A Comprehensive Review of Emulsion-Based Nisin Delivery Systems for Food Safety
Abstract
:1. Introduction
2. Nisin—Basic Facts and Physicochemical Properties
3. Factors Limiting Nisin Effectiveness
4. Emulsions—Terminology, Methods of Preparation and Physicochemical Characterization
Property | Macroemulsions | Nanoemulsions | Microemulsions | Pickering Emulsions |
---|---|---|---|---|
Size (Radius) | 100 nm–100 µm | 10–100 nm | 2–100 nm | 0.1–100 µm |
Shape | Spherical | Spherical | Spherical, lamellar rod micelles or sponge-like | Spherical |
Stability | Thermodynamically unstable, weakly kinetically stable | Thermodynamically unstable, kinetically stable | Thermodynamically stable | Highly stable due to irreversible adsorption of particles |
Polydispersity Index | Often high (0.2–0.5) | Typically low (0.1–0.3) | Typically low (0.1–0.3) | Typically low (0.1–0.3) |
Stabilization Mechanism | Surfactants | Surfactants | Surfactants and co-surfactants | Solid particles (e.g., silica, proteins, cellulose, bacteria) |
Transparency | Opaque | Translucent/transparent | Transparent | Opaque |
- a.
- High-energy methods rely on applying high shear forces to disperse the discontinuous phase into microscopic droplets. These are as follows:
- i
- ii
- Microfluidization is an emulsification technique where a pre-formed emulsion is subjected to high pressure and forced through precisely designed microchannels. This process divides the emulsion into multiple microstreams that collide with each other, generating intense shear and impact forces [57,58].
- iii
- b.
- Low-energy methods require minimal energy because they utilize the system’s inherent chemical energy (or chemical potential of components). These are as follows:
- i
- The Phase Inversion Temperature (PIT) method takes advantage of the temperature-dependent behavior of certain emulsifiers, which can shift between hydrophilic and lipophilic properties. By carefully controlling the temperature, this technique induces a phase inversion, resulting in the formation of nanoemulsions with highly stable and uniformly sized droplets [54,61].
- ii
- The Phase Inversion Composition (PIC) method is a process that involves altering the composition of a system by introducing substances such as electrolytes or alcohols. These additives modify the properties of the emulsifier, thereby triggering a phase inversion that results in the formation of nanoemulsions [62].
- iii
- iv
- Emulsion Inversion Point (EIP) technique involves the creation of a water-in-oil (W/O) emulsion with a high oil-to-water ratio. As water is gradually added, a critical point is reached where the water content exceeds the oil content, causing a phase inversion from W/O to oil-in-water (O/W) emulsion [54,61].
- v
- Membrane emulsification is an energy-efficient technique in which the dispersed phase is forced through the pores of a specialized membrane, thereby generating droplets on its surface. These droplets are then detached and carried away by the flow of the continuous phase or through the rotation of the membrane itself [65].
Method | Energy | Macroemulsions | Nanoemulsions | Microemulsions | Pickering Emulsions |
---|---|---|---|---|---|
Simple Stirring/Shaking | low | ✓ | ✗ | ✗ | ✓ 1 |
Magnetic Stirring | low | ✓ | ✗ | ✗ | ✓ |
High-Speed Homogenization (HPH) | high | ✓ | ✓ | ✗ | ✓ |
High-Pressure Homogenization | high | ✓ | ✓ | ✗ | ✓ |
Microfluidization | high | ✗ | ✓ | ✗ | ✓ |
Ultrasonication | high | ✗ | ✓ | ✗ | ✓ |
Phase Inversion Temperature (PIT) | low | ✗ | ✓ | ✓ 2 | ✗ |
Spontaneous Emulsification | low | ✗ | ✓ | ✓ 2 | ✗ |
Emulsion Inversion Point (EIP) | low | ✗ | ✓ | ✗ | ✗ |
Membrane emulsification | low | ✗ | ✓ | ✗ | ✓ |
Method | Purpose | References |
---|---|---|
DLS | Particle size and polydispersity index | [77,89,90,91,92,93,94,95,96,97,98,99] |
Small Angle X-ray scattering (SAXS) | Micelles’ structure | [92] |
ζ potential | Electrophoretic mobility | [77,89,99,100,101] |
SEM | Particle morphology | [96] |
TEM | Particle morphology | [89,93,98,101,102] |
Optical Microscopy | Emulsion morphology | [98,102] |
FT-IR | Chemical structure and intermolecular interactions | [93,96,98] |
UV-VIS | Turbidity (coalescence and aggregation phenomena) or transparency | [77,93,95,96] |
