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1 Diffusion mechanisms of solutes in chitosan-based edible films behaviour in liquid and solid media and comparison between macro and nano scale Mafalda A.C. Quintas a,b, Ana I. Bourbon a, Joana T. Martins a, Diogo A.C. Quintas c, Ana C. Pinheiro a, António A. Vicente a a IBB Institute for Biotechnology and Bioengineering, Centre of Biological Engineering, Universidade do Minho, Braga, Portugal (avicente@deb.uminho.pt) b CBQF - Escola Superior de Biotecnologia, Universidade Católica Portuguesa, Porto, Portugal (maquintas@esb.ucp.pt) c Centre for Telecommunications Research, King s College London, London, United Kingdom (diogo.quintas@kcl.ac.uk) ABSTRACT The use of biopolymers for food package and the concept of active and intelligent packaging have received a lot of interest over the last years. The main objective of this work was to investigate the diffusion mechanism of bioactive compounds from chitosan based films into liquid and solid media and to assess behaviour at the nano-scale. For studying the transport to solid medium, Fick s 2 nd law with proper boundary conditions was applied to the release of natamycin to cheese. For describing the behaviour of compound release to liquid media, a model accounting for both Fickian diffusion and polymer relaxation (Linear Superimposition Model - LSM) was applied to data on glycomacropeptide (GMP) release to water and on natamycin release to Phosphate Buffer Solution (PBS). Investigation on transport phenomena on a nanolayered film was carried by applying the LSM model to data on methylene blue released from chitosan/κ-carrageenan nanolayered films to PBS. From the regression results and analysis of model description of the data, it was possible to infer the transport mechanism in the different tested systems. Diffusion from chitosan films to a solid medium followed Fick s behaviour. As for liquid media, transport from chitosan films was a result of Fick s diffusion and molecule release from the matrix disentangled by swelling, i.e. polymer relaxation. Release of compounds from films produced at the nano-scale ranged from anomalous behaviour to almost Fickian behaviour depending on the position where the compound was incorporated. These results support that special attention must be given to transport properties when design packaging for food products. Moreover, reinforce the idea that phenomena at the nano-scale are different from the ones observed in the macro-scale and that further studies are required for transport phenomena in nanomaterials phenomena like erosion and disassembly should be considered in the future. Keywords: mass transport; Fickian diffusion; case II transport; chitosan edible films; nanolayers INTRODUCTION Consumers increasing demand the use of biodegradable polymers from renewable sources for either packaging or drug release systems. A sound understanding of the transport mechanism in these materials is therefore needed. For both pharmaceutical and food packaging applications, the active compound can either be dispersed in the polymer matrix or conjugated/attached with the polymer molecules. Recently, the use of nanostructures such as nanolayered films (i.e. multilayers with thickness control on the nanometer scale [1]) to incorporate drugs or active compounds as been proposed. Pure diffusion, polymer matrix swelling, polymer erosion and degradation are mechanisms that lead to compound release from polymeric devices [2-4]. Depending on both the system (polymer/active compound) and environmental conditions, a different mechanism may prevail. Understanding the different release mechanism may be crucial for product development and its potential applications. The mechanisms associated with mass transport in polymeric systems may be generally classified as of three different types: ideal Fickian diffusion (Brownian transport); Case II transport (polymer relaxation driven) and anomalous behaviour (ranging from Fickian to Case II transport). Fick s 2 nd law has been extensively used for describing this phenomenon in transient problems:
2 C t D C x Depending on initial and boundary conditions, Fick s law can describe a wealth of behaviours, e.g. for polymers immersed in a sufficiently large amount of liquid media, besides concentration gradient, polymer relaxation can also play an important role. As for the case of polymers in contact with solids, relaxation is minimized and thus, concentration gradient becomes the preponderant mechanism and substantially different boundary conditions must be taken into account. At the nano-scale, in particular in the case of nanolayered films, few works can be found on the release mechanisms from polymers. However, research seems to indicate that the release behaviour depends on the permeability and on the disassembly or erosion of the multilayer structure and on other experimental variables [5]. To assess the transport properties of the active compound inside the polymeric matrix, it is important to use mathematical models that describe the physical mechanism without an unnecessary mathematical complexity [6]. This can be done on the basis of experimental data observation and fitting procedures. The main objective of this work was to investigate the diffusion mechanism of bioactive compounds from chitosan-based films into liquid and solid media and to assess behaviour at the nanoscale. For studying the transport to solid medium, data on the release of natamycin to cheese was used. For describing the behaviour of compound release to liquid media, experimental results were obtained on natamycin release to Phosphate Buffer Solution (PBS) and on glycomacropeptide (GMP) to water. Behaviour at the nano-scale was investigated with data on methylene blue (MB) release from chitosan/κ-carrageenan nanolayered films to PBS. MATERIALS & METHODS Procedures Release of natamycin from chitosan films in cheese and PBS results were obtained from published results [7]. To allow comparison of transport mechanisms in the different studied systems in this work, results from natamycin release in cheese were calculated as M active coumpound /g film and used for estimating the diffusion parameters to cheese. Release of glycomacropeptide (GMP) from chitosan films in liquid medium Chitosan films were prepared by dissolving 2 % (w/v) chitosan in a 1 % lactic acid solution with 1% glycerol and.2 % tween 8. GMP was incorporated at 1 % (dry basis). 