Kathleen Oehlke and Ralf Greiner
Abstract
The potential of nanoencapsulation of bioactive compounds is based on overcoming incompatibilities between bioactive compounds and food, increasing the stability of bioactive compounds by their protection from adverse conditions and increasing the bioavailability of bioactive compounds. They can be applied in clear suspensions and provide high kinetic stability which both may be favourable in terms of the later product properties.
Lipid-, protein- or polysaccharide-based engineered nanometer-sized materials (ENM) can be prepared by self-assembly, emulsification, ionic or covalent crosslinking of biopolymers, or comminution of larger materials. Nowadays, combinations of materials and techniques are developed to overcome shortcomings of “first generation” ENM. Actual and perceived risks include the resorption of intact particles and their accumulation in certain organs or tissues and exceedingly high concentrations of bioactive compounds in plasma over long periods of time. Both are serious issues and have to be evaluated on a case-by-case basis, since general conclusions cannot be drawn based on the current literature. While the development of carrier systems as such advances quickly, research towards interactions with the food matrix remains challenging.
Introduction
Engineered nanometer-sized materials (ENM) have gained increasing interest as potential delivery systems for bioactive compounds. At first, their potential was investigated in pharmaceutical research and was then also recognised in food and nutrition research, especially since functional food or neutraceuticals are an important market. While basic mechanisms are similar in both fields, the limitation to food grade materials requires considerable attention and can be challenging in the process of product development. The term ENM is not ultimately defined, but usually includes a size limit of around 100 nm in at least one dimension. This means that ENM include a number of classes such as spherical particles, fibres or films. In addition, at least one new property or functionality is usually mentioned to be distinctive for ENM compared to the bulk material. However, there is no consensus, which new or changed property this could be, i.e. is the improved delivery of an encapsulated compound already a new property? Properties or functionalities are most likely related to the increased surface area of the smaller materials. The term ENM is related to materials that are formed on purpose, but does not include naturally occurring structures of that size range.
The following article will discuss ENM as carrier systems for bioactive compounds in food. The most important methods to prepare food grade ENM will be briefly discussed, before functionalities of ENM will be mentioned. Since research is mostly directed to improve the bioavailability of bioactive compounds, this topic will be discussed in more detail.
The encapsulation of bioactive compounds is usually aimed at:
overcoming incompatibilities between bioactive compounds and food, e.g. due to different hydrophilicities;
increasing the stability of bioactive compounds by their protection from adverse conditions; or
increasing the bioavailability of bioactive compounds by modulating their solubility, bioaccessibility, membrane permeability or stability in the gastro-intestinal tract (GIT).
From a technological point of view ENM may be preferable over larger delivery systems because of:
the fact that the small particles cause less light diffraction so that the suspension is clear;
less sedimentation or creaming of particles or emulsion droplets, respectively; and
changed physico-chemical properties, e.g. the melting point of fat in a solid lipid nanoparticle (SLN) is below that of the bulk material.
Preparation of ENM and Their Properties
Self-assembly
Amphiphilic molecules like surfactants and some proteins tend to associate with each other due to favoured chemical states resulting in the formation of micelles, microemulsions or liposomes. Since this process occurs due to hydrophobic interactions, it does not require much energy input or a special device.
Micelles are relatively simple spherical or rod-like structures while liposomes, which consist of a phospholipid double layer, are more complex. Both types are characterised by regions of different polarity or water content and can therefore solubilise many low molecular weight compounds with high solubilisation capacities. The encapsulation in micelles or liposomes allows the inclusion of lipophilic compounds into aqueous systems. Likewise, the solubilisation of compounds in w/o microemulsions or reversed micelles allows introducing hydrophilic compounds into a lipophilic environment.
Furthermore, emulsifiers can increase the permeability of the intestinal wall thereby acting as sorption promoters for the bioactive compound. This leads to increased absorption rates or even the direct uptake into the lymphoid system. Besides, emulsifier-based ENM and liquid lipid phases lead to a quick release and resorption of the bioactive compound resulting in short Tmax and often high peak concentrations of the bioactive compound. Whether or not this is a critical point would have to be evaluated for each compound.
While the underlying mechanisms of self-assembly result in narrow size ranges, there can be more variation in the achieved particle size with other formation mechanisms. Processing conditions like temperature, contact time, concentrations or pH largely affect the size of the later ENM, so that in some cases ranges of two to three orders of magnitude are possible.