Electron Paramagnetic Resonance (EPR) | Interfacial properties | [77,90,91,92,93,95,96] |
High-Performance Size-Exclusion Chromatography-(HPSEC)-Multi-angle Laser Light Scattering (MALLS) | Weight-average, molecular masses-root mean, square radius (RZ) | [99,101,103] |
Electrical conductivity measurements | Information about the continuous phase in w/o microemulsions | [42,91,92] |
Rheological Analysis | Viscosity | [45,90,102] |
5. Encapsulation Systems of Nisin Based on Emulsion
5.1. Coarse Emulsions
5.2. Nanoemulsions
5.3. Microemulsions
5.4. Pickering Emulsions
5.5. Double Emulsions
5.6. Use of Nanoemulsions for the Preparation of Other Delivery Systems
5.6.1. Organogels
5.6.2. Nano/Microcapsules
5.6.3. Film/Coating-Based Delivery Systems
5.6.4. Smart Packaging
6. Nisin’s Prospects in the Future
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Galanakis, C.M. The future of food. Foods 2024, 13, 506. [Google Scholar] [CrossRef] [PubMed]
- Peltner, J.; Thiele, S. Convenience-based food purchase patterns: Identification and associations with dietary quality, sociodemographic factors and attitudes. Public Health Nutr. 2018, 21, 558–570. [Google Scholar] [CrossRef]
- Rukavina, M. Navigating food safety: Insights, innovations, and consumer trends in changing food patterns. J. Verbrauch. Lebensm. 2024, 19, 1–2. [Google Scholar] [CrossRef]
- McLinden, T.; Sargeant, J.M.; Thomas, M.K.; Papadopoulos, A.; Fazil, A. Component costs of foodborne illness: A scoping review. BMC Public Health 2014, 14, 509. [Google Scholar] [CrossRef]
- Gálvez, A.; Abriouel, H.; López, R.L.; Omar, N.B. Bacteriocin-based strategies for food biopreservation. Int. J. Food Microbiol. 2007, 120, 51–70. [Google Scholar] [CrossRef] [PubMed]
- Singh, V.P. Recent approaches in food bio-preservation—A review. Open Vet. J. 2018, 8, 104–111. [Google Scholar] [CrossRef] [PubMed]
- Anand, S.P.; Sati, N. Artificial preservatives and their harmful effects: Looking toward nature for safer alternatives. Int. J. Pharm. Sci. Res. 2013, 4, 2496–2501. [Google Scholar] [CrossRef]
- Quinto, E.J.; Caro, I.; Villalobos-Delgado, L.H.; Mateo, J.; De-Mateo-Silleras, B.; Redondo-Del-Río, M.P. Food safety through natural antimicrobials. Antibiotics 2019, 8, 208. [Google Scholar] [CrossRef]
- Drider, D.; Bendali, F.; Naghmouchi, K.; Chikindas, M.L. Bacteriocins: Not only antibacterial agents. Probiotics Antimicrob. Proteins 2016, 8, 177–182. [Google Scholar] [CrossRef]
- Putri, D.A.; Lei, J.; Rossiana, N.; Syaputri, Y. Biopreservation of food using bacteriocins from lactic acid bacteria: Classification, mechanisms, and commercial applications. Int. J. Food Microbiol. 2024, 2024, 8723968. [Google Scholar] [CrossRef]
- Mokoena, M.P. Lactic acid bacteria and their bacteriocins: Classification, biosynthesis and applications against uropathogens: A mini-review. Molecules 2017, 22, 1255. [Google Scholar] [CrossRef] [PubMed]
- Rogers, L.A. The inhibiting effect of Streptococcus lactis on Lactobacillus bulgaricus. J. Bacteriol. 1928, 16, 321–325. [Google Scholar] [CrossRef] [PubMed]
- Delves-Broughton, J. Bacteria|Nisin. In Encyclopedia of Food Microbiology, 2nd ed.; Batt, C.A., Tortorello, M.L., Eds.; Academic Press: Oxford, UK, 2014; pp. 187–193. [Google Scholar] [CrossRef]
- Wang, R.; Yu, S.; Huang, Y.; Liu, Y. Synthesis, high yield strategy and application of nisin: A review. Int. J. Food Sci. Technol. 2023, 58, 2829–2841. [Google Scholar] [CrossRef]
- Gharsallaoui, A.; Oulahal, N.; Joly, C.; Degraeve, P. Nisin as a food preservative: Part 1: Physicochemical properties, antimicrobial activity, and main uses. Crit. Rev. Food Sci. Nutr. 2016, 56, 1262–1274. [Google Scholar] [CrossRef]
- Horinouchi, S.; Ueda, K.; Nakayama, J.; Ikeda, T. Cell-to-Cell Communications among Microorganisms. In Comprehensive Natural Products II: Chemistry and Biology; Elsevier Ltd.: Amsterdam, The Netherlands, 2010; Volume 4, pp. 283–337. [Google Scholar]
- Reunanen, J. Lantibiotic Nisin and Its Detection Methods; University of Helsinki: Helsinki, Finland, 2007. [Google Scholar]
