Abstract
Nisin is frequently added as food additive to soft cheese to increase food safety against foodborne pathogens like Listeria monocytogenes. The goal of this study was the extension of the antimicrobial activity of nisin in sour curd cheese (SCC) by self-releasing adsorbed nisin from Neusilin UFL2 over production-based pH shift. First, the antimicrobial activity of nisin adsorbed to Neusilin UFL2 (UFL2-N) and free nisin was investigated in BHI broth at a pH range from 7.5 to 4.5 for each of six L. monocytogenes field isolates. UFL2-N showed similar minimal inhibition concentration to L. monocytogenes over time as free nisin. Distribution of nebulized, fluorescence-labelled UFL2 was homogenous on SCC surface. Thereafter, SCC surface was inoculated with L. monocytogenes and 0.004, 0.013, 0.026, and 0.132 mg mL−1 UFL2-N or free nisin. In SCC, L. monocytogenes was below quantification limit at 0.132 mg mL−1 UFL2-N or free nisin after 2 days of ripening. Collectively, UFL2-N enabled a slow release and antilisterial activity in vitro as well as in cheese manufacturing.
Similar content being viewed by others
References
Aasen IM, 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 87:35–43. https://doi.org/10.1016/S0168-1605(03)00047-3
Allerberger F (2003) Listeria: growth, phenotypic differentiation and molecular microbiology. FEMS Immunol Med Microbiol 3:183–189
Belitz H-D, Grosch W, Schieberle P (2001) Milch und Milchprodukte. In: Belitz H-D, Grosch W, Schieberle P (eds) Lehrbuch der Lebensmittelchemie. Springer, Heidelberg, pp 490–535
Bhatti M, Veeramachaneni A, Shelef LA (2004) Factors affecting the antilisterial effects of nisin in milk. Int J Food Microbiol 97:215–219
Buettner C, Noll M (2018) Differences in microbial key players in anaerobic degradation between biogas and sewage treatment plants. Int Biodeterior Biodegrad 133:124–132. https://doi.org/10.1016/j.ibiod.2018.06.012
Cheroutre-Vialette M, Lebert I, Hebraud M, Labadie J, Lebert A (1998) Effects of pH or aw stress on growth of Listeria monocytogenes. Int J Food Microbiol 42:71–77. https://doi.org/10.1016/S0168-1605(98)00064-6
Chollet E, Sebti I, Martial-Gros A, Degraeve P (2008) Nisin preliminary study as a potential preservative for sliced ripened cheese: NaCl, fat and enzymes influence on nisin concentration and its antimicrobial activity. Food Control 19:982–989. https://doi.org/10.1016/j.foodcont.2007.10.005
De Martinis ECP, Crandall AD, Mazzotta AS, Montville TJ (1997) Influence of pH, salt, and temperature on nisin resistance in Listeria monocytogenes. J Food Prot 60:420–423
Delves-Broughton J, Blackburn P, Evans RJ, Hugenholtz J (1996) Applications of the bacteriocin, nisin. Antonie Van Leeuwenhoek 69:193–202. https://doi.org/10.1007/BF00399424
EU (2011) Commission Regulation (EU) No 1129/2011 of 11 November 2011 amending Annex II to Regulation (EC) No 1333/2008 of the European Parliament and of the Council by establishing a union list of food additives. Commission Regulation (EU) No 1129/2011 of 11 November 2011 amending Annex II to Regulation (EC) No 1333/2008 of the European Parliament and of the Council by establishing a union list of food additives
Ferreira MA, Lund BM (1996) The effect of nisin on Listeria monocytogenes in culture medium and long-life cottage cheese. Lett Appl Microbiol 22:433–438
Fretz R, Sagel U, Ruppitsch W, Pietzka AT, Stöger A, Huhulescu S, Heuberger S, Pichler J, Much P, Pfaff G, Stark K, Prager R, Flieger A, Feenstra O, Allerberger F (2010) Listeriosis outbreak caused by acid curd cheese ‘Quargel’, Austria and Germany 2009. Euro Surveill. https://doi.org/10.2807/ese.15.05.19477-en
Gill C, Reichel M (1989) Growth of the cold-tolerant pathogens Yersinia enterocolitica, Aeromonas hydrophila and Listeria monocytogenes on high-pH beef packaged under vacuum or carbon dioxide. Food Microbiol 6:223–230
Hammami R, Zouhir A, Le Lay C, Ben Hamida J, Fliss I (2010) BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol. https://doi.org/10.1186/1471-2180-10-22
Ibarguren C, Naranjo PM, Stötzel C, Audisio MC, Sham EL, Farfán Torres EM, Müller FA (2014) Adsorption of nisin on raw montmorillonite. Appl Clay Sci 90:88–95. https://doi.org/10.1016/j.clay.2013.12.031
Kudamala S, Murthy KVR (2017) Applicability of a novel carrier, Neusilin UFL2, for the preparation of domperidone liquisolid tablets. World J Pharm Pharam Sci 6:1662–1671
