpus gracilis seeds against selected food-related bacteria. Food Control 22, 517-522.
75. García-García, R., López-Malo, A., and Palou, E. (2011). Bactericidal action of binary and ternary mixtures of carvacrol, thymol, and eugenol against Listeria innocua. J. Food Sci. 76,M95-M100.
76. George, D. R., Smith, T. J., Shiel, R. S., Sparagano, O. A. E., and Guy, J. H. (2009). Mode of action and variability in efficacy of plant essential oils showing toxicity against the poultry red mite, Dermanyssus gallinae. Vet. Parasitol. 161,276-282.
77. Ghannoum, M. A., and Rice, L. B. (1999). Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12, 501-517.
78. Gilbert, Y., Deghorain, M., Wang, L., Xu, B., Pollheimer, P. D., Gru-ber, H. J., Errington, J., Hallet, B., Haulot, X., Verbelen, C., Hols, P., and Dufrêne, Y. F. (2007). Single-molecule force spectroscopy and imaging of the vancomycin/D-Ala-D-Ala interaction. Nano Lett. 7, 796-801.
79. Gill, A. O., Delaquis, P., Russo, P., and Holley, R. A. (2002). Evaluation of antilisterial action of cilantro oil on vacuum packed ham. Int. J. Food Microbiol. 73, 83-92.
80. Gill, A. O., and Holley, R. A. (2004). Mechanisms of bactericidal action of cinnamaldehyde against Listeria monocytogenes and of eugenol against L. monocytogenes and Lactobacillus sakei. Appl. Environ. Microbiol. 70, 5750-5755.
81. Gill, A. O., and Holley, R. A. (2006). Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. FoodMicrobiol. 108, 1-9.
82. Gill, A. O., and Holley, R. A. (2006). Inhibition of membrane bound ATPases of Escherichia coli and Listeria monocytogenes by plant oil aromatics. Int. J. Food Microbiol. 111, 170-174.
83. Gustafson, J. E., Liew, Y. C., Chew, S., Markham, J., Bell, H. C., Wyl-lie, S. G., and Warmington, J. R. (1998). Effects of tea tree oil on Escherichia coli. Lett. Appl. Microbiol. 26, 194-198.
84. Gutierrez, J., Barry-Ryan, C., and Bourke, P. (2008). The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. Int. J. Food Microbiol. 124,91-97.
85. Gutierrez, J., Barry-Ryan, C., and Bourke, P. (2009). Antimicrobial activity of plant essential oils using food model media: efficacy, syner-gistic potential and interactions with food components. Food Microbiol. 26, 142-150.
86. Hafedh, H., Fethi, B. A., Mejdi, S., Emira, N., and Amina, B. (2010). Effect of Mentha longifolia L. ssp longifolia essential oil on the morphology of four pathogenic bacteria visualized by atomic force microscopy. Afr. J. Microbiol. Res. 4, 1122-1127.
87. Hammer, K. A., Carson, C. F., and Riley, T. V. (1999). Antimicrobial activity of essential oils and other plant extracts. J. Appl. Microbiol. 86, 985-990.
88. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011). Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332.
89. Helander, I. M., Alakomi, H. L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M., and Von Wright, A. (1998). Characterization of the action of selected essential oil components on Gram-negative bacteria. J. Agric. Food Chem. 46, 3590-3595.
90. Hemaiswarya,S.,andDoble, M. (2009). Synergistic interaction of eugenol with antibiotics against Gram negative bacteria. Phytomedicine 16, 997-1005.
91. Hemaiswarya, S., Soudaminikkutty, R., Narasumani, M. L., and Doble, M. (2011). Phenylpropanoids inhibit protofilament formation of Escherichia coli cell division protein FtsZ. J. Med. Microbiol. 60, 1317-1325.
92. Horváth, G., Kovács, K., Kocsis, B., and Kustos, I. (2009). Effect of thyme (Thymus vulgaris L.) essential oil and its main constituents on the outer membrane protein composition of erwinia strains studied with microfluid chip technology. Chro-matographia 70, 1645-1650.
93. Hughes, B. G., and Lawson, L. D. (1991). Antimicrobial effects of Allium sativum L. (garlic), Allium ampeloprasum L. (elephant garlic), and Allium cepa L. (onion), garlic compounds and commercial garlic supplement products. Phytother. Res. 5, 154-158.
94. Iscan, G., Kirimer, N., Kürkcüoglu, M., Baser, K. H. C., and Demirci, F. (2002). Antimicrobial screening of Mentha piperita essential oils. J. Agric. Food Chem. 50, 3943-3946.