- Shin, J.M.; Gwak, J.W.; Kamarajan, P.; Fenno, J.C.; Rickard, A.H.; Kapila, Y.L. Biomedical applications of nisin. J. Appl. Microbiol. 2016, 120, 1449–1465. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Du, Y.; Qiu, Z.; Liu, Z.; Qiao, J.; Li, Y.; Caiyin, Q. Nisin variants generated by protein engineering and their properties. Bioengineering 2022, 9, 251. [Google Scholar] [CrossRef]
- Sonomoto, K.; Chinachoti, N.; Endo, N.; Ishizaki, A. Biosynthetic production of nisin Z by immobilized Lactococcus lactis IO-1. J. Mol. Catal. B Enzym. 2000, 10, 325–334. [Google Scholar] [CrossRef]
- Jančič, U.; Gorgieva, S. Bromelain and nisin: The natural antimicrobials with high potential in biomedicine. Pharmaceutics 2022, 14, 76. [Google Scholar] [CrossRef]
- Hurst, A. Nisin. In Advances in Applied Microbiology; Perlman, D., Laskin, A.I., Eds.; Academic Press: Cambridge, MA, USA, 1981; Volume 27, pp. 85–123. [Google Scholar] [CrossRef]
- Liu, W.; Hansen, J.N. Some chemical and physical properties of nisin, a small-protein antibiotic produced by Lactococcus lactis. Appl. Environ. Microbiol. 1990, 56, 2551–2558. [Google Scholar] [CrossRef]
- Tramer, J.; Fowler, G.G. Estimation of nisin in foods. J. Sci. Food Agric. 1964, 15, 522–528. [Google Scholar] [CrossRef]
- Davies, E.A.; Bevis, H.E.; Potter, R.; Harris, J.; Williams, G.C.; Delves-Broughton, J. Research note: The effect of pH on the stability of nisin solution during autoclaving. Lett. Appl. Microbiol. 1998, 27, 186–187. [Google Scholar] [CrossRef]
- Thomas, L.V.; Ingram, R.E.; Bevis, H.E.; Davies, E.A.; Milne, C.F.; Delves-Broughton, J. Effective use of nisin to control Bacillus and Clostridium spoilage of a pasteurized mashed potato product. J. Food Prot. 2002, 65, 1580–1585. [Google Scholar] [CrossRef] [PubMed]
- Authority, E.F.S. Opinion of the Scientific Panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to The use of nisin (E 234) as a food additive. EFSA J. 2006, 4, 314. [Google Scholar] [CrossRef]
- Li, Q.; Montalban-Lopez, M.; Kuipers, O.P. Increasing the antimicrobial activity of nisin-based lantibiotics against gram-negative pathogens. Appl. Environ. Microbiol. 2018, 84, e00052-18. [Google Scholar] [CrossRef]
- Breukink, E.; de Kruijff, B. The lantibiotic nisin, a special case or not? Biochim. Biophys. Acta 1999, 1462, 223–234. [Google Scholar] [CrossRef]
- Tagg, J.R.; Dajani, A.S.; Wannamaker, L.W. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 1976, 40, 722–756. [Google Scholar] [CrossRef]
- Hagiwara, A.; Imai, N.; Nakashima, H.; Toda, Y.; Kawabe, M.; Furukawa, F.; Delves-Broughton, J.; Yasuhara, K.; Hayashi, S.M. A 90-day oral toxicity study of nisin A, an anti-microbial peptide derived from Lactococcus lactis subsp. lactis, in F344 rats. Food Chem. Toxicol. 2010, 48, 2421–2428. [Google Scholar] [CrossRef]
- O’Reilly, C.; Grimaud, G.M.; Coakley, M.; O’Connor, P.M.; Mathur, H.; Peterson, V.L.; O’Donovan, C.M.; Lawlor, P.G.; Cotter, P.D.; Stanton, C.; et al. Modulation of the gut microbiome with nisin. Sci. Rep. 2023, 13, 7899. [Google Scholar] [CrossRef]
- Pablo, M.A.; Gaforio, J.J.; Gallego, A.M.; Ortega, E.; Gálvez, A.M.; Alvarez de Cienfuegos López, G. Evaluation of immunomodulatory effects of nisin-containing diets on mice. FEMS Immunol. Med. Microbiol. 1999, 24, 35–42. [Google Scholar] [CrossRef]
- Additives, E.; Panel, o.F.; Food, N.S.a.t.; Younes, M.; Aggett, P.; Aguilar, F.; Crebelli, R.; Dusemund, B.; Filipič, M.; Frutos, M.J.; et al. Safety of nisin (E 234) as a food additive in the light of new toxicological data and the proposed extension of use. EFSA J. 2017, 15, e05063. [Google Scholar] [CrossRef]
- Soltani, S.; Hammami, R.; Cotter, P.D.; Rebuffat, S.; Said, L.B.; Gaudreau, H.; Bédard, F.; Biron, E.; Drider, D.; Fliss, I. Bacteriocins as a new generation of antimicrobials: Toxicity aspects and regulations. FEMS Microbiol. Rev. 2020, 45, fuaa039. [Google Scholar] [CrossRef]
- Abd-Elhamed, E.Y.; El-Bassiony, T.A.E.; Elsherif, W.M.; Shaker, E.M. Enhancing Ras cheese safety: Antifungal effects of nisin and its nanoparticles against Aspergillus flavus. BMC Vet. Res. 2024, 20, 493. [Google Scholar] [CrossRef]
- Bouttefroy, A.; Mansour, M.; Linder, M.; Milliere, J.B. Inhibitory combinations of nisin, sodium chloride, and pH on Listeria monocytogenes ATCC 15313 in broth by an experimental design approach. Int. J. Food Microbiol. 2000, 54, 109–115. [Google Scholar] [CrossRef] [PubMed]