Emulsification
The formation of ENM by emulsification is typically achieved by high pressure homogenisation, micro-fluidisation or by sonication with ultrasound. Depending on the lipid and the emulsifiers the resulting structures are solid lipid nanoparticles (SLN), nanostructured lipid carriers (NLC) or nanoemulsions (NE). Usually they are characterised by a high stability under moderate conditions with respect to pH, temperature or salt concentration. Nanoemulsions are entirely liquid and sometimes do not offer the projected chemical stabilisation of the bioactive compound. This was attempted to be overcome by using a solid lipid matrix, i.e. SLN. However, a completely solid lipid matrix is often connected with low encapsulation rates, expulsion of the bioactive compound during storage or burst release of the encapsulated compound. Furthermore, the crystallisation process and the degree of crystallinity affect the stability of SLN under GIT conditions and the digestibility. Therefore, changes during the storage period are expected to influence the aforementioned properties.
These shortcomings can at least to a certain extent be overcome by the incorporation of a liquid lipid, leading to the formation of a solid/liquid matrix called nanostructured lipid carriers (NLC) (Tamjidi et al. 2013).
The stability in the GIT is an issue for each of these ENM and is affected by the pH, ionic strength and the presence of lipase. A sufficient zeta potential or sufficient sterically stabilising emulsifier layer as well as a suitable combination of emulsifier and lipid phase are required to form lipid based ENM that are stable under GIT conditions, at least as long as lipase is absent. In contrast to the above mentioned emulsifier based or liquid lipid carriers, SLN prolong the release and hence absorption of the bioactive compound and thus lead to longer Tmax.
Ionic Crosslinking
Ionic crosslinking of electrically charged polysaccharide and salt ions results in the formation of a hydrocolloid gel. Under certain conditions the gel takes the form of distinct nanoparticles like sodium tri-polyphosphate (TPP) cross-linked chitosan. The formation occurs spontaneously upon mixing of the components. When adding these gels to a food matrix, the limited stability in the presence of higher pHs and salt concentrations has to be taken into account. A major shortcoming of such structures is the typical burst release of encapsulated bioactive compounds. This might to some extent be overcome by drying the particles, e.g. by spray-drying or freeze-drying. In this case, swelling of the glassy matrix is required before the encapsulant is released. However, it may be difficult to stabilise the particles by drying ensuring a similar particle size after re-hydration. Usually, large amounts of a cryoprotectant will be necessary. On the other hand, polysaccharides offer unique properties like muco-adhesiveness that offers prolonged contact times between the bioactive compound and the intestinal wall. Furthermore, chitosan has been reported to open the tight junctions reversibly which might also result in increased absorption rates. Alternatives for the cross-linking are currently under investigation aiming at higher encapsulation rates and slower release kinetics.
While ionic cross-linking leads to relatively weakly attached structures, the formation of covalent bonds is related to stronger networks. Stronger networks can be favourable in terms of higher encapsulations rates and / or slower release kinetics. Such networks can be achieved by chemical or enzymatic cross-linking. Chitosan networks can, for example, be formed using glutaraldehyde, which, however, is not suitable for food applications. A more suitable example is a network of proteins that are cross-linked by transglutaminase.
Comminution
Comminution of coarse plant or inorganic material can lead to the formation of ENM. This could be agricultural side products like pomace or press-cake that are rich in bioactive compounds or minerals. An increased bioavailability due to the smaller particle size has been reported for lignan glucosides from sesame meal or calcium rich pearl powder. Since no use of food additives is necessary such formulations may meet the consumers’ preference for “clean label” products. A drawback could be the possible presence of unwanted compounds present in the pomace. Furthermore, bioactives could be bound to the plant matrix, so that the bioaccessibility will still be low despite the small particle size. Nevertheless, the comminution usually leads to an improved solubility and would therefore be a good option for BCS class II compounds (see below).
Flame Spray Pyrolysis
Flame spray pyrolysis has been used to prepare ferric phosphate particles yielding improved sensory properties with a bioavailability comparable to that of conventional FeSO4 solutions. The combination with other minerals for improved solubility or the coating with an emulsifier layer for stabilisation against precipitation have further increased the potential of these materials (Zimmermann and Hilty 2011).
These are the most important examples for the preparation of food grade ENM as delivery systems. Others have recently been reviewed by Ezhilarasi et al. (2013). An overview with examples for further reading is given in Table 1.
Table 1. Overview of types of ENM as delivery systems for bioactive compounds
|
Preparation / formation mechanism |
Examples |
Structures |
References |
|
Self assembly |
|||
|
|
|
Zimet et al. (2011), Radhika and Moorthy (2012) |
|
|
 |
McClements (2012) |
|
|
 |
Farhang et al. (2012) |
|
Emulsification |
|||
|
|
   |
Fathi et al. (2012) |
|
Cross-linking of polymers |
|||
|
|
 |
Dudhani and Kosaraju (2010) |
|
|
Chen et al. (2006) |
|
|
Comminution of larger materials |
|||
|
|
Liao et al., (2010),Chen et al. (2008) |
|
|
Flame spray pyrolysis |
|
Rohner et al. (2007) |
ENM to Increase Stability of Bioactive Compounds by Protection from Adverse Conditions
The encapsulation of bioactive compounds can lead to an increased stability of the respective compound both in food matrices and under GIT conditions. This effect is based on the function of the ENM as physical barrier against oxygen, unfavourable pH, free radicals or light. It is not only the type of ENM in general that influences the stability of the encapsulated compounds but also the different components and their combinations. With respect to the stability under GIT conditions, ENM that release the compound slowly and are stable against gastric digestion are of particular interest. However, due to the limitation to food grade compounds, the development of such structures is challenging.