95. Jung, H. G., and Fahey, G. C. (1983). Nutritional implications of phenolic monomers and lignin: a review. J. Anim.Sci. 57,206-219.
96. Juven, B. J., Kanner, J., Schved, F., and Weisslowicz, H. (1994). Factors that interact with the antibacterial action of thyme essential oil and its active constituents. J. Appl. Bacteriol. 76, 626-631.
97. Kalemba, D., and Kunicka, A. (2003). Antibacterial and antifungal properties of essential oils. Curr. Med. Chem. 10,813-829.
98. Kawakishi, S., and Kaneko, T. (1985). Interaction of oxidized glutathione with allyl isothiocyanate. Phyto-chemistry 24,715-718.
99. Kawakishi, S., and Kaneko, T. (1987). Interaction of proteins with allyl isothiocyanate. J. Agric. Food Chem. 35, 85-88.
100. Kawakishi, S., and Namiki, M. (1982). Oxidative cleavage of the disulfide bond of cystine by allyl isothiocyanate. J. Agric. Food Chem. 30, 618-620.
101. Kim, J., Marshall, M. R., and Wei, C. I. (1995). Antibacterial activity of some essential oil components against five foodborne pathogens. J. Agric. Food Chem. 43, 2839-2845.
102. Kim, S. I., Roh, J. Y., Kim, D. H., Lee, H. S., and Ahn, Y J. (2003). Insecticidal activities of aromatic plant extracts and essential oils against Sitophilus oryzae and Callosobruchus chinensis. J Stored Prod Res 39,293-303.
103. Kojima,M. (1971). Studies on the effects of isothiocyanates and their analogues on microorganisms. J. Ferment. Technol. 49, 740-746.
104. Koutsoudaki, C., Krsek, M., and Rodger, A. (2005). Chemical composition and antibacterial activity of the essential oil and the gum of Pistacia lentiscus Var. chia. J. Agric. Food Chem. 53,7681-7685.
105. Kumar,M.,andBerwal,J.S. (1998). Sensitivity of food pathogens to garlic (Allium sativum). J. Appl. Microbiol. 84,213-215.
106. Kwon, J. A., Yu, C. B., and Park, H. D.(2003). Bacteriocidal effects and inhibition of cell separation of cin-namic aldehyde on Bacillus cereus. Lett. Appl. Microbiol. 37, 61-65.
107. Kyung, K. H. (2011). Antimicrobial properties of Allium species. Curr. Opin. Biotechnol. doi: 10.1016/j.copbio.2011.08.004
108. La Storia, A., Ercolini, D., Marinello, E,Di Pasqua, R., Villani, F., and Mauriello, G. (2011). Atomic force microscopy analysis shows sur face structure changes in carvacrol-treated bacterial cells. Res. Microbiol. 162, 164-172.
109. Laekeman, G. M., Van Hoof, L., Haemers, A., Berghe, D. A. V., Herman, A. G., and Vlietinck, A. J. (1990). Eugenol a valuable compound for in vitro experimental research and worthwhile for further in vivo investigation. Phytother. Res. 4, 90-96.
110. Lambert, P. A., and Hammond, S. M. (1973). Potassium fluxes, first indications of membrane damage in micro-organisms. Biochem. Biophys. Res. Commun. 54, 796-799.
111. Lambert, R. J. W., Skandamis, P. N., Coote, P. J., and Nychas, G. J. E. (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.
112. Liao, H., Zhang, F., Liao, X., Hu, X., Chen, Y., and Deng, L. (2010). Analysis of Escherichia coli cell damage induced by HPCD using microscopies and fluorescent staining. Int. J. FoodMicrobiol. 144,169-176.
113. Lin, C.M., Preston Iii, J. F., and Wei, C. I. (2000). Antibacterial mechanism of allyl isothiocyanate. J. Food Prot. 63, 727-734.
114. Liu, S., Sun, Y., Li, W., Yu, H., Li, X., Liu, Z., Zeng, J., Zhou, Y., Chen, C., and Jia, J. (2010). The antibacterial mode of action of allitridi for its potential use as a therapeutic agent against Helicobacter pylori infection. FEMS Microbiol. Lett. 303, 183-189.
115. Luciano, F. B., and Holley, R. A. (2009). Enzymatic inhibition by allyl isothiocyanate and factors affecting its antimicrobial action against Escherichia coli O157:H7. Int. J. Food Microbiol. 131,240-245.