- Daeschel, M.A. CHAPTER 4—Applications and interactions of bacteriocins from lactic acid bacteria in foods and beverages. In Bacteriocins of Lactic Acid Bacteria; Hoover, D.G., Steenson, L.R., Eds.; Academic Press: Cambridge, MA, USA, 1993; pp. 63–91. [Google Scholar] [CrossRef]
- Gänzle, M.G.; Weber, S.; Hammes, W.P. Effect of ecological factors on the inhibitory spectrum and activity of bacteriocins. Int. J. Food Microbiol. 1999, 46, 207–217. [Google Scholar] [CrossRef] [PubMed]
- Bell, R.G.; Lacy, K.M.D. Factors influencing the determination of nisin in meat products. Int. J. Food Sci. Technol. 2007, 21, 1–7. [Google Scholar] [CrossRef]
- Henning, S.; Metz, R.; Hammes, W.P. New aspects for the application of nisin to food products based on its mode of action. Int. J. Food Microbiol. 1986, 3, 135–141. [Google Scholar] [CrossRef]
- Jung, D.S.; Bodyfelt, F.W.; Daeschel, M.A. Influence of fat and emulsifiers on the efficacy of nisin in inhibiting Listeria monocytogenes in fluid milk. J. Dairy. Sci. 1992, 75, 387–393. [Google Scholar] [CrossRef]
- Bhatti, M.; Veeramachaneni, A.; Shelef, L.A. Factors affecting the antilisterial effects of nisin in milk. Int. J. Food Microbiol. 2004, 97, 215–219. [Google Scholar] [CrossRef]
- Zapico, P.; de Paz, M.; Medina, M.; Nuñez, M. The effect of homogenization of whole milk, skim milk and milk fat on nisin activity against Listeria innocua. Int. J. Food Microbiol. 1999, 46, 151–157. [Google Scholar] [CrossRef]
- Castro, M.P.; Rojas, A.M.; Campos, C.A.; Gerschenson, L.N. Effect of preservatives, tween 20, oil content and emulsion structure on the survival of Lactobacillus fructivorans in model salad dressings. LWT—Food Sci. Technol. 2009, 42, 1428–1434. [Google Scholar] [CrossRef]
- Tadros, T.F. Emulsions: Formation, Stability, Industrial Applications; Walter de Gruyter GmbH & Co KG: Berlin, Germany, 2016. [Google Scholar]
- McClements, D.J. Food Emulsions: Principles, Practices, and Techniques; CRC Press: Boca Raton, FL, USA, 2004. [Google Scholar] [CrossRef]
- McClements, D.J. Edible nanoemulsions: Fabrication, properties, and functional performance. Soft Matter 2011, 7, 2297–2316. [Google Scholar] [CrossRef]
- McClements, D.J. Nanoemulsions versus microemulsions: Terminology, differences, and similarities. Soft Matter 2012, 8, 1719–1729. [Google Scholar] [CrossRef]
- Yang, Y.; Fang, Z.; Chen, X.; Zhang, W.; Xie, Y.; Chen, Y.; Liu, Z.; Yuan, W. An overview of pickering emulsions: Solid-particle materials, classification, morphology, and applications. Front. Pharmacol. 2017, 8, 287. [Google Scholar] [CrossRef] [PubMed]
- McClements, D.J. Critical review of techniques and methodologies for characterization of emulsion stability. Crit. Rev. Food Sci. Nutr. 2007, 47, 611–649. [Google Scholar] [CrossRef] [PubMed]
- Sharma, M.K.; Shah, D.O. Introduction to Macro- and Microemulsions. ACS Symposium Series; American Chemical Society: Washington, DC, USA, 1985. [Google Scholar]
- Walstra, P. Physical Chemistry of Foods; Instrumentation Science & Technology; CRC Press: Boca Raton, FL, USA, 2002. [Google Scholar] [CrossRef]
- McClements, D.J.; Rao, J. Food-grade nanoemulsions: Formulation, fabrication, properties, performance, biological fate, and potential toxicity. Crit. Rev. Food Sci. Nutr. 2011, 51, 285–330. [Google Scholar] [CrossRef]
- Tadros, T.; Izquierdo, P.; Esquena, J.; Solans, C. Formation and stability of nano-emulsions. Adv. Colloid. Interface Sci. 2004, 108–109, 303–318. [Google Scholar] [CrossRef]
- Patrignani, F.; Lanciotti, R. Applications of high and ultra high pressure homogenization for food safety. Front. Microbiol. 2016, 7, 1132. [Google Scholar] [CrossRef]
- Mert, I.D. The applications of microfluidization in cereals and cereal-based products: An overview. Crit. Rev. Food Sci. Nutr. 2020, 60, 1007–1024. [Google Scholar] [CrossRef]
- He, X.; Chen, J.; He, X.; Feng, Z.; Li, C.; Liu, W.; Dai, T.; Liu, C. Industry-scale microfluidization as a potential technique to improve solubility and modify structure of pea protein. Innov. Food Sci. Emerg. Technol. 2021, 67, 102582. [Google Scholar] [CrossRef]
- Modarres-Gheisari, S.M.M.; Gavagsaz-Ghoachani, R.; Malaki, M.; Safarpour, P.; Zandi, M. Ultrasonic nano-emulsification—A review. Ultrason. Sonochem. 2019, 52, 88–105. [Google Scholar] [CrossRef]
