Essential Oil-Based Nanoparticles as Antimicrobial Agents in Food: Comparison
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Please note this is a comparison between Version 2 by Lindsay Dong and Version 1 by MICAELA GUIDOTTI TAKEUCHI.

The use of essential oils (EO) loaded with nanoparticles is the most promising alternative to increase food quality and safety. Their association with different nanosystems allows novel developments in the micronutrition, health promotion, and pathogen control fields, preventing the aggravation of bacterial microevolution and combating antibiotic resistance. Benefits to the environment are also provided, as they are biodegradable and biocompatible. 

  • food science
  • nanotechnology
  • essential oils

1. Introduction

The EOs are plant-derived compounds with complex aromatic structures and high volatility. The volatilomes [11][1] are presented as the total fraction of strong-smelling molecules produced in specialized plant cells (oil cells, ducts, or glands) [12][2]. They are secondary plant metabolites, which play essential roles in the dynamics of plants with their habitat through protection against pathogens and attraction of polarizers [13][3]. They can be extracted from all parts of plants (from leaves to roots) by using different methodologies. The presence, yield, and chemotype of EOs are influenced by many climatic and plant nutritional factors, as well as stress conditions. For commercial EO production (where increases in the yield are desirable), breeding and selection programs are implemented as a measure to foster specific compositions [14][4]. The structural profiles of commercial EOs have been previously provided by gas chromatography and mass spectrometry analysis [8,15,16][5][6][7]. In general, their molecular structure reveals two or three major compounds, corresponding to more than 20% of the full molecule, usually responsible for their biological properties [17,18,19][8][9][10].

However, EOs show a set of undesirable physiochemical properties that prevent their widespread use. They are highly volatile, light-sensitive [26][11], can produce off-flavors, modify the color of food products [27][12], interfere with food texture, and have lower bioavailability [28][13]. In this sense, some nanotechnological approaches are currently applied to overcome these disadvantages without affecting the therapeutic properties. The nanoencapsulation of EOs by different nanocarriers (Figure 1), mainly those with affinity for hydrophobic molecules such as liposomes, nanoemulsions, solid lipid nanoparticles (SLN), nanostructured lipid carriers (NLC), polymer nanocapsules, cyclodextrins, and chitosan-based system (CHT), among others, is a promising alternative for advances in the preservation and microbial control (Table 1) of food products [29,30,31][14][15][16]. Moreover, the different nanocarriers designed for food applications have to be biocompatible, biodegradable, scaled up, and classified as GRAS (generally recognized as safe) [28][13], which requires technical evidence of safety [32][17].
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Figure 1. Illustrative chart regarding the use and advantages of different organic nanoparticles loading essential oils (EOs) throughout the food production process. EO: essential oil; SLN: solid lipid nanoparticle; NLC: nanostructured lipid carriers.

2. Production Chain in the Food Industry (FI)

All steps of the food production and processing system (farm to fork) are prone to microbial contamination, with direct consequences to the final consumer, causing different foodborne diseases. Therefore, FIs have a huge challenge in searching new strategies for pathogen control. The misuse of antimicrobials has resulted in a selection of bacteria that are more tolerant and resistant to chemical agents, causing risks to human health, due to ineffective therapeutic efforts [33][18]. In addition, consumers are concerned about the adverse effects of synthetic components used in food [34][19]. Regulatory issues related to banning the use of these compounds in animal production [35][20] are in line with the trend towards consuming foods treated with safe and natural antimicrobials [36][21].
Antimicrobial resistance has been known since the discovery of antibiotics. The continuous and rapid evolution of microorganisms overcome the effect of antimicrobial agents. Therefore, the drug resistance is a major concern, as human and animal health, food production, and environment are interconnected [37][22]. Compared to traditional antimicrobial drugs, EO can reach different microbial targets [38][23], such as binding bacterial proteins and lowering pH [39][24] that improve the therapeutic effect against multidrug-resistant bacteria present in food [40][25], such as Klebsiella pneumoniae, Campylobacter jejuni, Staphylococcus aureus, Pseudomonas aeruginosa, Salmonella spp., Shigella sp., Enterococcus sp., and Escherichia coli [41][26], and can be used from animal production to the finished product.
Food-grade nanoparticulate products are already available on the market and include nano-additives and nano-ingredients made from ω-3 fatty acids, incorporated into yogurts [42][27] and fruit juices [43][28]. They have the function of not only enriching the product, but also promoting the sensory acceptability of fish oil [44][29]. Other products developed by Aquanova® include nanoemulsions loading vitamins. Other nanoencapsulated vitamins (Lypo-Spheric Vitamin, Livon Laboratories, Inc. Company Profile, Henderson, NV, USA) manufactured by LivOn Labs offer protection against their degradation in the gastrointestinal system, increasing the bioavailability [45][30]. There are also some reports related to the NP application for sensory enhancements, to inhibit flavor loss (infused pure cocoa nanoclusters, RBC Life Sciences ® Inc, Irving, TX, USA) [46][31], incorporate natural colorants (β-carotene, curcumin; NutraLease ®, Ma’ale Adumim, Israel) [47][32], and offer nanotechnological advantages, such as Nestlé® patented water-in-oil emulsion (10–500 nm), to facilitate microwave thawing of frozen products [48][33]. The possibilities of applications are wide, including expressive fat reduction (from 16% to 1%) in ice cream production (Unilever ®, London, UK) [49][34] and incorporation of antimicrobial compounds [49][34] in packaging, and in decontamination of industrial equipment [47][32], demonstrating the diversity of application in food matrices and a dynamic approach to food and feed quality assurance [33][18].

