Effects of nisin and lysozyme on growth inhibition and biofilm formation capacity of staphylococcus aureus strains isolated from raw milk and cheese samples

Journal of Food Protection

Volumn 75, Issue 9, 2012, Pages 1627-1633

  Sudagidan, Mert ^a   Yemenicioǧlu, Ahmet ^b  

^a MEHMET AKIF ERSOY UNIVERSITY   (Turkey)

^b IZMIR INSTITUTE OF TECHNOLOGY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

STAPHYLOCOCCUS AUREUS;

EID: 84865758140     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-001     Document Type: Article

References (43)

1. Aydin, A., K. Muratoglu, M. Sudagidan, K. Bostan, B. Okuklu, and S. Harsa. 2011. Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne Pathog. Dis. 8:63-69.
2. Bauer, R., and L. M. T. Dicks. 2005. Mode of action of lipid IItargeting lantibiotics. Int. J. Food Microbiol. 101:201-216. (Pubitemid 40615862)
3. Bera, A., S. Herbert, A. Jakob, W. Vollmer, and F. Götz. 2005. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55:778-787. (Pubitemid 40203693)
4. Blake, K. L., C. P. Randall, and A. J. O'Neill. 2011. In vitro studies indicate a high resistance potential for the lantibiotic nisin in Staphylococcus aureus and define a genetic basis for nisin resistance. Antimicrob. Agents Chemother. 55:2362-2368.
5. Bruno, M. E. C., A. Kaiser, and T. J. Montville. 1992. Depletion of proton motive force by nisin in Listeria monocytogenes cells. Appl. Environ. Microbiol. 58:2255-2259.
6. Carlson, S., and H. M. Bauer. 1957. Nisin, ein antibakterieller wirkstoff aus Streptococcus lactis unter berucksichtigung des resistenz problems. Arch. Hyg. Bakteriol. 141:445-459.
7. Carpentier, B., and O. Cerf. 1993. Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 75:499-511. (Pubitemid 24025162)
8. Chen, H., and D. G. Hoover. 2003. Bacteriocins and their food applications. J. Food Sci. 2:82-100.
9. Cloete, T. E. 2003. Resistance mechanisms of bacteria to antimicrobial compounds. Int. Biodeterior. Biodegrad. 51:277-282. (Pubitemid 36695771)
10. Code of Federal Regulations. 2010. 21 CFR 184.1538, Title 21, vol. 3. Direct food substances affirmed as generally recognized as safe. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=184. 1538. Accessed 27 July 2011.
11. Cucarella, C., C. Solano, J. Valle, B. Amorena, Í. Lasa, and J. R. Penadés. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896. (Pubitemid 32319293)
12. Cucarella, C., M. Á. Tormo, C. Úbeda, M. P. Trotonda, M. Monzón, C. Peris, B. Amorena, Í. Lasa, and J. R. Penadés. 2004. Role of biofilm-associated protein Bap in the pathogenesis of bovine Staphylococcus aureus. Infect. Immun. 72:2177-2185. (Pubitemid 38419932)
13. Davidson, P. M., and M. A. Harrison. 2002. Resistance and application to food antimicrobials, sanitizers, and other process controls. Food Technol. 56:69-78. (Pubitemid 35468530)
14. Dubin, G. 2003. Defense against own arms: staphylococcal cysteine proteases and their inhibitors. Acta Biochim. Pol. 50:715-724. (Pubitemid 38623803)
15. Fedtke, I., F. Götz, and A. Peschel. 2004. Bacterial evasion of innate host defenses - the Staphylococcus aureus lesson. Int. J. Med. Microbiol. 294:189-194. (Pubitemid 39281049)
16. Food and Agriculture Organization of the United Nations and World Health Organization. 2010. GSFA provisions for nisin. Available at: http: //www.codexalimentarus.net/gsfaonline/additives/detaills.html?id=1. Accessed 27 July 2011.
17. Grade, S., M. Avila, and M. Nunez. 2004. Fast induction of nisin resistance in Streptococcus thermophilus INIA 463 during growth in milk. Int. J. Food Microbiol. 96:165-172. (Pubitemid 39208844)
18. Hamama, A., N. El Hankouri, and M. El Ayadi. 2002. Fate of enterotoxigenic Staphylococcus aureus in the presence of nisinproducing Lactococcus lactis strain during manufacture of Jben, a Moroccan traditional fresh cheese. Int. Dairy J. 12:933-938. (Pubitemid 36016814)
19. Harris, L. J., H. P. Fleming, and T. R. Klaenhammer. 1991. Sensitivity and resistance of Listeria monocytogenes ATCC 19115, Scott A and UAL500 to nisin. J. Food Protog. 54:836-840.
20. Herbert, S., A. Bera, C. Nerz, D. Graus, A. Paschel, C. Goerke, M. Meehl, A. Cheung, and F. Götz. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in Staphylococci. PLoS Pathog. 3:981-993.