- Jafari, M.; He, Y.; Bhandari, B. Optimization of nano-emulsions production by microfluidization. Eur. Food Res. Technol. 2007, 225, 733–741. [Google Scholar] [CrossRef]
- Anton, N.; Vandamme, T.F. The universality of low-energy nano-emulsification. Int. J. Pharm. 2009, 377, 142–147. [Google Scholar] [CrossRef] [PubMed]
- Salager, J.-L.; Forgiarini, A.; Marquez, L.; Peña, A.; Pizzino, A.; Rodriguez, M.P.; Rondón-González, M. Using Emulsion Inversion in Industrial Processes. Adv. Colloid. Interface Sci. 2004, 108–109, 259–272. [Google Scholar] [CrossRef] [PubMed]
- Gurpreet, K.; Singh, S. Review of nanoemulsion formulation and characterization techniques. Indian. J. Pharm. Sci. 2018, 80, 781–789. [Google Scholar] [CrossRef]
- Solans, C.; Morales, D.; Homs, M. Spontaneous emulsification. Curr. Opin. Colloid Interface Sci. 2016, 22, 88–93. [Google Scholar] [CrossRef]
- Goindi, S.; Kaur, A.; Kaur, R.; Kalra, A.; Chauhan, P. 19—Nanoemulsions: An emerging technology in the food industry. In Emulsions; Grumezescu, A.M., Ed.; Academic Press: Cambridge, MA, USA, 2016; pp. 651–688. [Google Scholar] [CrossRef]
- Rao, J.; McClements, D.J. Formation of flavor oil microemulsions, nanoemulsions and emulsions: Influence of composition and preparation method. J. Agric. Food Chem. 2011, 59, 5026–5035. [Google Scholar] [CrossRef]
- Kaustav, B. Importance of surface energy in nanoemulsion. In Nanoemulsions; Kai Seng, K., Voon Loong, W., Eds.; IntechOpen: Rijeka, Croatia, 2019; p. Ch. 6. [Google Scholar] [CrossRef]
- Taylor, P. Ostwald ripening in emulsions. Adv. Colloid Interface Sci. 1998, 75, 107–163. [Google Scholar] [CrossRef]
- Gupta, A.; Eral, H.B.; Hatton, T.A.; Doyle, P.S. Nanoemulsions: Formation, properties and applications. Soft Matter 2016, 12, 2826–2841. [Google Scholar] [CrossRef]
- Chung, C.; McClements, D.J. Chapter 17—Characterization of Physicochemical Properties of Nanoemulsions: Appearance, Stability, and Rheology. In Nanoemulsions; Jafari, S.M., McClements, D.J., Eds.; Academic Press: Cambridge, MA, USA, 2018; pp. 547–576. [Google Scholar] [CrossRef]
- Mason, T.G.; Wilking, J.N.; Meleson, K.; Chang, C.B.; Graves, S.M. Nanoemulsions: Formation, structure, and physical properties. J. Phys. Condens. Matter 2006, 18, R635. [Google Scholar] [CrossRef]
- Gräwert, T.W.; Svergun, D.I. Structural modeling using solution small-angle X-ray scattering (SAXS). J. Mol. Biol. 2020, 432, 3078–3092. [Google Scholar] [CrossRef]
- Li, T.; Senesi, A.J.; Lee, B. Small Angle X-ray Scattering for Nanoparticle Research. Chem. Rev. 2016, 116, 11128–11180. [Google Scholar] [CrossRef] [PubMed]
- Jin, W.; Xu, W.; Liang, H.; Li, Y.; Liu, S.; Li, B. 1—Nanoemulsions for food: Properties, production, characterization, and applications. In Emulsions; Grumezescu, A.M., Ed.; Academic Press: Cambridge, MA, USA, 2016; pp. 1–36. [Google Scholar] [CrossRef]
- Sah, M.K.; Gautam, B.; Pokhrel, K.P.; Ghani, L.; Bhattarai, A. Quantification of the quercetin nanoemulsion technique using various parameters. Molecules 2023, 28, 2540. [Google Scholar] [CrossRef] [PubMed]
- Kupikowska-Stobba, B.; Domagała, J.; Kasprzak, M.M. Critical review of techniques for food emulsion characterization. Appl. Sci. 2024, 14, 1069. [Google Scholar] [CrossRef]
- Sánchez-Ortega, I.; García-Almendárez, B.E.; Santos-López, E.M.; Reyes-González, L.R.; Regalado, C. Characterization and antimicrobial effect of starch-based edible coating suspensions. Food Hydrocoll. 2016, 52, 906–913. [Google Scholar] [CrossRef]
- Bešić, E.; Rajić, Z.; Šakić, D. Advancements in electron paramagnetic resonance (EPR) spectroscopy: A comprehensive tool for pharmaceutical research. J. Acta Pharm. 2024, 74, 551–594. [Google Scholar] [CrossRef] [PubMed]
- Mudalige, T.; Qu, H.; Van Haute, D.; Ansar, S.M.; Paredes, A.; Ingle, T. Chapter 11—Characterization of nanomaterials: Tools and challenges. In Nanomaterials for Food Applications; López Rubio, A., Fabra Rovira, M.J., Martínez Sanz, M., Gómez-Mascaraque, L.G., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 313–353. [Google Scholar] [CrossRef]
- ISO 22412:2017; Particle Size Analysis — Dynamic Light Scattering (DLS). International Organization for Standardization (ISO): Geneva, Switzerland, 2017.