28 ml of the solution was casted and dried in an oven at 35 ºC, overnight. After drying, films were stored at 2 ºC and 53 % RH. For release experiments, three 2 cm x 2 cm squares were obtained from films and immersed into distilled water (1:1) at 4 ºC, under moderate stirring. The compounds release kinetics was evaluated by monitoring the concentration of the bioactive compounds (by UV-VIS spectroscopy at 23 nm) in the surrounding solution until an equilibrium value was reached. Release of Methylene Blue (MB) from chitosan/k-carrageenan nanolayered films in PBS Support aminolyzed polyethylene terephthalate (PET) pieces were dipped into κ-carrageenan solution for 15 min and subsequently rinsed with distilled water at ph 7. The samples were dried with a flow of nitrogen. The procedure was repeated, this time using chitosan (or MB) as the polyelectrolyte and rinsed with distilled water at ph 3 (or 7). The dipping/ washing/ drying process was repeated until the deposition of 5 layers. The MB was incorporated in the κ-carrageenan/chitosan nanolayered film, in the second, fourth or sixth layer, replacing the corresponding chitosan layer in those positions. Samples were maintained at 2 ºC and 5 % relative humidity (RH) before analysis. The release of MB from the multilayer coating on PET was evaluated by incubating the loaded film in stirred 4 ml of PBS at 37 ºC and ph 2. At preset intervals,.25 ml supernatant was taken and.25 ml of fresh PBS was added to keep the volume of the release medium constant. MB concentration was determined by UV-VIS spectroscopy, at 6 nm. Statistical Procedures Equation 1 was fitted to the experimental data by non-linear regression analysis, using MATLAB (MathWorks, USA). Equation 2 with the modifications mentioned along the text was fitted to data by nonlinear regression analysis, using a package of STATISTICA v 7. (Statsoft. Inc, USA). In both cases, the Levenberg-Marquadt algorithm for the least squares function minimisation was used. The quality of the regressions was evaluated on the basis of the adjusted determination coefficient, R 2 adj; the squared root mean square error, RMSE; and residuals visual inspection of randomness and normality. The
3 precision of the estimated parameters was evaluated by the Standardised Halved Width (SHW %), which was defined as the ratio between the 95 % Standard Error and the value of the estimate. RESULTS & DISCUSSION Release from chitosan films to a solid medium: natamycin to cheese For polymers in contact with foods, swelling of the polymer by water uptake is negligible and the solution of Fick s partial differential equation can be formulated as [8]: 1 [Eq.1] where M is the total mass of compound released from the polymeric matrix per unit of film mass at time t; α is a factor proportional to the volume of solid to volume of polymer ratio and inversely proportional to the partition coefficient of the migrant between polymer and the solid medium; C is the initial concentration of migrant in the film; q is the n th positive root of the equation: tan q α q ; and is the diffusion rate constant (i.e., the diffusion coefficient divided by the quadratic thickness of the film). This model was able to accurately describe the experimental results of natamycin release from the films to cheese (see Figure 1). Estimated parameters were = (g compound /g film ), =.291 and = min -1 ; the calculated RMSE was ,6 model prediction,5,4,3,2, time (hours),5,4,3,2,1-8 8 Figure 1. Fitting of Eq. 1 to experimental data on release of natamycin from chitosan films to a solid matrix cheese. Inset shows the detail of the model fitting to the initial experimental data. Release from chitosan films to liquid media When immersed in liquid media, hydrophilic polymers which is the case of most biopolymers such as chitosan - gradually start to hydrate, causing relaxation of the polymer chain with consequent volume expansion, i.e. swelling [9-11]. To account for both Fickian and case II transport effects on the observed anomalous behaviour in hydrophilic matrices, a linear superimposition of both mechanisms can be used [9] Fick s diffusion can be described by the solution of Fick s second law for a plane sheet with constant boundary conditions (immersed in a large, well agitated, volume of water) [8]. As for polymer relaxation, it is related to the dissipation of stress induced by entry of the penetrant and can be described as a distribution of relaxation times, each following a first order kinetic type equation [9]. Hence, compound release from a hydrophilic polymer slab can be described by:, 1 exp, 1 [Eq.2] here, M, and M, are the contributions of the Fickian and relaxation processes for compound release; k and k are Fickian diffusion and relaxation rate constants, respectively. This general model can then be used to describe Fickian M, and i ; anomalous (M, and i or Case II transport (M, and i.
