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Inhibition of Listeria monocytogenes in Hot Dogs by Surface Application of Freeze-Dried Bacteriocin-Containing Powders from Lactic Acid Bacteria

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Abstract

Six lactic acid bacteria (LAB) strains, Lactococcus lactis BFE 920, L. lactis subsp. lactis ATCC 11454, L. lactis subsp. cremoris ATCC 14365, Lactobacillus curvatus L442, Lact. curvatus LTH 1174, and Lact. bavaricus MN, were grown in cheddar cheese whey supplemented with complex nutrient sources. Cell-free culture supernatants were freeze-dried, and the resulting bacteriocin-containing powders were applied on the surface of hot dogs that were inoculated (~4 log cfu/hot dog) with a five-strain Listeria monocytogenes cocktail. Hot dogs were vacuum-sealed and stored at 4 °C for 4 weeks. L. monocytogenes was enumerated, using both tryptic soy agar (TSA) and oxford listeria agar (OXA), on day 0 and at 1, 2, 3, and 4 weeks of the refrigerated storage. In hot dogs containing only the L. monocytogenes inoculum, L. monocytogenes counts increased from 4 up to 7 log cfu/hot dog. All samples containing freeze-dried bacteriocin-containing powders exhibited significantly lowered (P < 0.05) L. monocytogenes populations on the surface of hot dogs throughout the 4-week study except for bavaricin MN powder. Bacterial counts on hot dogs packed without any powder were statistically equal on day 0 when enumerated on OXA. Freeze-dried bacteriocin-containing powders from Lact. curvatus L442 and L. lactis subsp. cremoris ATCC 14365 decreased L. monocytogenes populations on the surface of hot dogs by greater than 2 log cfu/hot dog throughout the 4-week study. For the powdered bacteriocin preparations from L. lactis BFE 920, L. lactis subsp. lactis ATCC 11454, and Lact. curvatus LTH 1174, L. monocytogenes populations were determined to be approximately 3-log cfu/hot dog after 4 weeks of storage.

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References

  1. CDC (2014) Findings (2011) estimates of foodborne illness. Available: http://www.cdc.gov/foodborneburden/. Accessed 24 Aug 2015

  2. Centers for Disease Control and Prevention (CDC) (2015) Listeriosis. Available: http://search.cdc.gov/search?query=listeriosis&utf8=%E2%9C%93&affiliate=cdc-main

  3. Montville T, Matthews K, Kniel K (2012) Food microbiology: An introduction. ASM Press, Washington, p 419

    Google Scholar 

  4. Cheeseman M (2010) Agency response letter GRAS notice No. GRN 000228, 26 7 2010. Available: http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm221704.htm. Accessed 10 Aug 2015

  5. Barmpalia I, Geornaras I, Belk K, Scanga J, Kendall P, Smith G, Sofos J (2004) Control of Listeria monocytogenes on frankfurters with antimicrobials in the formulation and by dip** in organic acid solutions. J Food Prot 67(11):2456–2464

    CAS  Google Scholar 

  6. Leistner L, Gorris L (1995) Food preservation by hurdle technology. Trends Food Sci Technol 6:41–46

    Article  CAS  Google Scholar 

  7. Kouakou P, Ghalfi H, Dortu C, Evrard P, Thonart P (2010) Combined use of bacteriocin-producing strains to control Listeria monocytogenes regrowth in raw pork. Int J Food Sci Technol 45:937–943

    Article  CAS  Google Scholar 

  8. Cosentino S, Fadda M, Deplano M, Melis R, Pomata R, Pisano M (2012) Antilisterial activity of Nisin-like bacteriocin-producing Lactococcus lactis subsp. lactis isolated from traditional Sardinian dairy products. J Biomed Biotechnol. doi:10.1155/2012/376428

    Google Scholar 

  9. Dortu C, Huch M, Holzapfel W, Franz C, Thonart P (2008) Antilisterial activity of bacteriocin-producing Lactobacillus curvatus CWBWI-B28 and Lactobacillus sakei CWBI-B1365 on raw beef and poultry meat. Lett Appl Microbiol 47:581–586