- McClements, D.J. Food Emulsions: Principles, Practices, and Techniques, 3rd ed.; CRC Press: Boca Raton, FL, USA, 2015. [Google Scholar]
- Borreani, J.; Leonardi, C.; Moraga, G.; Quiles, A.; Hernando, I. How do different types of emulsifiers/stabilizers affect the in vitro intestinal digestion of O/W emulsions? Food Biophys. 2019, 14, 313–325. [Google Scholar] [CrossRef]
- Gilbert, L.; Savary, G.; Grisel, M.; Picard, C. Predicting sensory texture properties of cosmetic emulsions by physical measurements. Chemometr Intell. Lab. Syst. 2013, 124, 21–31. [Google Scholar] [CrossRef]
- Jafari, S.M.; Beheshti, P.; Assadpoor, E. Rheological behavior and stability of d-limonene emulsions made by a novel hydrocolloid (Angum gum) compared with Arabic gum. J. Food Eng. 2012, 109, 1–8. [Google Scholar] [CrossRef]
- Aswathanarayan, J.B.; Vittal, R.R. Nanoemulsions and their potential applications in food industry. Front. Sustain. Food Syst. 2019, 3, 95. [Google Scholar] [CrossRef]
- Gilbert, L.; Picard, C.; Savary, G.; Grisel, M. Rheological and textural characterization of cosmetic emulsions containing natural and synthetic polymers: Relationships between both data. Colloids Surf. A Physicochem. Eng. Asp. 2013, 421, 150–163. [Google Scholar] [CrossRef]
- Wooster, T.J.; Golding, M.; Sanguansri, P. Impact of oil type on nanoemulsion formation and ostwald ripening stability. Langmuir 2008, 24, 12758–12765. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Reineccius, G. Preparation and stability of W/O/W emulsions containing sucrose as weighting agent. Flavour. Fragr. J. 2016, 31, 51–56. [Google Scholar] [CrossRef]
- Bi, L.; Yang, L.; Bhunia, A.K.; Yao, Y. Carbohydrate nanoparticle-mediated colloidal assembly for prolonged efficacy of bacteriocin against food pathogen. Biotechnol. Bioeng. 2011, 108, 1529–1536. [Google Scholar] [CrossRef]
- Chatzidaki, M.D.; Balkiza, F.; Gad, E.; Alexandraki, V.; Avramiotis, S.; Georgalaki, M.; Papadimitriou, V.; Tsakalidou, E.; Papadimitriou, K.; Xenakis, A. Reverse micelles as nano-carriers of nisin against foodborne pathogens. Part II: The case of essential oils. Food Chem. 2019, 278, 415–423. [Google Scholar] [CrossRef]
- Chatzidaki, M.D.; Papadimitriou, K.; Alexandraki, V.; Balkiza, F.; Georgalaki, M.; Papadimitriou, V.; Tsakalidou, E.; Xenakis, A. Reverse micelles as nanocarriers of nisin against foodborne pathogens. Food Chem. 2018, 255, 97–103. [Google Scholar] [CrossRef]
- Chatzidaki, M.D.; Papadimitriou, K.; Alexandraki, V.; Tsirvouli, E.; Chakim, Z.; Ghazal, A.; Mortensen, K.; Yaghmur, A.; Salentinig, S.; Papadimitriou, V.; et al. Microemulsions as potential carriers of nisin: Effect of composition on structure and efficacy. Langmuir 2016, 32, 8988–8998. [Google Scholar] [CrossRef] [PubMed]
- Guo, H.; Yang, W.; Lei, B.; Zhao, F.; Guo, L.; Qian, J. Synergistic antimicrobial effect of nisin-octanoic acid nanoemulsions against E. coli and S. aureus. Arch. Microbiol. 2023, 205, 203. [Google Scholar] [CrossRef]
- Maté, J.; Periago, P.M.; Palop, A. Combined effect of a nanoemulsion of D-limonene and nisin on Listeria monocytogenes growth and viability in culture media and foods. Food Sci. Technol. Int. 2016, 22, 146–152. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Vriesekoop, F.; Yuan, Q.; Liang, H. Effects of nisin on the antimicrobial activity of d-limonene and its nanoemulsion. Food Chem. 2014, 150, 307–312. [Google Scholar] [CrossRef]
- Jiang, Y.; Ma, D.; Ji, T.; Sameen, D.E.; Ahmed, S.; Li, S.; Liu, Y. Long-Term antibacterial effect of electrospun polyvinyl alcohol/polyacrylate sodium nanofiber containing nisin-loaded nanoparticles. Nanomaterials 2020, 10, 1803. [Google Scholar] [CrossRef]
- Liu, Q.; Zhang, M.; Bhandari, B.; Xu, J.; Yang, C. Effects of nanoemulsion-based active coatings with composite mixture of star anise essential oil, polylysine, and nisin on the quality and shelf life of ready-to-eat Yao meat products. Food Control 2020, 107, 106771. [Google Scholar] [CrossRef]
- Lu, P.; Zhao, H.; Zhang, M.; Bi, X.; Ge, X.; Wu, M. Thermal insulation and antibacterial foam templated from bagasse nanocellulose/nisin complex stabilized Pickering emulsion. Colloids Surf. B Biointerfaces 2022, 220, 112881. [Google Scholar] [CrossRef] [PubMed]
- Sarkar, P.; Bhunia, A.K.; Yao, Y. Emulsion stabilized with starch octenyl succinate prolongs nisin activity against Listeria monocytogenes in a cantaloupe juice model. J. Food Sci. 2016, 81, M2982–M2987. [Google Scholar] [CrossRef] [PubMed]
- Sadiq, S.; Imran, M.; Habib, H.; Shabbir, S.; Ihsan, A.; Zafar, Y.; Hafeez, F.Y. Potential of monolaurin based food-grade nano-micelles loaded with nisin Z for synergistic antimicrobial action against Staphylococcus aureus. LWT—Food Sci. Technol. 2016, 71, 227–233. [Google Scholar] [CrossRef]
