Competitiveness and antibacterial potential of bacteriocin-producing starter cultures in different types of fermented sausages

Journal of Food Protection

Volumn 71, Issue 9, 2008, Pages 1817-1827

  Ravyts, Frédéric ^a   Barbuti, Silvana ^b   Frustoli, Maria Angela ^b   Parolari, Giovanni ^b   Saccani, Giovanna ^b   De Vuyst, Luc ^a   Leroy, Frédéric ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b Stazione Sperimentale per l'Industria delle Conserve Alimentari   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); LACTOBACILLUS SAKEI; LISTERIA MONOCYTOGENES;

EID: 51949084401     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-71.9.1817     Document Type: Article

References (54)

1. Albano, H., M. Oliveira, R. Aroso, N. Cubero, T. Hogg, and P. Teixeira. 2007. Antilisterial activity of lactic acid bacteria isolated from "Alheiras" (traditional Portuguese fermented sausages): in situ assays. Meat Sci. 76:796-800.
2. Anonymous. 1 December 2007. USDA/FSIS microbiology laboratory guidebook: isolation and identification of Listeria monocytogenes from red meat, poultry, egg and environmental samples. Available at: http://www.fsis.usda.gov/ PDF/MLG_8_05.pdf. U.S. Department of Agriculture, Food Safety Inspection Service, Washington, D.C.
3. Aymerich, T., M. G. Artigas, M. Garriga, J. M. Monfort, and M. Hugas. 2000. Effect of sausage ingredients and additives on the production of enterocin A and B by Enterococcus faecium CTC492. Optimization of in vitro production and anti-listerial effect in dry fermented sausages. J. Appl. Microbiol. 88:686-694.
4. Aymerich, T., B. Martin, M. Garriga, and M. Hugas. 2003. Microbial quality and direct PCR identification of lactic acid bacteria and non-pathogenic staphylococci from artisanal low-acid sausages. Appl. Environ. Microbiol. 69:4583-4594.
5. Benkerroum, N., A. Daoudi, T. Hamraoui, H. Ghalfi, C. Thiry, M. Duroy, P. Evrart, D. Roblain, and P. Thonart. 2005. Lyophilized preparations of bacteriocinogenic Lactobacillus curvatus and Lactococcus lactis subsp. lactis as potential protective adjuncts to control Listeria monocytogenes in dry-fermented sausages. J. Appl. Microbiol. 98:56-63.
6. Buncic, S., S. M. Avery, and S. M. Moorhead. 1997. Insufficient antilisterial capacity of low inoculum Lactobacillus cultures on long-term stored meats at 4°C. Int. J. Food Microbiol. 34:157-170.
7. Callewaert, R., M. Hugas, and L. De Vuyst. 2000. Competitiveness and bacteriocin production of Enterococci in the production of Spanish-style dry fermented sausages. Int. J. Food Microbiol. 57:33-42.
8. Campbell-Platt, G., and P. E. Cook. 1995. Fermented meats. Blackie Academic and Professional, London.
9. Castano, A., M. C. G. Fontan, J. M. Fresno, M. E. Tornadijo, and J. Carballo. 2002. Survival of Enterobacteriaceae during processing of Chorizo de cebolla, a Spanish fermented sausage. Food Control 13:107-115.
10. Comi, G., R. Urso, L. Iacumin, K. Rantsiou, P. Cattaneo, C. Cantoni, and L. Cocolin. 2005. Characterisation of naturally fermented sausages produced in the North East of Italy. Meat Sci. 69:381-392.
11. Coppola, R., M. Iorizzo, R. Saotta, E. Sorrentino, and L. Grazia. 1997. Characterization of micrococci and staphylococci isolated from soppressata molisana, a Southern Italy fermented sausage. Food Microbiol. 14:47-53.
12. Cordano, A. M., and J. Rocourt. 2001. Occurrence of Listeria monocytogenes in food in Chile. Int. J. Food Microbiol. 70:175-178.
13. Cotter, P. D., C. Hill, and R. P. Ross. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788.
14. de Carvalho, A. A. T., R. A. de Paula, H. C. Mantovani, and C. A. de Moraes. 2006. Inhibition of Listeria monocytogenes by a lactic acid bacterium isolated from Italian salami. Food Microbiol. 23:213-219.
15. Duffy, E. A., K. E. Belk, J. N. Sofos, G. R. Bellinger, A. Pape, and G. C. Smith. 2001. Extent of microbial contamination in United States pork retail products. J. Food Prot. 64:172-178.