Examples for increased stability in model food matrices are manifold. Several studies have shown that the incorporation of different bioactive compounds in different types of ENM can lead to an increased stability of the compound. However, to maintain a high chemical stability of the bioactive compound the formulation or processing parameters have to be optimised accordingly. The oxidative stability of β-carotene incorporated into SLN, for example, depended largely on their composition and processing parameters. Especially the role of the type of emulsifier used has been demonstrated. The comparison of Tween and lecithin has shown that it might be necessary to find a compromise between particle and bioactive stability (Helgason et al. 2009, Hentschel et al. 2008). Furthermore, the additional encapsulation of α-tocopherol resulted in an increased oxidative stability of β-carotene (Hentschel et al. 2008). On the other hand, LNC used to encapsulate pro-epigallocatechin gallate (pro-EGCG) could not prevent partial deacetylation during storage at ambient temperature (Barras et al. 2009). In contrast, the stability of catechin and epigallocatechin gallate (EGCG) at pH 7.4 was enhanced by the incorporation into chitosan–tripolyphosphate (CS-TPP) nanometre-sized capsules possibly due to (i) an interaction between chitosan and the catechins, and/or (ii) the restricted diffusion of O2 and the surrounding solution through the polymer barrier into the small particle space (Dube et al. 2010). The same reasons may account for the reduction of the degradation of docosahexaenoic acid (DHA) to 5-10 % by the encapsulation into β-lactoglobulin or β-lactoglobulin/pectin complexes compared to 80 % loss of free DHA during 100 h at 40 °C (Zimet and Livney 2009). Interactions with the food matrix were not taken into account in these studies, but should be taken into consideration when applying these systems to food products.
ENM to Increase the Oral Bioavailability of Bioactive Compounds
The low bioavailability of many bioactive compounds is a challenging aspect of the development of functional food. Besides a low chemical stability under GIT conditions, reasons for low bioavailability and plasma concentrations are a low bioaccessibility, low solubility, low membrane permeability or fast clearance rates (first-pass metabolism).
These points are included in the Biopharmaceutical Classification Scheme (BCS) that consists of four classes that are used to classify substances based on their bioavailability. Combinations of these factors are common, so that in total four classes are defined. It is necessary that carrier systems address the problems and carrier / bioactive combinations are carefully designed to overcome them (McClements et al. 2009).
Class I type compounds (e.g. theophyllines) are characterised by a high solubility and high permeability. From a physiological point of view, these compounds have a high bioavailability and would not need a carrier system. However, their chemical stability may be low or their solubility does not fit the food system, so that encapsulation might be required. A limitation of Class II compounds (e.g. CoQ10, tocopherol) is their low solubility, but they possess a sufficient permeability. These compounds are usually lipophilic so that lipid-based ENM can be useful to enhance their bioavailability. Interactions between ENM and bile salt micelles determine their uptake rates. In addition, small particle size (e.g. minerals, nanocrystals) or amorphous states increase the solubility. Class III compounds (e.g. catechins) are sufficiently soluble under GIT conditions, but possess a low permeability. In such cases components of ENM with mucoadhesisve properties may help to increase the bioavailability by increasing the contact time of the bioactive compound with the GIT and / or by opening the tight junctions so that diffusion of bioactive compounds is facilitated. Most difficult to manage are Class IV compounds with low solubility and low permeability (e.g. curcumin, quercetin, soy isoflavonoids). This class requires a carrier that can increase the solubility, e.g. a lipid phase or surfactant rich carrier. Furthermore, a mucoadhesive compound could prolong the contact time with the GIT. Thus, liposomes maybe with a polysaccharide coating could be suitable carrier systems for such compounds.
If a fast clearance rate in the liver by the first-pass metabolism is the reason for too low plasma levels, the direct uptake into the lymphoid system could help to deliver bioactive compounds to the target organ or tissue (see lipid based formulations).