116. Luciano, F. B., Hosseinian, F. S., Beta, T., and Holley, R. A. (2008). Effect of free-SH containing compounds on allyl isothiocyanate antimicrobial activity against Escherichia coli O157:H7. J. Food Sci. 73, M214-M220.
117. Lv, F., Liang, H., Yuan, Q., and Li, C. (2011). In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res. Int. 44, 3057-3064.
118. Mann, C. M., Cox, S. D., and Markham, J. L. (2000). The outer membrane of Pseudomonas aeruginosa NCTC 6749 contributes to its tolerance to the essential oil of Melaleuca alterni-folia (tea tree oil). Lett. Appl. Microbiol. 30, 294-297.
119. Marino, M., Bersani, C., and Comi, G. (2001). Impedance measurements to study the antimicrobial activity of essential oils from Lamiaceae and Compositae. Int. J. Food Microbiol. 67,187-195.
120. Miron, T., Rabinkov, A., Mirelman, D., Wilchek, M., and Weiner, L. (2000). The mode of action of allicin: its ready permeability through phos-pholipid membranes may contribute to its biological activity. Biochim. Biophys. Acta 1463,20-30.
121. Nakamura, C. V., Ueda-Nakamura, T., Bando, E., Negrão Melo, A. F., Garcia Cortez, D. A., and Dias Filho Filho, B. P. (1999). Antibacterial activity of Ocimum gratissimum L. essential oil. Mem. Inst. Oswaldo Cruz 94, 675-678.
122. Nannapaneni, R., Chalova, V. I., Cran-dall, P. G., Ricke, S. C., Johnson, M. G., and O'Bryan, C. A. (2009). Campylobacter and Arcobac-ter species sensitivity to commercial orange oil fractions. Int. J. Food Microbiol. 129, 43-49.
123. Nazer, A. I., Kobilinsky, A., Tholozan, J. L., and Dubois-Brissonnet, F. (2005). Combinations of food antimicrobials at low levels to inhibit the growth of Salmonella sv. Typhimurium: a synergistic effect? Food Microbiol. 22, 391-398.
124. Nguefack, J., Budde, B. B., and Jakob-sen, M. (2004a). Five essential oils from aromatic plants of Cameroon: their antibacterial activity and ability to permeabilize the cytoplasmic membrane of Listeria innocua examined by flow cytometry. Lett. Appl. Microbiol. 39, 395-400.
125. Nguefack, J., Leth, V., Amvam Zollo, P. H., and Mathur, S. B. (2004b). Evaluation of five essential oils from aromatic plants of Cameroon for controlling food spoilage and mycotoxin producing fungi. Int. J. Food Microbiol. 94, 329-334.
126. Nguefack, J., Tamgue, O., Dongmo, J. B. L., Dakole, C. D., Leth, V., Vismer, H. F., Amvam Zollo, P. H., and Nkengfack, A. E. (2012). Synergistic action between fractions of essential oils from Cymbopogon citratus, Ocimum gratissimum and Thymus vulgaris against Penicillium expansum. Food Control 23, 377-383.
127. Nielsen, P. V., and Rios, R. (2000). Inhibition of fungal growth on bread by volatile components from spices and herbs, and the possible application in active packaging, with special emphasis on mustard essential oil. Int. I Food Microbiol. 60,219-229.
128. Nielsen, S. B., and Otzen, D. E. (2010). Impact of the antimicrobial peptide novicidin on membrane structure and integrity. J. Colloid Interface Sci. 345, 248-256.
129. Nikaido, H. (1994). Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264, 382-388.
130. Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656.
131. Odds, R C. (2003). Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52,1.
132. Onawunmi, G. O. (1989). Evaluation of the antimicrobial activity of citral. Lett. Appl. Microbiol. 9,105-108.
133. Oussalah, M., Caillet, S., and Lacroix, M. (2006). Mechanism of action of Spanish oregano, Chinese cinnamon, and savory essential oils against cell membranes and walls of Escherichia coli O157:H7 and Listeria monocytogenes. J. Food Prot. 69, 1046-1055.
134. Oussalah, M., Caillet, S., Saucier, L., and Lacroix, M. (2007). Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 18,414-420.
135. Paibon, W., Yimnoi, C. A., Tembab, N., Boonlue, W., Jampachaisri, K., Nuengchamnong, N., Waranuch, N., and Ingkaninan, K. (2011). Comparison and evaluation of volatile oils from three different extraction methods for some Thai fragrant flowers. Int. J. Cosmet. Sci. 33, 150-156.