16. Edwards, U., T. Rogall, H. Blocker, M. Emde, and E. C. Bottger. 1989. Isolation and direct complete nucleotide determination of entire genes - characterization of a gene coding for 16S-ribosomal RNA. Nucleic Acids Res. 17:7843-7853.
17. Farber, J. M., E. Daley, R. Holley, and W. R. Usborne. 1993. Survival of Listeria-monocytogenes during the production of uncooked German, American and Italian-style fermented sausages. Food Microbiol. 10:123-132.
18. Fontana, C., P. S. Cocconcelli, and G. Vignolo. 2005. Monitoring the bacterial population dynamics during fermentation of artisanal Argentinean sausages. Int. J. Food Microbiol. 103:131-142.
19. Gandhi, M., and M. L. Chikindas. 2007. Listeria: a foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113:1-15.
20. Gevers, D., G. Huys, and J. Swings. 2001. Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol. Lett. 205:31-36.
21. Gianfranceschi, M., A. Gattuso, A. Fiore, M. C. D'Ottavio, M. Casale, A. Palumbo, and P. Aureli. 2006. Survival of Listeria monocytogenes in uncooked Italian dry sausage (salami). J. Food Prot. 69:1533-1538.
22. Hugas, M., M. Garriga, M. T. Aymerich, and J. M. Monfort. 1995. Inhibition of Listeria in dry fermented sausages by the bacteriocinogenic Lactobacillus sakei CTC 494. J. Appl. Bacteriol. 79:322-330.
23. Hugas, M., M. Garriga, T. Aymerich, and J. M. Monfort. 1993. Biochemical characterization of lactobacilli from dry fermented sausages. Int. J. Food Microbiol. 18:107-113.
24. Hugas, M., B. Neumeyer, F. Pages, M. Garriga, and W. P. Hammes. 1996. Antimicrobial activity of bacteriocin-producing cultures in meat products. 2. Comparison of the antilisterial potential of bacteriocin-producing lactobacilli in fermenting sausages. Fleischwirtschaft 76:649-652.
25. Hugas, M., B. Neumeyer, F. Pages, M. Garriga, and W. P. Hammes. 1997. Comparison of bacteriocin-producing lactobacilli on Listeria growth in fermented sausages. Fleischwirtschaft 76:649-652.
26. Iacumin, L., G. Comi, C. Cantoni, and L. Cocolin. 2006. Molecular and technological characterization of Staphylococcus xylosus isolated from naturally fermented Italian sausages by RAPD, Rep-PCR and Sau-PCR analysis. Meat Sci. 74:281-288.
27. Jamuna, M., and K. Jeevaratnam. 2004. Isolation and partial characterization of bacteriocins from Pediococcus species. Appl. Microbiol. Biotechnol. 65:433-439.
28. Kaya, M., and H. Y. Gokalp. 2004. The behavior of Listeria monocytogenes in sucuks produced with different lactic starter cultures. Turk. J. Vet. Anim. Sci. 28:1113-1120.
29. Koutsoumanis, K., C. C. Tassou, P. S. Taoukis, and G. J. E. Nychas. 1998. Modelling the effectiveness of a natural antimicrobial on Salmonella enteritidis as a function of concentration, temperature and pH, using conductance measurements. J. Appl. Microbiol. 84:981-987.
30. Leroy, F., and L. De Vuyst. 1999. The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC 494, a potential starter culture for sausage fermentation. Appl. Environ. Microbiol. 65:5350-5356.
31. Leroy, F., and L. De Vuyst. 1999. Temperature and pH conditions that prevail during fermentation of sausages are optimal for production of the antilisterial bacteriocin sakacin K. Appl. Environ. Microbiol. 65:974-981.
32. Leroy, F., and L. De Vuyst. 2001. Growth of the bacteriocin-producing Lactobacillus sakei strain CTC 494 in MRS broth is strongly reduced due to nutrient exhaustion: a nutrient depletion model for the growth of lactic acid bacteria. Appl. Environ. Microbiol. 67: 4407-4413.
33. Leroy, F., and L. De Vuyst. 2003. A combined model to predict the functionality of the bacteriocin-producing Lactobacillus sakei strain CTC 494. Appl. Environ. Microbiol. 69:1093-1099.
34. Leroy, F., and L. De Vuyst. 2005. Simulation of the effect of sausage ingredients and technology on the functionality of the bacteriocin-producing Lactobacillus sakei CTC 494 strain. Int. J. Food Microbiol. 100:141-152.