- Sarkar, P.; Bhunia, A.K.; Yao, Y. Nisin Adsorption in colloidal systems formed with phytoglycogen octenyl succinate. Food Biophys. 2016, 11, 311–318. [Google Scholar] [CrossRef]
- Chen, Y.; Duan, Y.; Zhao, H.; Liu, K.; Liu, Y.; Wu, M.; Lu, P. Preparation of bio-based foams with a uniform pore structure by nanocellulose/nisin/waterborne-polyurethane-stabilized Pickering emulsion. Polymers 2022, 14, 5159. [Google Scholar] [CrossRef] [PubMed]
- Bouaziz, Z.; Djebbi, M.; Soussan, L.; Janot, J.; Ben Haj Amara, A.; Balme, S. Adsorption of nisin into layered double hydroxide nanohybrids and in-vitro controlled release. Mater. Sci. Eng. C 2017, 76, 673–683. [Google Scholar] [CrossRef]
- Chen, H.; Davidson, P.M.; Zhong, Q. Antimicrobial properties of nisin after glycation with lactose, maltodextrin and dextran and the thyme oil emulsions prepared thereof. Int. J. Food Microbiol. 2014, 191, 75–81. [Google Scholar] [CrossRef]
- Yin, W.; Wang, Y.; Liu, L.; He, J. Biofilms: The microbial “protective clothing” in extreme environments. Int. J. Mol. Sci. 2019, 20, 3423. [Google Scholar] [CrossRef]
- Hossain, M.I.; Rahaman Mizan, M.F.; Toushik, S.H.; Roy, P.K.; Jahid, I.K.; Park, S.H.; Ha, S.-D. Antibiofilm effect of nisin alone and combined with food-grade oil components (thymol and eugenol) against Listeria monocytogenes cocktail culture on food and food-contact surfaces. Food Control 2022, 135, 108796. [Google Scholar] [CrossRef]
- Settanni, L.; Palazzolo, E.; Guarrasi, V.; Aleo, A.; Mammina, C.; Moschetti, G.; Germanà, M.A. Inhibition of foodborne pathogen bacteria by essential oils extracted from citrus fruits cultivated in Sicily. Food Control 2012, 26, 326–330. [Google Scholar] [CrossRef]
- Li, P.-H.; Chiang, B.-H. Process optimization and stability of d-limonene-in-water nanoemulsions prepared by ultrasonic emulsification using response surface methodology. Ultrason. Sonochem. 2012, 19, 192–197. [Google Scholar] [CrossRef] [PubMed]
- Giannopoulou, D.; Lampropoulou, A.; Maragou, M.; Koliadima, A. Exploring the influence of different vegetable oils on the stability of nanoemulsions in the presence and absence of nisin and limonene. J. Chem. Technol. Biotechnol. 2024, 100, 645–653. [Google Scholar] [CrossRef]
- Pagnossa, J.; Rocchetti, G.; de Abreu Martins, H.H.; Pereira Bezerra, J.D.; El-Saber Batiha, G.; El-Masry, E.A.; Cocconcelli, P.S.; Santos, C.; Lucini, L.; Hilsdorf Piccoli, R. Morphological and metabolomics impact of sublethal doses of natural compounds and its nanoemulsions in Bacillus cereus. Food Res. Int. 2021, 149, 110658. [Google Scholar] [CrossRef] [PubMed]
- Agler, M.T.; Werner, J.J.; Iten, L.B.; Dekker, A.; Cotta, M.A.; Dien, B.S.; Angenent, L.T. Shaping reactor microbiomes to produce the fuel precursor n-butyrate from pretreated cellulosic hydrolysates. Environ. Sci. Technol. 2012, 46, 10229–10238. [Google Scholar] [CrossRef]
- Scheffler, S.L.; Huang, L.; Bi, L.; Yao, Y. In vitro digestibility and emulsification properties of phytoglycogen octenyl succinate. J. Agric. Food Chem. 2010, 58, 5140–5146. [Google Scholar] [CrossRef]
- Altuna, L.; Herrera, M.L.; Foresti, M.L. Synthesis and characterization of octenyl succinic anhydride modified starches for food applications. A review of recent literature. Food Hydrocoll. 2018, 80, 97–110. [Google Scholar] [CrossRef]
- Sarkar, P.; Bhunia, A.K.; Yao, Y. Impact of starch-based emulsions on the antibacterial efficacies of nisin and thymol in cantaloupe juice. Food Chem. 2017, 217, 155–162. [Google Scholar] [CrossRef]
- Luo, S.; Chen, J.; Zeng, Y.; Dai, J.; Li, S.; Yan, J.; Liu, Y. Effect of water-in-oil-in-water (W/O/W) double emulsions to encapsulate nisin on the quality and storage stability of fresh noodles. Food Chem. X 2022, 15, 100378. [Google Scholar] [CrossRef]
- Hughes, N.E.; Marangoni, A.G.; Wright, A.J.; Rogers, M.A.; Rush, J.W.E. Potential food applications of edible oil organogels. Trends Food Sci. Technol. 2009, 20, 470–480. [Google Scholar] [CrossRef]
- Kaushik, I. Organogelation: It’s Food Application. MOJ Food Process Technol. 2017, 4, 66–72. [Google Scholar] [CrossRef]
- Dickinson, E. Emulsion gels: The structuring of soft solids with protein-stabilized oil droplets. Food Hydrocoll. 2012, 28, 224–241. [Google Scholar] [CrossRef]
- Bei, W.; Zhou, Y.; Xing, X.; Zahi, M.R.; Li, Y.; Yuan, Q.; Liang, H. Organogel-nanoemulsion containing nisin and D-limonene and its antimicrobial activity. Front. Microbiol. 2015, 6, 1010. [Google Scholar] [CrossRef]
- Ji, S.; Lu, J.; Liu, Z.; Srivastava, D.; Song, A.; Liu, Y.; Lee, I. Dynamic encapsulation of hydrophilic nisin in hydrophobic poly (lactic acid) particles with controlled morphology by a single emulsion process. J. Colloid. Interf. Sci. 2014, 423, 85–93. [Google Scholar] [CrossRef]