136. Pajohi, M. R. (2011). Synergistic antibacterial activity of the essential oil of Cuminum cyminum seed and nisin in a food model. J. Appl. Microbiol. 110,943.
137. Panizzi, L., Flamini, G., Cioni, P. L., and Morelli, I. (1993). Composition and antimicrobial properties of essential oils of four mediterranean lamiaceae. J. Ethnopharmacol. 39, 167-170.
138. Paparella, A., Taccogna, L., Aguzzi, I., Chaves-López, C., Serio, A., Marsilio, E, and Suzzi, G. (2008). Flow cytometric assessment of the antimicrobial activity of essential oils against Listeria monocytogenes. Food Control 19,1174-1182.
139. Paul, S. (2011). Trachyspermum ammi (L.) fruit essential oil influencing on membrane permeability and surface characteristics in inhibiting food -borne pathogens. Food Control 22, 725.
140. Pauli, A., and Kubeczka, K. H. (2010). Antimicrobial properties of volatile phenylpropanes. Nat. Prod. Com-mun. 5, 1387-1394.
141. Pei, R. S., Zhou, F., Ji, B. P., and Xu, J. (2009). Evaluation of combined antibacterial effects of eugenol, cin-namaldehyde, thymol, and car-vacrol against E. coli with an improved method. J. Food Sci. 74, M379-M383.
142. Pelissari, F. M., Grossmann, M. V. E., Yamashita, F., and Pined, E. A. G. (2009). Antimicrobial, mechanical, and barrier properties of cassava starch-chitosan films incorporated with oregano essential oil. J. Agric. Food Chem. 57, 7499-7504.
143. Pereira, C. G., and Meireles, M. A. A. (2010). Supercritical fluid extraction of bioactive compounds: fundamentals, applications and economic perspectives. Food Bioprocess Technol. 3, 340-372.
144. Pérez-Fons, L., Aranda, F. J., Guillén, J., Villalaín, J., and Micol, V. (2006). Rosemary (Rosmarinus offic-inalis) diterpenes affect lipid polymorphism and fluidity in phospho-lipid membranes. Arch. Biochem. Biophys. 453, 224-236.
145. Perry, C. C., Weatherly, M., Beale, T., and Randriamahefa, A. (2009). Atomic forcemicroscopy study of the antimicrobial activity of aqueous garlic versus ampicillin against Escherichia coli and Staphylococ-cus aureus. J. Sci. Food Agric. 89, 958-964.
146. Phillips, C., and Laird, K. (2011). Vapour of a citrus essential oil blend and its antimicrobial properties. U.S. Patent 20110136761.
147. Rabinkov, A., Miron, T., Konstanti-novski, L., Wilchek, M., Mirelman, D., and Weiner, L. (1998). The mode of action of allicin: trapping of radicals and interaction with thiol containing proteins. Biochim. Biophys. Acta 1379, 233-244.
148. Rammanee, K., and Hongpattarakere, T. (2011). Effects of tropical citrus essential oils on growth, aflatoxin production, and ultrastructure alterations of Aspergillus flavus and Aspergillus parasiticus. Food Bioprocess Technol. 4, 1050-1059.
149. Rao, A., Zhang, Y., Muend, S., and Rao, R. (2010). Mechanism of anti-fungal activity of terpenoid phenols resembles calcium stress and inhibition of the TOR pathway. Antimicrob. Agents Chemother. 54, 5062-5069.
150. Rasooli, I., Rezaei, M. B., and Allameh, A. (2006). Ultrastructural studies on antimicrobial efficacy of thyme essential oils on Listeria monocytogenes. Int. I Infect. Dis. 10, 236-241.
151. Rattanachaikunsopon, P., and Phumkhachorn, P. (2010). Assessment of factors influencing antimicrobial activity of carvacrol and cymene against Vibrio cholerae in food. J. Biosci. Bioeng. 110, 614-619.
152. Rhayour, K., Bouchikhi, T., Tantaoui-Elaraki, A., Sendide, K., and Remmal, A. (2003). The mechanism of bactericidal action of oregano and clove essential oils and of their phenolic major components on Escherichia coli and Bacillus sub tilis. J. Essent. Oil Res. 15,356-362.
153. Roller, S. (2003). Natural Antimicrobials for the Minimal Processing of Foods. Cambridge: Woodhead Publishing, Limited.
154. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010). Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U.S.A. 107,2230-2234.
