Inhibition and inactivation of salmonella typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol

Journal of Food Protection

Volumn 76, Issue 2, 2013, Pages 205-212

  Soni, Kamlesh A ^a   Oladunjoye, Ademola ^a   Nannapaneni, Ramakrishna ^a   Schilling, M Wes ^a   Silva, Juan L ^a   Mikel, Benjy ^a   Bailey, R Hartford ^b  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARVACROL; ESSENTIAL OIL; POLYSTYRENE DERIVATIVE; STAINLESS STEEL; TERPENE;

ARTICLE; BACTERIUM ADHERENCE; BIOFILM; FOOD CONTAMINATION; FOOD HANDLING; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; PHYSIOLOGY; SALMONELLA TYPHIMURIUM;

BACTERIAL ADHESION; BIOFILMS; FOOD CONTAMINATION; FOOD HANDLING; MONOTERPENES; OILS, VOLATILE; POLYSTYRENES; SALMONELLA TYPHIMURIUM; STAINLESS STEEL;

ORIGANUM; SALMONELLA; SALMONELLA TYPHIMURIUM; THYMUS VULGARIS;

EID: 84874067150     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-196     Document Type: Article

References (40)

1. Adetunji, V. O., and I. A. Odetokun. 2012. Biofilm formation in human and tropical foodborne isolates of Listeria strains. Am. J. Food Technol. 7:517-531.
2. Allison, D. G., B. Ruiz, C. SanJose, A. Jaspe, and P. Gilbert. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167:179-184.
3. Anderson, G. G., and G. A. O'Toole. 2008. Innate and induced resistance mechanisms of bacterial biofilms. Curr. Top. Microbiol. Immunol. 322:85-105.
4. Borucki, M. K., J. D. Peppin, D. White, F. Loge, and D. R. Call. 2003. Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 69:7336-7342.
5. Bridier, A., R. Briandet, V. Thomas, and F. Dubois-Brissonnet. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27:1017-1032.
6. Burt, S. 2004. Essential oils: their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 94:223-253.
7. Burt, S. A., R. van der Zee, A. P. Koets, A. M. de Graaff, F. van Knapen, W. Gaastra, H. P. Haagsman, and E. J. Veldhuizen. 2007. Carvacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157:H7. Appl. Environ. Microbiol. 73:4484-4490.
8. Daferera, D. J., B. N. Ziogas, and M. G. Polissiou. 2003. The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium, and Clavibacter michiganensis subsp. michiganensis. Crop Prot. 22:39-44.
9. Gelinas, P., and J. Goulet. 1983. Neutralization of the activity of eight disinfectants by organic matter. J. Appl. Bacteriol. 54:243-247.
10. Giaouris, E., N. Chorianopoulos, and G. J. Nychas. 2005. Effect of temperature, pH, and water activity on biofilm formation by Salmonella enterica enteritidis PT4 on stainless steel surfaces, as indicated by the bead vortexing method and conductance measurements. J. Food Prot. 68:2149-2154.
11. Jacques, M., V. Aragon, and Y. D. Tremblay. Biofilm formation in bacterial pathogens of veterinary importance. Anim. Health. Res. Rev. 11:97-121.
12. Joseph, B., S. K. Otta, and I. Karunasagar. 2001. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64:367-372.
13. Kendall, P., L. C. Medeiros, V. Hillers, G. Chen, and S. DiMascola. 2003. Food handling behaviors of special importance for pregnant women, infants and young children, the elderly, and immunecompromised people. J. Am. Diet. Assoc. 103:1646-1649.
14. Kim, H., J. H. Ryu, and L. R. Beuchat. 2007. Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm. Appl. Environ. Microbiol. 73:1256-1265.
15. Knowles, J. R., S. Roller, D. B. Murray, and A. S. Naidu. 2005. Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 71:797-803.
16. Kroupitski, Y., R. Pinto, M. T. Brandl, E. Belausov, and S. Sela. 2009. Interactions of Salmonella enterica with lettuce leaves. J. Appl. Microbiol. 106:1876-1885.
17. Li, X., Z. Yan, and J. Xu. 2003. Quantitative variation of biofilms among strains in natural populations of Candida albicans. Microbiology 149:353-362.
18. Lopez, P., C. Sanchez, R. Batlle, and C. Nerin. 2005. Solid- and vapor-phase antimicrobial activities of six essential oils: susceptibility of selected foodborne bacterial and fungal strains. J. Agric. Food Chem. 53:6939-6946.
19. Lopez, P., C. Sanchez, R. Batlle, and C. Nerin. 2007. Vapor-phase activities of cinnamon, thyme, and oregano essential oils and key constituents against foodborne microorganisms. J. Agric. Food Chem. 55:4348-4356.