Ma Y-H, Wang Q, Gong J, Wu XY (2016) Formulation of granules for site-specific delivery of an antimicrobial essential oil to the animal intestinal tract. J Pharm Sci 105:1124–1133. https://doi.org/10.1016/j.xphs.2015.10.001
Mallappa MK, Kesarla R, Banakar S (2015) Calcium alginate-Neusilin US2 nanocomposite microbeads for oral sustained drug delivery of poor water soluble drug aceclofenac sodium. J Drug Deliv. https://doi.org/10.1155/2015/826981
Martinez-Rios V, Dalgaard P (2018) Prevalence of Listeria monocytogenes in European cheeses: a systematic review and meta-analysis. Food Control 84:205–214. https://doi.org/10.1016/j.foodcont.2017.07.020
McElhatton A, Marshall RJ (2007) Food safety: a practical and case study approach. Springer, New York
Meira SMM, Jardim AI, Brandelli A (2015) Adsorption of nisin and pediocin on nanoclays. Food Chem 188:161–169. https://doi.org/10.1016/j.foodchem.2015.04.136
Ming X, Daeschel MA (1993) Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott A. J Food Prot 56:944–948
Muyzer G, De Waal E, Uitterlinden A (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Nogva HK, Naterstad KR, Holck A, Lillehaug D (2000) Application of 5′-nuclease PCR for quantitative detection of Listeria monocytogenes in pure cultures, water, skim milk, and unpasteurized whole milk. Appl Environ Microbiol 66:4266–4271
Noll M, Kleta S, Al Dahouk S (2018) Antibiotic susceptibility of 259 Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany. J Infect Public Health 11:572–577. https://doi.org/10.1016/j.jiph.2017.12.007
Pawar DD, Malik S, Bhilegaonkar KN, Barbuddhe SB (2000) Effect of nisin and its combination with sodium chloride on the survival of Listeria monocytogenes added to raw buffalo meat mince. Meat Sci 56:215–219. https://doi.org/10.1016/S0309-1740(00)00043-7
Peyratout CS, Dähne L (2004) Tailor-made polyelectrolyte microcapsules: from multilayers to smart containers. Angew Chem Int Ed Engl 43:3762–3783. https://doi.org/10.1002/anie.200300568
Prombutara P, Kulwatthanasal Y, Supaka N, Sramala I, Chareonpornwattana S (2012) Production of nisin-loaded solid lipid nanoparticles for sustained antimicrobial activity. Food Control 24:184–190. https://doi.org/10.1016/j.foodcont.2011.09.025
Ramsaran H, Chen J, Brunke B, Hill A, Griffiths MW (1998) Survivial of bioluminescent Listeria monocytogenes and Escherichia coli 0157:H7 in soft cheeses. J Dairy Sci 81:1810–1817. https://doi.org/10.3168/jds.S0022-0302(98)75750-9
Rogga KJ, Samelis J, Kakouri A, Katsiari MC, Savvaidis IN, Kontominas MG (2005) Survival of Listeria monocytogenes in Galotyri, a traditional Greek soft acid-curd cheese, stored aerobically at 4°C and 12°C. Int Dairy J 15:59–67. https://doi.org/10.1016/j.idairyj.2004.05.002
Santaniello M, Giannini G (2016) A versatile and stable mixture of fish oil and resveratrol in a powder formulation. Nutr Food Technol https://doi.org/10.16966/2470-6086.125
Sulzer G, Busse M (1991) Growth inhibition of Listeria spp. on camembert cheese by bacteria producing inhibitory substances. Int J Food Microbiol 14:287–296. https://doi.org/10.1016/0168-1605(91)90120-E
Sun Z, Zhong J, Liang X, Liu J, Chen X, Huan L (2009) Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob Agents Chemother 53:1964–1973. https://doi.org/10.1128/AAC.01382-08
Were LM, Bruce B, Davidson PM, Weiss J (2004) Encapsulation of nisin and lysozyme in liposomes enhances efficacy against Listeria monocytogenes. J Food Prot 67:922–927. https://doi.org/10.4315/0362-028X-67.5.922
Yen LC, Sofos JN, Schmidt GR (1991) Effect of meat curing ingredients on thermal destruction of Listeria monocytogenes in ground pork. J Food Prot 54:408–412. https://doi.org/10.4315/0362-028X-54.6.408
Acknowledgements
This research was financially supported by Federal Ministry for Economic Affairs and Energy on the basis of a decision by the German Bundestag (KF3083302SK3) and technical alliance Oberfranken (TAO).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Szendy, M., Westhaeuser, F., Baude, B. et al. Controlled release of nisin from Neusilin particles to enhance food safety of sour curd cheese. J Food Sci Technol 56, 1613–1621 (2019). https://doi.org/10.1007/s13197-019-03577-0
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-019-03577-0