155. Rupasinghe, H. P. V., Boulter-Bitzer, J., Ahn, T., and Odumeru, J. A. (2006). Vanillin inhibits pathogenic and spoilage microorganisms in vitro and aerobic microbial growth in fresh-cut apples. Food Res. Int. 39, 575-580.
156. Sánchez, E., García, S., and Heredia, N. (2010). Extracts of edible and medicinal plants damage membranes of Vibrio cholerae. Appl. Environ. Microbiol. 76, 6888-6894.
157. Sánchez-González, L., Vargas, M., González-Martínez, C., Chiralt, A., and Cháfer, M. (2011). Use of essential oils in bioactive edible coatings: a review. Food Eng. Rev. 3, 1-16.
158. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., Jones, J. L., and Griffin, P. M. (2011). Foodborne illness acquired in the United States-major pathogens. Emerging Infect. Dis. 17, 7-15.
159. Schipilliti, L., Dugo, G., Santi, L., Dugo, P., and Mondello, L. (2011). Authentication of bergamot essential oil by gas chromatography-combustion-isotope ratio mass spectrometer (GC-C-IRMS). J. Essent. Oil Res. 23, 60-71.
160. Schneider, T., Kruse, T., Wimmer, R., Wiedemann, I., Sass, V., Pag, U., Jansen, A., Nielsen, A. K., Mygind, P. H., Raventós, D. S., Neve, S., Ravn, B., Bonvin, A. M. J. J., De Maria, L., Andersen, A. S., Gammelgaard, L. K., Sahl, H. G., and Kristensen, H. H. (20 10). Plectasin, a fungal defensin, targets the bacterial cell wall precursor lipid II. Science 328, 1168-1172.
161. Schnitzler, P., Astani, A., and Reichling, J. (2011). Screening for antiviral activities of isolated compounds from essential oils. Evid. Based Complement. Alternat. Med. PMID: 253643
162. Shapira, R., and Mimran, E. (2007). Isolation and characterization of Escherichia coli mutants exhibiting altered response to thymol. Microb. DrugResist. 13, 157-165.
163. Shofran, B. G., Purrington, S. T., Breidt, E, and Fleming, H. P. (1998). Antimicrobial properties of sinigrin and its hydrolysis products. J. Food Sci. 63, 621-624.
164. Sikkema, J., De Bont, J. A. M., and Poolman, B. (1995). Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59,201-222.
165. Silva, F., Ferreira, S., Duarte, A., Men-donça, D. I., and Domingues, F. C. (2011). Antifungal activity of Coriandrum sativum essential oil, its mode of action against Candida species and potential synergism with amphotericin B. Phytomedicine 19, 42-47.
166. Smith-Palmer, A., Stewart, J., and Fyfe, L. (1998). Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett. Appl. Microbiol. 26, 118-122.
167. Somolinos, M., García, D., Condón, S., Mackey, B., and Pagán, R. (2010). Inactivation of Escherichia coli by citral. J. Appl. Microbiol. 108, 1928-1939.
168. Sullan, R. M. A., Li, J. K., Hao, C., Walker, G. C., and Zou, S. (2010). Cholesterol-dependent nanomechanical stability of phase-segregated multicomponent lipid bilayers. Biophys. J. 99, 507-516.
169. Tajkarimi, M. M., Ibrahim, S. A., and Cliver, D. O. (2010). Antimicrobial herb and spice compounds in food. Food Control 21,1199-1218.
170. Thoroski, J. (1989). Eugenol induced inhibition of extracellular enzyme pro duction by Bacillus cereus. J. Food Prot. 52, 399-403.
171. Trombetta, D., Castelli, F., Sarpietro, M. G., Venuti, V., Cristani, M., Daniele, C., Saija, A., Mazzanti, G., and Bisignano, G. (2005). Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 49, 2474-2478.
172. Tserennadmid, R., Takó, M., Galgóczy, L., Papp, T., Pesti, M., Vágvölgyi, C., Almássy, K., and Krisch, J. (2011). Anti yeast activities of some essential oils in growth medium, fruit juices and milk. Int. J. Food Microbiol. 144, 480-486.
173. Turgis, M., Han, J., Caillet, S., and Lacroix, M. (2009). Antimicrobial activity of mustard essential oil against Escherichia coli O157:H7 and Salmonella typhi. Food Control 20, 1073-1079.
174. Turina, A. D. V., Nolan, M. V., Zygadlo, J. A., and Perillo, M. A. (2006). Natural terpenes: self-assembly and membrane partitioning. Biophys. Chem. 122,101-113.