35. Leroy, F., K. Lievens, and L. De Vuyst. 2005. Modeling bacteriocin resistance and inactivation of Listeria innocua LMG 13568 by Lactobacillus sakei CTC 494 under sausage fermentation conditions. Appl. Environ. Microbiol. 71:7567-7570.
36. Leroy, F., J. Verluyten, and L. De Vuyst. 2006. Functional meat starter cultures for improved sausage fermentation. Int. J. Food Microbiol. 106:270-285.
37. Lucke, F. K. 2000. Utilization of microbes to process and preserve meat. Meat Sci. 56:105-115.
38. Marilao, C. G., M. R. Calapardo, C. E. Ciron, and F. B. Elegado. 2007. Antilisterial action of Pediococcus acidilactici AA5a in pork sausage fermentation. Philippine Agric. Sci. 90:40-45.
39. Mataragas, M., E. H. Drosinos, E. Tsakalidou, and J. Metaxopoulos. 2004. Influence of nutrients on growth and bacteriocin production by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L442. Antonie Leeuwenhoek 85:191-198.
40. Meisel, C., K. H. Gehlen, A. Fischer, and W. P. Hammes. 1989. Inhibition of the growth of Staphylococcus aureus in dry sausages by Lactobacillus curvatus, Micrococcus varians and Debaryomyces hansenii. Food Biotechnol. 3:145-168.
41. Nesbakken, T., G. Kapperud, and D. A. Caugant. 1996. Pathways of Listeria monocytogenes contamination in the meat processing industry. Int. J. Food Microbiol. 31:161-171.
42. Odriscoll, B., C. G. M. Gahan, and C. Hill. 1996. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl. Environ. Microbiol. 62:1693-1698.
43. Rantsiou, K., R. Urso, L. Iacumin, C. Cantoni, P. Cattaneo, G. Comi, and L. Cocolin. 2005. Culture-dependent and -independent methods to investigate the microbial ecology of Italian fermented sausages. Appl. Environ. Microbiol. 71:1977-1986.
44. Rebecchi, A., S. Crivori, P. G. Sarra, and P. S. Cocconcelli. 1998. Physiological and molecular techniques for the study of bacterial community development in sausage fermentation. J. Appl. Microbiol. 84:1043-1049.
45. Samelis, J., J. Metaxopoulos, M. Vlassi, and A. Pappa. 1998. Stability and safety of traditional Greek salami - a microbiological ecology study. Int. J. Food Microbiol. 44:69-82.
46. Sauer, C. J., J. Majkowski, S. Green, and R. Eckel. 1997. Foodborne illness outbreak associated with a semi-dry fermented sausage product. J. Food Prot. 60:1612-1617.
47. Scotter, S. L., S. Langton, B. Lombard, C. Lahellec, S. Schulten, N. Nagelkerke, P. H. in't Veld, and P. Rollier. 2001. Validation of ISO method 11290. Part 2. Enumeration of Listeria monocytogenes in foods. Int. J. Food Microbiol. 70:121-129.
48. Thevenot, D., M. L. Delignette-Muller, S. Christieans, and C. Vernozy-Rozand. 2005. Fate of Listeria monocytogenes in experimentally contaminated French sausages. Int. J. Food Microbiol. 101: 189-200.
49. Thevenot, D., M. L. Delignette-Muller, S. Christieans, and C. Vernozy-Rozand. 2005. Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and their products. Int. J. Food Microbiol. 102:85-94.
50. Thevenot, D., A. Dernburg, and C. Vernozy-Rozand. 2006. An updated review of Listeria monocytogenes in the pork meat industry and its products. J. Appl. Microbiol. 101:7-17.
51. Tilden, J., W. Young, A. M. McNamara, C. Custer, B. Boesel, M. LambertFair, J. Majkowski, D. Vugia, S. B. Werner, J. Hollingsworth, and J. G. Morris. 1996. A new route of transmission for Escherichia coli: infection from dry fermented salami. Am. J. Public Health 86:1142-1145.
52. Tyopponen, S., A. Markkula, E. Petaja, M. L. Suihko, and T. Mattila-Sandholm. 2003. Survival of Listeria monocytogenes in North European type dry sausages fermented by bioprotective meat starter cultures. Food Control 14:181-185.
53. Urso, R., K. Rantsiou, C. Cantoni, G. Comi, and L. Cocolin. 2006. Technological characterization of a bacteriocin-producing Lactobacillus sakei and its use in fermented sausages production. Int. J. Food Microbiol. 110:232-239.
54. Verluyten, J., F. Leroy, and L. de Vuyst. 2004. Influence of complex nutrient source on growth of and curvacin A production by sausage isolate Lactobacillus curvatus LTH 1174. Appl. Environ. Microbiol. 70:5081-5088.