    Article  CAS  Google Scholar 

  10. Kouakou P, Ghalfi H, Destain J, Dubois-Dauphin R, Evrard P, Thonart P (2009) Effects of curing sodium nitrite additive and natural meat fat on growth control of Listeria monocytogenes by the bacteriocin-producing Lactobacillus curvatus strain CWBI-B28. Food Microbiol 26:623–628

    Article  CAS  Google Scholar 

  11. Benkerroum N, Daoudi A, Hamraoui T, Ghalfi H, Thiry C, Duroy MEP, Roblain D, Thonart P (2005) Lyophilized preparations of bacteriogenic 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

    Article  CAS  Google Scholar 

  12. Buncic S, Avery S, Moorhead S (1997) Insufficient antilisterial capacity of low inoculum Lactobacillus cultures on long-term stored meats at 4 °C. Food Microbiol 34:157–170

    Article  CAS  Google Scholar 

  13. Hartmann H, Wilke T, Erdmann R (2011) Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. Int J Food Microbiol 146:192–199

    Article  CAS  Google Scholar 

  14. Milillo S, Story R, Pak D, O’Bryan C, Crandall P, Ricke S (2013) Antimicrobial properties of three lactic acid bacterial cultures and their cell free supernatants against Listeria monocytogenes. J Environ Sci Heal B 48:63–68

    Article  CAS  Google Scholar 

  15. Aasen I, Markussen S, Møretrø T, Katla T, Axelsson L, Naterstad K (2003) Interactions of the bacteriocins sakacin P and nisin with food constituents. Int J Food Microbiol 87:23–43

    Article  Google Scholar 

  16. Franklin N, Cooksey K, Getty J (2004) Inhibition of Listeria monocytogenes on the surface of individually packaged hot dogs with a packaging film coating containing nisin. J Food Prot 67:480–485

    CAS  Google Scholar 

  17. Katla T, Naterstad K, Vancanneyt M, Swings J, Axelsson L (2003) Differences in susceptibility of Listeria monocytogenes strains to sakacin A, pediocin PA-1, and nisin. Appl Environ Microbiol 69(8):4431–4437

    Article  CAS  Google Scholar 

  18. Winkowski K, Crandall A, Montville T (1993) Inhibition of Listeria monocytogenes by Lactobacillus bavaricus MN in beef systems at refrigeration temperatures. Appl Environ Microbiol 59(8):2552–2557

    CAS  Google Scholar 

  19. Zhang J, Liu G, Li P, Qu Y (2010) Pentocin 31-1, a novel meat-borne bacteriocin and its application as biopreservative in chill-stored tray-packaged pork meat. Food Control 21:198–202

    Article  CAS  Google Scholar 

  20. Trinetta V, Floros J, Cutter C (2010) Sakacin A-containing pullulan film: an active packaging system to control epidemic clones of Listeria monocytogenes in ready-to-eat foods. J Food Saf 30:366–381

    Article  CAS  Google Scholar 

  21. Randazzo C, Pitino I, Scifo G, Caggia C (2009) Biopreservation of minimally processed iceberg lettuces using a bacteriocin produced by Lactococcus lactis wild strain. Food Control 20:756–763

    Article  CAS  Google Scholar 

  22. Bizani D, Morrissy J, Dominguez A, Brandelli A (2008) Inhibition of Listeria monocytogenes in dairy products using the bacteriocin-like peptide cerein 8A. Int J Food Microbiol 21:229–233

    Article  Google Scholar 

  23. Sarika A, Lipton A, Aishwarya M, Dhivya R (2012) Isolation of a bacteriocin-producing Lactococcus lactis and application of its bacteriocin to manage spoilage bacteria in high-value marine fish under different storage temperatures. Appl Biochem Biotechnol 167:1280–1289