- Sangcharoen, N.; Klaypradit, W.; Wilaipun, P. Antimicrobial activity of microencapsulated nisin with ascorbic acid and ethylenediaminetetraacetic acid prepared using double emulsion and freeze-drying technique against Salmonella Enteritidis ATCC 13076 in culture broth and minced fish. Agr. Nat. Resour. 2023, 57, 65–76. [Google Scholar] [CrossRef]
- Calderón-Oliver, M.; Pedroza-Islas, R.; Escalona-Buendía, H.B.; Pedraza-Chaverri, J.; Ponce-Alquicira, E. Comparative study of the microencapsulation by complex coacervation of nisin in combination with an avocado antioxidant extract. Food Hydrocoll. 2017, 62, 49–57. [Google Scholar] [CrossRef]
- Pinilla, C.M.B.; Isaía, H.A.; Brandelli, A. Development and characterization of innovative polymeric oil-core nanocarriers for nisin delivery. Lett. Appl. NanoBioSci. 2022, 12, 18. [Google Scholar] [CrossRef]
- Tang, T.; Chen, Y.; Zhao, Z.; Bai, Q.; Leisner, J.J.; Liu, T. Nisin-loaded chitosan/sodium alginate microspheres enhance the antimicrobial efficacy of nisin against Staphylococcus aureus. J. Appl. Microbiol. 2024, 135, lxae259. [Google Scholar] [CrossRef]
- Falguera, V.; Quintero, J.P.; Jiménez, A.; Muñoz, J.A.; Ibarz, A. Edible films and coatings: Structures, active functions and trends in their use. Trends Food Sci. Technol. 2011, 22, 292–303. [Google Scholar] [CrossRef]
- Hashemi, M.; Pourmousavi, F.S.; Mohajer, F.; Mohammad, S.; Noori, A.M. Impacts of nano-gelatin coating containing thymol and nisin on chemical quality indices of rainbow trout fillets stored at 4 °C. Jundishapur J. Nat. Pharm. Prod. 2022, 17, e122177. [Google Scholar] [CrossRef]
- Eldib, R.; Khojah, E.; Elhakem, A.; Benajiba, N.; Helal, M. Chitosan, nisin, silicon dioxide nanoparticles coating films effects on blueberry (Vaccinium myrtillus) quality. Coatings 2020, 10, 962. [Google Scholar] [CrossRef]
- Mavalizadeh, A.; Fazlara, A.; Pourmahdi, M.; Bavarsad, N. The effect of separate and combined treatments of nisin, Rosmarinus officinalis essential oil (nanoemulsion and free form) and chitosan coating on the shelf life of refrigerated chicken fillets. J. Food Meas. Charact. 2022, 16, 4497–4513. [Google Scholar] [CrossRef]
- Kazemeini, H.; Azizian, A.; Shahavi, M.H. Effect of chitosan nano-gel/emulsion containing bunium persicum essential oil and nisin as an edible biodegradable coating on Escherichia coli O157:H7 in rainbow trout fillet. J. Water Environ. Nanotechnol. 2019, 4, 343–349. [Google Scholar] [CrossRef]
- Yuan, D.; Hao, X.; Liu, G.; Yue, Y.; Duan, J. A novel composite edible film fabricated by incorporating W/O/W emulsion into a chitosan film to improve the protection of fresh fish meat. Food Chem. 2022, 385, 132647. [Google Scholar] [CrossRef] [PubMed]
- Khajehali, E.; Shekarforoush, S.S.; Nazer, A.H.K.; Hoseinzadeh, S. Effects of nisin and modified atmosphere packaging (MAP) on the quality of emulsion-type sausage. J. Food Qual. 2012, 35, 119–126. [Google Scholar] [CrossRef]
- Khorsandi, A.; Eskandari, M.H.; Aminlari, M.; Shekarforoush, S.S.; Golmakani, M.T. Shelf-life extension of vacuum packed emulsion-type sausage using combination of natural antimicrobials. Food Control 2019, 104, 139–146. [Google Scholar] [CrossRef]
- Guiga, W.; Swesi, Y.; Galland, S.; Peyrol, E.; Degraeve, P.; Sebti, I. Innovative multilayer antimicrobial films made with Nisaplin® or nisin and cellulosic ethers: Physico-chemical characterization, bioactivity and nisin desorption kinetics. Innov. Food Sci. Emerg. Technol. 2010, 11, 352–360. [Google Scholar] [CrossRef]
- Imran, M.; Revol-Junelles, A.-M.; René, N.; Jamshidian, M.; Akhtar, M.J.; Arab-Tehrany, E.; Jacquot, M.; Desobry, S. Microstructure and physico-chemical evaluation of nano-emulsion-based antimicrobial peptides embedded in bioactive packaging films. Food Hydrocoll. 2012, 29, 407–419. [Google Scholar] [CrossRef]
- Ahankari, S.S.; Subhedar, A.R.; Bhadauria, S.S.; Dufresne, A. Nanocellulose in food packaging: A review. Carbohydr. Polym. 2021, 255, 117479. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kapolos, J.; Giannopoulou, D.; Papadimitriou, K.; Koliadima, A. A Comprehensive Review of Emulsion-Based Nisin Delivery Systems for Food Safety. Foods 2025, 14, 1338. https://doi.org/10.3390/foods14081338
Kapolos J, Giannopoulou D, Papadimitriou K, Koliadima A. A Comprehensive Review of Emulsion-Based Nisin Delivery Systems for Food Safety. Foods. 2025; 14(8):1338. https://doi.org/10.3390/foods14081338
Chicago/Turabian StyleKapolos, John, Dimitra Giannopoulou, Konstantinos Papadimitriou, and Athanasia Koliadima. 2025. "A Comprehensive Review of Emulsion-Based Nisin Delivery Systems for Food Safety" Foods 14, no. 8: 1338. https://doi.org/10.3390/foods14081338
APA StyleKapolos, J., Giannopoulou, D., Papadimitriou, K., & Koliadima, A. (2025). A Comprehensive Review of Emulsion-Based Nisin Delivery Systems for Food Safety. Foods, 14(8), 1338. https://doi.org/10.3390/foods14081338