20. Lunden, J., T. Autio, A. Markkula, S. Hellstrom, and H. Korkeala. 2003. Adaptive and cross-adaptive responses of persistent and nonpersistent Listeria monocytogenes strains to disinfectants. Int. J. Food Microbiol. 82:265-272.
21. Mangalappalli-Illathu, A. K., and D. R. Korber. 2006. Adaptive resistance and differential protein expression of Salmonella enterica serovar Enteritidis biofilms exposed to benzalkonium chloride. Antimicrob. Agents Chemother. 50:3588-3596.
22. Mereghetti, L., R. Quentin, N. Marquet-Van Der Mee, and A. Audurier. 2000. Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 66:5083-5086.
23. Monil, D., K. A. Soni, R. Nannapaneni, M. W. Schilling, and J. L. Silva. 2012. Reductions of Listeria monocytogenes biofilms on stainless steel and polystyrene surface by essential oils. J. Food Prot. 75:1332-1337.
24. Nostro, A., A. Marino, A. R. Blanco, L. Cellini, M. Di Giulio, F. Pizzimenti, A. Sudano Roccaro, and G. Bisignano. 2009. In vitro activity of carvacrol against Staphylococcal preformed biofilm by liquid and vapour contact. J. Med. Microbiol. 58:791-797.
25. Nostro, A., A. Sudano Roccaro, G. Bisignano, A. Marino, M. A. Cannatelli, F. C. Pizzimenti, P. L. Cioni, F. Procopio, and A. R. Blanco. 2007. Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J. Med. Microbiol. 56:519-523.
26. Perez-Conesa, D., L. McLandsborough, and J. Weiss. 2006. Inhibition and inactivation of Listeria monocytogenes and Escherichia coli O157:H7 colony biofilms by micellar-encapsulated eugenol and carvacrol. J. Food Prot. 69:2947-2954.
27. Polonio, R. E., L. A. Mermel, G. E. Paquette, and J. F. Sperry. 2001. Eradication of biofilm-forming Staphylococcus epidermidis (RP62A) by a combination of sodium salicylate and vancomycin. Antimicrob. Agents Chemother. 45:3262-3266.
28. Richards, J. J., T. E. Ballard, and C. Melander. 2008. Inhibition and dispersion of Pseudomonas aeruginosa biofilms with reverse amide 2- aminoimidazole oroidin analogues. Org. Biomol. Chem. 6:1356-1363.
29. Rodrigues, D., N. Cerca, P. Teixeira, R. Oliveira, H. Ceri, and J. Azeredo. 2011. Listeria monocytogenes and Salmonella enterica enteritidis biofilms susceptibility to different disinfectants and stressresponse and virulence gene expression of surviving cells. Microb. Drug Resist. 17:181-189.
30. Sandberg, M., A. Maattanen, J. Peltonen, P. M. Vuorela, and A. Fallarero. 2008. Automating a 96-well microtitre plate model for Staphylococcus aureus biofilms: an approach to screening of natural antimicrobial compounds. Int. J. Antimicrob. Agents 32:233-240.
31. Sillankorva, S., P. Neubauer, and J. Azeredo. 2008. Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A. BMC Biotechnol. 8:79.
32. Somolinos, M., D. Garcia, R. Pagan, and B. Mackey. 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.
33. Soni, K. A., and R. Nannapaneni. 2010. Removal of Listeria monocytogenes biofilms with bacteriophage P100. J. Food Prot. 73:1519-1524.
34. Spoering, A. L., and K. Lewis. 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183:6746-6751.
35. Stepanovic, S., I. Cirkovic, V. Mijac, and M. Svabic-Vlahovic. 2003. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol. 20:339-343.
36. Stringfellow, K., P. Anderson, D. Caldwell, J. Lee, J. Byrd, J. McReynolds, J. Carey, D. Nisbet, and M. Farnell. 2009. Evaluation of disinfectants commonly used by the commercial poultry industry under simulated field conditions. Poult. Sci. 88:1151-1155.
37. Ueda, S., and Y. Kuwabara. 2007. Susceptibility of biofilm Escherichia coli, Salmonella Enteritidis, and Staphylococcus aureus to detergents and sanitizers. Biocontrol Sci. 12:149-153.
38. Ultee, A., E. P. Kets, and E. J. Smid. 1999. Mechanisms of action of carvacrol on the foodborne pathogen Bacillus cereus. Appl. Environ. Microbiol. 65:4606-4610.
39. Vestby, L. K., T. Moretro, S. Langsrud, E. Heir, and L. L. Nesse. 2009. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal and feed factories. BMC Vet. Res. 5:20.
40. Wong, H. S., K. M. Townsend, S. G. Fenwick, G. Maker, R. D. Trengove, and R. M. O'Handley. 2000. Comparative susceptibility of Salmonella Typhimurium biofilms of different ages to disinfectants. Biofouling 26:859-64.