4 Case study: glycomacropeptide (GMP) release to water In order to evaluate the physical mechanisms involved in GMP release to the liquid medium, the linear superimposition model (Eq. 2) was modified and fitted to the experimental data: Concerning the Fickian part of the model,,. 2, the first term of the Taylor series was used (estimated k values lead to Fourier numbers >.2 (results not shown)). As for the relaxation part of the model,,. 2, it was modified depending on the tested transport mechanism: i) assuming that transport was due only to concentration gradient and chitosan film relaxation had no effect on the transport mechanism (i.e. Fick s behaviour; i = ); ii) transport was due to the sum of concentration gradient and one main type of relaxation of the film (i = 1); and iii) there was a contribution of Fick s diffusion and two different types of polymer relaxation for the release of compounds from the film (i = 2). Figure 2 shows the model description. It can be observed that Fick s behaviour alone (i = ) is unable to describe the experimental data and, hence, the physical mechanism of the transport phenomena involved here. As for anomalous transport considering one main relaxation (i=1) or two relaxations (i=2), both models were able to predict the experimentally observed behaviour (Figure 2). (a),25 (b),14,12,1,8,6,4,2,5,4,3,2,1-2 2 i = i = 1 i = 2,2,15,1,5,4,2-1 1 i = i = 1 i = Figure 2. Linear Superimposition Model description of (a) GMP release from chitosan films to water and (b) Natamycin release from chitosan films to PBS. Inset shows the detail of the model fitting to the initial experimental data. Table 1, shows the results of fitting Eq. 2 to the experimental data (considering one main relaxation, i=1 and two governing relaxations, i=2). Both models presented similar residues distribution, showing compliance with regression analysis underlying assumptions [6] results not shown. From a mathematical point a view, the model considering two relaxations presents a better regression result: adjusted R 2 is 1 % higher compared with the adjusted R 2 for the model with one relaxation and RMSE is reduced by 17 %. However, the quality of estimated parameters evaluated by SHW (%) - worsens for the model with two relaxations. These results, together with the less complexity rule of mathematical modelling, allow concluding that mass transport of GMP through chitosan films in liquid media is essentially governed by anomalous behaviour and that only one main relaxation, influencing transport, occurs in the polymeric matrix Table 1. Fitting of the Linear Superimposition Model (LSM) (modified Eq. 2) to experimental data on release to liquid medium: quality of the regression on the basis of RMSE and R 2 adj; and estimated parameters and evaluation of estimate precision using the SHW % (in parenthesis). Case Study GMP release to water Natamycin release to PBS LSM modification One relaxation (i=1) Two relaxations (i=2) One relaxation (i=1) Two relaxations (i=2) R 2 adj RMSE , (g compound/g film) (14.74%) (27%) (2.66%) (111.45%) (min -1 ) (33.65%) (9375%) (59.42%) 1.35 (215.75%), (g compound/g film) (2.37%) (752%) (14.47%) (25.24%) (min -1 ) (39.17%) (434%) (17.95%) (55.46%), (g compound/g film) na (13.92%) na (33.64%) (min -1 ) na (22.36%) na (73.81%) na not applicable
5 Case study: natamycin release to PBS The approach described above was followed when studying natamycin release to PBS (see Figure 2 and Table 1). Results also allowed concluding that in this case natamycin release was also due to Fick s and relaxation phenomena, and one main relaxation was sufficient to describe the observed behaviour. From the estimated parameters, it can be concluded that both GMP and natamycin are predominantly released via Fick s diffusion (,, ). However, both Fick s transport and relaxation phenomena occur at a faster rate for the case of natamycin release to PBS. This may be related with the nature of the polymer entanglement and bonds established for the two different incorporated compounds, and/or due to different ability of water and PBS to enter the polymeric matrix, affecting swelling. As for release of natamycin for liquid and solid media, beside differences in the observed transport mechanism, estimated diffusion constant rate is higher, as expected, in liquid than in solid media. Release from chitosan nanolayered films in liquid medium: Methylene Blue to Phosphate Buffer Solution Release of compounds to liquid media from nanolayered films is a less studied situation. Literature suggests that, depending on nanolayered films composition and on the released compound, release may follow a Fickian or an anomalous transport behaviour [12]. The Linear Superimposition Model is then a suitable approach to investigate transport mechanism in these systems. On figure 3, we can observe model adequacy to the experimental data. 1,2 (a) 1,2 (b) 1,8,6,4,2,4, ,8,6,4,2,4, ,2 (c) ,8,6,4,2,4, i = i = 1 Figure 3. Linear Superimposition Model description of Methylene Blue release from a nanolayered chitosan/κcarragenan film to PBS. MB assembled on the 2 nd (a), 4 th (b) and 6 th (c) layer. Inset shows the detail of the model fitting to the initial experimental data. These results show that, contrary to what happens in many conventional edible film systems (e.g. the results from the previous section), at the nano-scale and in the tested conditions, the transport mechanism seems to be dependent on the position of the solute related to the outermost layer. For the experiments of release of MB from the nanolaminate s 2 nd layer, polymer relaxation seems to play an important role on transport