3. Nanostructured Delivery Systems (NDSs)

The nanostructured delivery systems (NDSs) are molecularly composed of different biomaterials and are processed as several forms in order to interact specifically with the targets. There are a lot of benefits of the EOs nanoencapsulation approach, such as bioactive protection to the external environment (e.g., products rich in unsaturated lipids can be peroxided over time); sustained release; desirable shelf time; to mask eventual bioactive unpleasant odor and/or flavor; and act as smart packaging with moisture maintenance, protection against pathogens, and monitoring of conditions during distribution [72,81,106][35][36][37]. Different NPs loading EOs have been proposed for pathogen control or incorporated as adjuvants in food-based products [41][26]. Furthermore, nanoencapsulation presents itself as a method to protect against formation of degraded compounds with toxic derivatives, such as the conversion of safrole (4-allyl-1,2-methylene dioxybenzene), derived from plants of the Lauraceae family (including nutmeg and black pepper) with hepatocarcinogenic effects [81,107][36][38].

3.1. Liposomes

Liposomes are spherical vesicles composed of phospholipids spontaneously oriented as lipid bilayers (unilamellar or multilamellar) in aqueous solutions, given by the hydrophobic interactions of nonpolar acyl chains [108][39]. The amphiphilic nature of lipids is currently exploited to encapsulate food ingredients of different polarities, creating an efficient physical barrier system and protecting bioactives from environmental conditions [109][40]. The lipid bilayers allow interaction with the hydrophobic encapsulated compounds, being intrinsically related to NDS stability (fluidity, permeability, and polarity, among others), as well as encapsulation efficiency and sustained release profile [110][41]. In general, the analyzed reports showed that the EO-loaded liposomes provided optimized antimicrobial activity. Sebaaly et al. (2021) developed multilamellar liposomes composed of dipalmitoyl phosphatidylcholine (DPPC) encapsulating EO from Z. tingoassuiba, with a mean diameter of 9.37 ± 4.69 µm [111][42]. The in vitro antimicrobial activity was evaluated by the disc diffusion test. Antimicrobial activity against Staphylococcus aureus, Micrococcus luteus, and Streptococcus mutans, important pathogens related to the food infections, was observed [110][41].

3.2. Nanoemulsions (NEs)

Nanoemulsions (NEs) are stable systems composed of two immiscible phases [112][43], being processed as water-in-oil or oil-in-water, stabilized by amphiphilic surfactant and co-surfactant. They exhibit excellent structural properties, with particle size between 50–250 nm and a monodisperse distribution [113][44]. Food-grade NEs containing bioactive components can be used to develop biodegradable packaging films. Promising results were provided of NEs that prevented foodborne diseases. In this sense, carvacrol-based NE was tested in minimal processes as an alternative to calcium hypochlorite use against Escherichia coli O157:H7 and Salmonella Typhimurium in contaminated broccoli and radish seeds. A system containing 0.4% carvacrol was able to inactivate contamination in low levels (about 2–3 log CFU/g) in radish seeds. The treatment was not effective for broccoli seeds [52][45].

3.3. Solid Lipid Nanoparticles (SLNs)

SLNs emerged in 1991, firstly described by Professors Müller and Gasco, as an alternative to traditional colloidal systems such as liposomes [115,116][46][47]. This system is based on a lipid matrix composed of solid lipid stabilized by a surfactant [30,116][15][47]. SLNs have high affinity to load hydrophobic active into the solid matrix [117][48]. SLNs allow to improve the stability of loaded EOs under various adverse conditions, including food processing, heating, high pressure, drying, UV radiation, and bile salt [118][49]. Therefore, such a system was designed for applications in food distribution because it has interesting advantages to be used in this sector, such as the effective uptake of fat-soluble assets, sustained release profile, and long-term stability [119,120][50][51].

3.4. Nanostructured Lipid Carriers (NLCs)

NLCs are the second generation of lipid nanoparticles, composed of a lipid matrix formed by a blend between solid and liquid lipids in room temperature, stabilized by a surfactant [115][46]. They are also considered to be safe and promising nanocarriers for the delivery of hydrophobic compounds, despite their hydrophilicity (colloid liquid systems), which is paramount for the establishment of water-based foods. Therefore, NLCs have industrial relevance as these nanocarriers also combine specific advantages for food uses, such as the ability to be successfully incorporated into transparent and opaque foods and beverages [115][46]. The encapsulation of EOs by NLCs has been proposed to exhibit higher stability, minimized toxicity, and preserve the therapeutic properties of pristine EOs [124][52]. EO-loaded NLC formulations have been widely described to increase the antimicrobial activity of EOs and protect them against environmental damage conditions (light, hydrolysis, and evaporation, among others) [31,125][16][53].