    Article  CAS  Google Scholar 

  24. Nakamura K, Arakawa K, Kawai Y, Yasuta N, Chujo T, Watanabe M, Iloka H, Tanioka M, Nishimura J, Kitazawa H, Tsurumi K, Saito T (2013) Food preservative potential of gassericin A-containing concentrate prepared from cheese whey culture supernatant of Lactobacillus gasseri LA39. Anim Sci J 84:144–149

    Article  CAS  Google Scholar 

  25. Azuma T, Bagenda D, Yamamoto T, Kawai Y, Yamakazi K (2006) Inhibition of Listeria monocytogenes by freeze-dried piscicocin CS526 fermentate in food. Lett Appl Microbiol 44:138–144

    Article  Google Scholar 

  26. Dimitrieva-Moats G, Unlu G (2012) Development of freeze-dried bacteriocin-containing preparations from lactic acid bacteria to inhibit Listeria monocytogenes and Staphylococcus aureus. Probiotics Antimicrob Protein 4(1):27–38

    Article  CAS  Google Scholar 

  27. Rivas F, Castro M, Vallejo M, Marguet E, Campos C (2014) Sakacin Q produced by Lactobacillus curvatus ACU-1: functionality characterization and antilisterial activity on cooked meat surface. Meat Sci 97:475–479

    Article  CAS  Google Scholar 

  28. Unlu G, Nielsen B, Ionita C (2015) Production of antilisterial bacteriocins from lactic acid bacteria in dairy-based media: a comparative study. Probiotics Antimicrob Proteins 4:259–274

    Article  Google Scholar 

  29. Franz C, Du Toit M, von Holy A, Schillinger U, Holzapfel W (1997) Production of Nisin-like bacteriocins by Lactococcus lactis strains isolated from vegetables. J Basic Microbiol 3:187–196

    Article  Google Scholar 

  30. Foong S, Dickson J (2004) Attachment of Listeria monocytogenes on ready-to-eat meats. J Food Prot 67(3):456–4621

    Google Scholar 

  31. Mataragas M, Metaxopoulos J, Drosinos E (2002) Characterization of two bacteriocins produced by Leuconostoc mesenteroides L124 and Lactobacillus curvatus L 442, isolated from dry fermented sausages. World J Microbiol Biotechnol 18:847–856

    Article  CAS  Google Scholar 

  32. Cleveland J, Montville T, Nes I, Chikindas M (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 34:1–20

    Article  Google Scholar 

  33. Mataragas M, Drosinos E, Metaxopoloulos J (2003) Antagonistic activity of lactic acid bacteria against Listeria monocytogenes in sliced cooked cured pork shoulder stored under vacuum or modified atmosphere. Food Microbiol 20:259–265

    Article  Google Scholar 

  34. Sant’Anna V, Quadros D, Motta A, Brandelli A (2013) Antibacterial activity of bacteriocin-like substance P34 on Listeria monocytogenes in chicken sausage. Braz J Microbiol 44(4):1163–1167

    Article  Google Scholar 

Download references

Acknowledgments

This project was supported by [1] The United States Department of Agriculture (USDSA) Cooperative State Research, Education, and Extension (CSREES) Hatch (IDA01369); [2] Idaho Beef Council (IBC); [3] United Dairymen of Idaho (UDI); and [4] MJ Murdock Charitable Trust. We thank all colleagues and institutions that provided us with bacterial strains. We also thank Dr. William Price of the College of Agricultural and Life Sciences (CALS) Statistical Services and Dr. Lee Deobald of the Department of Chemistry, both at the University of Idaho, for their assistance with statistical analyses and freeze-drying experiments, respectively.

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Correspondence to Gülhan Ünlü.

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Ünlü, G., Nielsen, B. & Ionita, C. Inhibition of Listeria monocytogenes in Hot Dogs by Surface Application of Freeze-Dried Bacteriocin-Containing Powders from Lactic Acid Bacteria. Probiotics & Antimicro. Prot. 8, 102–110 (2016). https://doi.org/10.1007/s12602-016-9213-2

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