6 (Figure 3a) Eq. 2 using i= (Fickian behaviour) could not properly describe experimental data. For release experiments of MB from the 4 th layer, polymer relaxation is still important to describe the observed phenomenon (Figure 3b) nevertheless, Eq. 2 using i= slightly better described the experimental results, comparing with experiments on 2 nd layer. Release from the 6 th layer position also shows a better description if anomalous transport is considered. However, it is much closer to be predominately driven by a concentration gradient with no evidence of significant polymer reconfiguration once in contact with a liquid medium. Mathematically, Eq. 2 using i = 1 was always the best model for data description. However, due to high covariance and correlation, parameters were estimated with lower precision (results not shown). These results may indicate that at the nano-scale different phenomena occur and more studies are need. One should consider that other factors, such as the disassembly or erosion of the multilayer structure, are not accounted for in the Linear Superimposition Model and may be crucial in order to fully understand the mechanisms involved in this phenomenon at the nano-scale. CONCLUSION The results from this study allowed verifying different transport mechanisms in chitosan films. When in contact with solid medium, release of natamycin was mainly governed by Fick s diffusion, while when immersed into a liquid, polymer disentanglement occurred due to swelling. In this case, diffusion was governed by anomalous behaviour and only one main relaxation, influencing transport, occurs in the polymeric matrix. The same behaviour was found for GMP release to water. These results are important for the design of active packaging systems for food products. The results of fitting the Linear Superimposition Model to release of methylene blue from a chitosan/κcarrageenan nanolayered film suggest that a range of mechanisms from anomalous behaviour to almost Fickian behaviour may occur, depending on the layer where MB was incorporated. These results support that transport mechanisms at the nano-scale must be investigated and phenomena like erosion and disassembly should be considered, contrary to what is commonly observed at the macro-scale. This work allowed initial conclusions on the release mechanisms involved at nano-scale, which is of the utmost importance for the application of the nanolayered systems in food products, as a strategy for shelf-life extension. REFERENCES [1] Decher, G., 23. Polyelectrolyte multilayers, an overview, in Multilayer thin films - sequential assembly of nanocomposite materials, Decher, G.&Schlenoff, J.B., Editors. Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim. p [2] Faisant, N., Siepmann, J. & Benoit, J.P., 22. Plga-based microparticles: Elucidation of mechanisms and a new, simple mathematical model quantifying drug release. European Journal of Pharmaceutical Sciences. 15(4), [3] Jain, R.A., 2. The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (plga) devices. Biomaterials. 21(23), [4] Polakovic, M., Görner, T., Gref, R. & Dellacherie, E., Lidocaine loaded biodegradable nanospheres: Ii. Modelling of drug release. Journal of Controlled Release. 6(2-3), [5] Jiang, B. & Li, B., 29. Tunable drug loading and release from polypeptide multilayer nanofilms. International Journal of Nanomedicine. 4, [6] Bates, D. & Watts, D., 1988.Non-linear regression analysis and its applications. New York: John Wiley & Sons. [7] Fajardo, P., Martins, J.T., Fuciños, C., Pastrana, L., Teixeira, J.A. & Vicente, A.A., 21. Evaluation of a chitosanbased edible film as carrier of natamycin to improve the storability of saloio cheese. Journal of Food Engineering. 11(4), [8] Crank, J., 1975.The mathematics of diffusion. 2 ed. Oxford: Clarendon Press. [9] Berens, A.R. & Hopfenberg, H.B., Diffusion and relaxation in glassy polymer powders.2. Separation of diffusion and relaxation parameters. Polymer. 19(5), [1] Flores, S., Conte, A., Campos, C., Gerschenson, L. & Del Nobile, M., 27. Mass transport properties of tapiocabased active edible films. Journal of Food Engineering. 81(3), [11] Siepmann, J. & Peppas, N.A., 21. Modeling of drug release from delivery systems based on hydroxypropyl methylcellulose (hpmc). Advanced Drug Delivery Reviews. 48(2-3), [12] Wang, X., Hu, X., Daley, A., Rabotyagova, O., Cebe, P. & Kaplan, D.L., 27. Nanolayer biomaterial coatings of silk fibroin for controlled release. Journal of Controlled Release. 121(3),
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