3.5. Polymer Nanocapsules (NCs)

NCs are NDSs formed by a shell (polymer wall) and core (oil core) counterparts that have interesting physicochemical properties for application in food matrices, such as those derived from aliphatic polyester (ε-caprolactone), which are stable in storage and allow a sustained release of loaded actives. Such core–shell structure brings benefits that include the difficulty of contact with external substances and is better suited to lipophilic foods [128][54]. The encapsulation of EOs by polymer nanocapsules (NC) aims to improve hydrophilicity of insoluble compounds, protection against degradation, prevention of loss of volatile compounds caused by evaporation, and a sustained release. Their antimicrobial activity of NC loading Thymus capitatus EO with high amount of bioactives (43% thymol) was reported [8][5]. The association of polymers and thymol EO has immediate applicability against important pathogens in the FI (S. aureus, L. monocytogenes, B. cereus, S. typhi, S. dysenteriae, and E. coli).

3.6. Cyclodextrins (CDs)

Cyclodextrins (CDs) are cyclic oligosaccharides that have glucose units linked by α-(1,4)-glycosidic bonds, derived from the enzymatic degradation of starch [110][41], mainly by B. macerans [34][19]. They present a cone-shaped morphology with a hydrophobic cavity and 7.9 Å diameter, and are able to form inclusion complexes with low-aqueous-solubility molecules [50][55]. The inclusion complexes formed by CDs and EOs improve the EO solubility and physicochemical stability, providing a sustained release of these compounds [131][56], also acting as physical barrier to protect the EO in procedures such as freezing, thawing, and/or microwaving during food processing [34][19]. In the FI, they are used to improve flavor and sorption of bitter compounds. Recently, CDs have been noticed as constituents of active packaging of edible products [132][57].

3.7. Chitosan-Based Delivery Systems (CHT)

Chitosan (CHT) is a linear cationic polysaccharide formed by (1,4)-amino-deoxy-b-d-glucan chains derived from a deacetylated chitin of crabs and crustaceans, and is biocompatible, biodegradable, and cheap [64][58]. The use of CHT as a drug carrier has additional advantages as an NDS, such as the protection of the selected active, changes in temperature, and sustained release at the site of interest [136][59], given by the electrostatic interactions with anionic biological membranes. As a biopolymer, it can be processed as several forms and is abundant, cheap, and biodegradable [137][60]. CHT application in association with EOs has demonstrated higher antimicrobial activity against foodborne pathogens than biopolymer films and coatings [64][58]. Specifically, it has demonstrated its advantageous use as an NDS in food preservatives, as it allows a sustained release of active ingredients in the production of food films and coatings [64][58]. Its inherent antimicrobial activity has been attributed to the electrostatic forces between the cationic amino groups (NH3) of CHT and the negatively charged residues of the fatty acids located on the bacterial [138][61].

4. Nanopackaging and Smart Control of Food Pathogens

EOs are widely explored for use in food packaging due to their potential antimicrobial activity [98][62]. Antimicrobial packaging is also able to maintain both the nutritional and sensory quality of food, extending its shelf life. Such approach seems to be an effective alternative to the addition of synthetic preservatives in the packages, as it will be in contact with the food products. Therefore, EOs are currently incorporated into the packages, aiming to decrease the maximum population growth rate and/or prolong the lag phase of the target microorganism by contact inactivation. When used in adequate concentrations, in addition to inhibiting foodborne pathogenic bacteria (Listeria, Salmonella, Aeromonas, Clostridium botulinum, Enterobacter, and Staphylococci) and their toxins, EOs can also improve the sensory properties of the food products [144][63]. However, the EOs incorporation in active and smart packaging needs to meet crucial safety requirements. For instance, the slow denaturation of EOs from the packaging material to the food surface allows maintaining a high concentration of EOs over a long period of time when compared to the direct addition of EOs in food, the result of which differs by the rapid diffusion of the bioactive with a consequent reduction in antimicrobial activity [145][64]. The application of nanotechnology in packaging development presents interesting opportunities to exploit the antimicrobial properties of EOs [146][65]. This strategy has been widely explored, mainly because they act as a physical barrier leading to decreased spoilage and improved inhibition of pathogenic microorganism growth [147][66]. Nanofilms composed of a thin layer of polymers, created using layer-by-layer deposition techniques, have potential applications in the field of active food packaging. They have been applied directly on the product, whereas non-edible coatings have a protective function specifically on the packaging. Their applicability also extends to surfaces that are in contact with food during processing or to prevent the formation of biofilms [28][13].

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