In vivo studies towards the bioavailability of nanoencapsulated bioactive compounds using exclusively food grade materials are scarce in the literature. Currently there are studies about coenzyme Q10, vitamin E, lignan glucosides, vitamin D, steroid glycosides, capsaicin, quercetin, curcumin, calcium rich pearl powder, iron and chromium. Up to 132-fold bioavailability (average 2-10-fold) and up to 39-fold increased plasma levels were reported (Choi et al. 2013, Kakkar et al. 2011). As indicated above, literature study reveals that the effectiveness of delivery systems depends on both the carrier ENM and the bioactive compound. High bioavailability given as area under the curve resulted from high peak concentrations and high or moderate concentrations over an extended period of time due to retarded release. In most cases biokinetic parameters were changed, i.e. the highest peak concentration was reached earlier or was retarded compared to the conventional formulation. A weakness of the majority of currently available literature is that the ENM were administered as an isolated formulation, but not as part of a model food system. Exceptions include yoghurt (Fidler et al. 2004, Ercan and Nehir 2012), infant cereal (Fidler et al. 2004), apple juice (Roe et al. 2009) or gummi bears (Back et al. 2006) as food matrices. There is general consensus that interactions with the food matrix occur and might significantly influence the properties of the ENM. Therefore, conclusions about the usefulness of these ENM as part of the diet or a specific food product should be drawn with care.
Actual or Perceived Risks
The significantly enhanced bioavailability of nanoencapsulated bioactive compounds may lead to high peak concentrations in the blood or organs. Long-term intake of high concentrations that may exceed accepted daily allowance (ADI) values should be avoided. Therefore, added amounts of such delivery systems to possible functional food should be adjusted accordingly (Sauvant et al. 2012).
The possibility of intact ENM to enter the blood cycle and accumulate in organs is a serious concern. It was demonstrated that insoluble inorganic nanoparticles can diffuse into cells and also pass cell layers. However, the fate of soluble and / or digestible nanoparticles in the GIT is not fully understood (Roger et al. 2010, Powell et al. 2010). It is unlikely that intact particles enter the systemic circulation if they are soluble or digestible like food grade materials usually are. However, relatively small changes in the formulation may change the digestibility significantly (e.g. shown for SLN). Interactions between nanomaterials and cell layers will depend on both particle size and surface properties and hence on formulation details of the specific ENM. Therefore, general conclusions about possible risks cannot be drawn. Research in this field becomes even more complex due to the interactions between ENM and the food matrix that may alter properties and hence the potential toxicity of ENM. Much more research is necessary in this field, but is still struggling with the currently available analytical possibilities.
Besides the direct uptake of ENM, the so called “trojan horse effect” as an indirect effect and possible risk should not be neglected. The ability of certain compounds to increase the permeability of cell layers and / or membranes may lead to an increased absorption of undesirable food components like contaminants that would otherwise be eliminated from the body.
Drawbacks, Challenges and New Developments
Currently the focus in research moves to the development of multi-component systems. Examples are liposomes with a chitosan-layer, the use of NLC instead of SLN or protein coated polysaccharide particles. In this way low encapsulation rates or burst release of encapsulants could be improved or avoided, respectively.
Interactions with the food matrix are probably the most difficult task with respect to the development of ENM as ingredients for functional food. Unless the “food” is a clear beverage that otherwise only contains minor amounts of sugars or salts the properties of the ENM are difficult to access in the food matrix. The most prominent example by now is the formation of a protein corona that will significantly change the surface properties of the ENM. Also, in more complex food systems interactions with other structures will occur, e.g. SLN interact with oil droplets in o/w emulsions and may release the bioactive compound into the oil droplets. These are just two examples and it is reasonable to suggest that the type and effect of interactions are very sensitive to the properties of the ENM and the structures in the food matrix.
After ingestion ENM are subject to GIT conditions. Body temperature, different pH and ionic strength regimes, presence of enzymes and bile salts or the presence of mucus affect the properties and stability of ENM and the release of encapsulated bioactives. These points are currently under investigation, but again analytical possibilities are a limiting factor.
Summary and Conclusions
ENM possess high potential as delivery systems for bioactive compounds from different points of view (technological and physiological). Since structures, properties, functionalities and interactions are manifold, general conclusions about the benefits or risks of ENM as delivery systems cannot be drawn. Besides the particle size, surface properties, physical state, composition etc determine whether or not a delivery system can be successfully applied. If a new formulation should be established the following steps are recommended:
Determine limitations of the bioactive compound of interest to be overcome (e.g. solubility, stability, membrane permeability).
Identify which type(s) of ENM would most probably meet the resulting requirements.
Define the food matrix and identify or estimate probable interactions between ENM and the food matrix. If they might interfere with ENM stability or other properties in an unfavourable manner, check alternative ENM from step 2.
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Dr Kathleen Oehlke (e-mail: kathleen.oehlke@mri.bund.de) and Dr Ralf Greiner (e-mail: ralf.greiner@mri.bund.de) are with the Max-Rubner Institut, Department of Food Technology and Bioprocess Engineering, Haid-und-Neu-Str. 9, 76131 Karlsruhe, Germany
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