21. Jakobsen, R. A., R. Heggebø, E. B. Sunde, and M. Skjervheim. 2011. Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiol. 28:492-496.
22. Jarvis, B. 1967. Resistance to nisin and production of nisininactivating enzymes by several Bacillus species. J. Gen. Microbiol. 47:33-48.
23. Karlsson, A., and S. Arvidson. 2002. Variation in extracellular protease production among clinical isolates of Staphylococcus aureus due to different levels of expression of the protease repressor sarA. Infect. Immun. 70:4239-4246. (Pubitemid 34790932)
24. Le Loir, Y., F. Baron, and M. Gautier. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2:63-76. (Pubitemid 38846550)
25. Martí, M., M. P. Trotonda, M. Á. Tormo-Más, M. Vergara-Irigaray, A. L. Cheung, I. Lasa, and J. R. Penadés. 2010. Extracellular proteases inhibit protein-dependent biofilm formation in Staphylococcus aureus. Microb. Infect. 12:55-64.
26. Martínez, B., J. M. Obeso, A. Rodríguez, and P. García. 2008. Nisinbacteriophage cross resistance in Staphylococcus aureus. Int. J. Food Microbiol. 122:253-258.
27. Ming, X., and M. A. Daeschel. 1993. Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott A. J. Food Prot. 56:944-948. (Pubitemid 2010471)
28. Nostro, A., R. Scaffaro, G. Ginestra, M. D'Arrigo, L. Botta, A. Marino, and G. Bisignano. 2010. Control of biofilm formation by poly-ethylene-co-vinyl acetate films incorporating nisin. Appl. Microbiol. Biotechnol. 87:729-737.
29. Oliver, S. P., B. M. Jayarao, and R. A. Almeida. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog. Dis. 2:115-129. (Pubitemid 40770783)
30. Peschel, A., M. Otto, R. W. Jack, H. Kalbacheri, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410. (Pubitemid 29164628)
31. Pinto, M. S., A. F. de Carvalho, A. C. S. Pires, A. A. C. Souza, P. H. F. da Silva, and D. Sobral. 2011. The effects of nisin on Staphylococcus aureus count and the physicochemical properties of traditional minas serro cheese. Int. Dairy J. 21:90-96.
32. Piper, C., L. A. Draper, P. D. Cotter, R. P. Ross, and C. Hill. 2009. A comparison of the activities of lacticin 3147 and nisin against drugresistant Staphylococcus aureus and Enterococcus species. J. Antimicrob. Chemother. 26:1-6.
33. Qi, X., G. Poernomo, K. Wang, Y. Chen, M. B. Chan-Park, R. Xu, and M. W. Chang. 2011. Covalent immobilization of nisin on multiwalled carbon nanotubes: superior antimicrobial and anti-biofilm properties. Nanoscale 3:1874-1880.
34. Rilla, N., B. Martínez, and A. Rodríguez. 2004. Inhibition of a methicillin-resistant Staphylococcus aureus strain in afuega'l pitu cheese by the nisin z-producing strain Lactococcus lactis subsp. lactis IPLA 729. J. Food Prot. 67:928-933. (Pubitemid 38617205)
35. Ross, R. P., S. Morgan, and C. Hill. 2002. Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79:3-16. (Pubitemid 36153033)
36. Salton, M. R. J. 1957. The properties of lysozyme and its action on microorganisms. Bacteriol. Rev. 21:82-99.
37. Samelis, J., A. Kakouri, K. J. Rogga, I. N. Savvaidis, and M. G. Kontominas. 2003. Nisin treatments to control Listeria monocytogenes post-processing contamination on Anthotyros, a traditional Greek whey cheese, stored at 4uC in vacuum packages. Food Microbiol. 20:661-669. (Pubitemid 37425153)
38. Schneider, N., K. Werkmeiser, C. M. Becker, and M. Pischetsrieder. 2011. Prevalence and stability of lysozyme in cheese. Food Chem. 128:145-151.
39. Shaw, L., E. Golonka, J. Potempa, and S. J. Foster. 2004. The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology 150:217-228. (Pubitemid 38111488)
40. Stepanović, S., V. Djukić, V. Djordjević, and S. Djukić. 2003. Influence of the incubation atmosphere on the production of biofilm by staphylococci. Clin. Microbiol. Infect. 9:955-958. (Pubitemid 37236163)
41. Sudagidan, M., and A. Aydin. 2009. Screening virulence properties of staphylococci isolated from meat and meat products. Wien. Tierärztl. Monat. 96:128-134.
42. Sudagidan, M., C. Çavuşoǧlu, and F. Bacakoǧlu. 2008. Investigation of the virulence genes in methicillin-resistant Staphylococcus aureus strains isolated from biomaterial surfaces. Mikrobiyol. Bül. 42:29-39.
43. Suppakul, P., J. Miltz, K. Sonneveld, and S. W. Bigger. 2003. Active packaging technologies with an emphasis on antimicrobial packaging and its applications. J. Food Sci. 68:408-420. (Pubitemid 37181706)