175. Ultee, A., Bennik, M. H. J., and Moezelaar, R. (2002). The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 68, 1561-1568.
176. Ultee, A., Kets, E. P. W., Alberda, M., Hoekstra, F. A., and Smid, E. J. (2000). Adaptation of the food-borne pathogen Bacillus cereus to carvacrol. Arch. Microbiol. 174, 233-238.
177. Ultee, A., Kets, E. P. W., and Smid, E. J. (1999). Mechanisms of action of carvacrol on the food-borne pathogen. Appl. Environ. Microbiol. 65,4606-4610.
178. Ultee, A., and Smid, E. J. (2001). Influence of carvacrol on growth and toxin production by Bacillus cereus. Int. J. Food Microbiol. 64, 373-378.
179. Van Hoang, K., Stern, N. J., Saxton, A. M., Xu, F., Zeng, X., and Lin, J. (2011). Prevalence, development, and molecular mechanisms of bac-teriocin resistance in Campylobac-ter. Appl. Environ. Microbiol. 77, 2309-2316.
180. Veldhuizen, E. J. A., Tjeerdsma-Van Bokhoven, J. L. M., Zweijtzer, C., Burt, S. A., and Haagsman, H. P. (2006). Structural requirements for the antimicrobial activity of carvacrol. J. Agric. Food Chem. 54, 1874-1879.
181. Verma, R. P. (2003). Synthesis and reactions of 3-oxobutyl isothiocyanate (OB ITC). European J. Org Chem. 2003,415-420.
182. Walsh, S. E., Maillard, J. Y., Russell, A. D., Catrenich, C. E., Charbonneau, D.L., and Bartolo, R. G. (2003). Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria. J. Appl. Microbiol. 94,240-247.
183. Wang, J., Soisson, S. M., Young, K., Shoop, W., Kodali, S., Galgoci, A., Painter, R., Parthasarathy, G., Tang, Y. S., Cummings, R., Ha, S., Dorso, K., Motyl, M., Jayasuriya, H., Ondeyka, J., Herath, K., Zhang, C., Hernandez, L., Allocco, J., Basilio, Á., Tormo, J. R., Genilloud, O., Vicente, E,Pelaez, F., Colwell, L., Lee, S. H., Michael, B., Felcetto, T., Gill, C., Sil ver, L. L., Hermes, J. D., Bartizal, K., Barrett, J., Schmatz, D., Becker, J. W., Cully, D., and Singh, S. B. (2006). Platensimycin is a selective FabF inhibitor with potent antibiotic properties. Nature 441, 358-361.
184. Ward, S. M., Delaquis, P. J., Holley, R. A., and Mazza, G. (1998). Inhibition of spoilage and pathogenic bacteria onagar and pre-cooked roast beef by volatile horseradish distillates. Food Res. Int. 31, 19-26.
185. Wendakoon, C. N., and Morihiko, S. (1995). Inhibition of amino acid decarboxylase activity of Enterobacter aerogenes by active components in spices. J. Food Prot. 58,280-283.
186. Xu, J., Zhou, F., Ji, B. P., Pei, R. S., andXu, N. (2008). The antibacterial mechanism of carvacrol and thymol against Escherichia coli. Lett. Appl. Microbiol. 47, 174-179.
187. Yamazaki, K., Yamamoto, T., Kawai, Y., and Inoue, N. (2004). Enhancement of antilisterial activity of essential oil constituents by nisin and diglycerol fatty acid ester. Food Microbiol. 21, 283-289.
188. Zemek, J., Kosikova, B., Augustin, J., and Joniak, D. (1979). Antibiotic properties of lignin components. Folia Microbiol. (Praha) 24, 483-486.
189. Zemek, J., Valent, M., Pódová, M., Košíková, B., and Joniak, D. (1987). Antimicrobiai properties of aromatic compounds of plant origin. Folia Microbiol. (Praha) 32, 421-425.
190. Zeng, W C, Zhu, R. X., Jia, L. R., Gao, H., Zheng, Y., and Sun, Q. (2011). Chemical composition, antimicrobial and antioxidant activities of essential oil from Gnaphlium affine. Food Chem. Toxicol. 49, 1322-1328.
191. Zhang, Y., and Talalay, P. (1994). Anticarcinogenic activities of organic isothiocyanates: chemistry and mechanisms. Cancer Res. 54, 1976s-1981s.
192. Zink, D. L. (1997). The impact of consumer demands and trends on food processing. Emerging Infect. Dis. 3, 467-469.