Release of natamycin from alginate and pectin films intended for food packaging
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1 Release of natamycin from alginate and pectin films intended for food packaging Andréa Cristiane Krause Bierhalz a, Mariana Altenhofen da Silva a, Theo Guenter Kieckbusch a a School of Chemical Engineering, University of Campinas, Campinas, Brazil (theo@feq.unicamp.br) ABSTRACT Packages with antimicrobial activity provide a promising form of active packaging systems applicable in food processing. Polysaccharides, especially alginate and pectin, are good candidates to be used in active films since they show excellent functional properties and are biodegradable. In this study, single and composite films based on alginate and pectin containing natamycin as active agent were prepared and the release behavior in water and the diffusion coefficients were evaluated. The influence of natamycin on opacity, soluble matter in water and mechanical properties of the films were also investigated. Diffusion coefficients were determined using a solution to Fick s Law for a plane sheet and the mechanism involved in the diffusional process was investigated using the Power Law Model. Addition of natamycin promoted an increase in soluble matter in water and opacity and decreased the tensile strength when compared to films without the added anti-microbial agent. The natamycin mass released by immersion of the film in water fitted well to Fick s second law diffusional model, with effective diffusivity values ranging from (single pectin films) to cm /s (single alginate films). The values of the diffusional exponents ranged between 0.5 and 1.0, suggesting that the transport process had non-fickian (anomalous) characteristics and a solvent diffusion rate of the same order of magnitude as the polymer relaxation. The single alginate films exhibit more suitable attributes for use in packaging than the single pectin and composite films, indicating a greater potential for use as systems for release of active substances. Keywords: active film; alginate; pectin; natamycin; diffusion coefficient INTRODUCTION The increasing demand for safer and minimally processed food products has intensified the research on antimicrobial packaging. This innovative concept of packaging can prevent the product s deterioration, extending the shelf life and maintaining the sensorial attributes and safety of several food products [1]. Biodegradable films prepared from polysaccharide materials, such as algintate and pectin can be used to incorporate antimicrobials agents, delivering them to the food surfaces, where deterioration by microbial growth often begins. Alginates are hydrophilic polysaccharides derived from brown algae known as Phaeophyceae Alginates are composed of (1,4)-linked β-d-mannuronate (M) and α-l-guluronate (G) units, which are present in the linear macromolecule as homopolymeric blocks (poly-m and poly-g), together with blocks in alternating sequence (MG) []. Pectin is the main component of the citrus processing by-products and one of the most widely studied ionic polysaccharides with useful and versatile properties in many applications. The basic chemical structure of pectin is a linear polymer of D-galacturonic acid units with their methyl esters connected through α-(1,4)-glycosidic bonds [3]. According to their degree of methylation, pectins are divided into two categories: low-methoxyl pectins (LMP) and high methoxyl pectins (HMP), with a degree of methylation respectively lower and higher than 50%. The degree of methylation has a decisive effect on the mechanisms of gelation [4]. The extensive use of these two polymers arises from their ability to form gels in the presence of divalent cations such as calcium ions []. The more commonly antimicrobials used to preserve food are organic acids such as benzoic and sorbic acids, bacteriocins such as nisin and some plant extracts [5]. Natamycin is a natural antifungal agent produced during fermentation by the bacterium Streptomyces natelensis and is widely used in the food industry for the prevention of mold contamination of meats, cheese and fruits [6]. Several studies have been done on the release of antimicrobials incorporated into different packaging [7, 8, 9, 10]. Since the efficiency of antimicrobial films is based on the diffusion of active substances from the polymeric matrix to the food, the knowledge of the diffusivity of these compounds is a determinant factor in the development of an antimicrobial food packaging system [8]. A slower release and, therefore, a lower diffusion coefficient is desirable in this application to maintain a critical surface concentration of preservative [10].
2 The physical and chemical properties of the film are also important for packaging system efficiency. Addition of antimicrobial agents may cause changes in the polymeric structure of the film, affecting its mechanical properties and effectiveness as a barrier [11,1] Thus, possible interactions between antimicrobial agents and biopolymers should be considered in the development of active packaging. In this work, single and composite films based on alginate and pectin containing natamycin as active agent were prepared and the release behavior in water and the diffusion coefficients were evaluated. The influence of natamycin on thickness, opacity, soluble matter in water and mechanical properties of the films were also investigated. MATERIALS & METHODS Materials Medium viscosity sodium alginate, extracted from Macrocystis pyrifera seaweed, was purchased from Sigma Aldrich (St. Louis, USA) and amidated low methoxy pectin (LM 101AS) donated by of CPKelco (Limeira, Brazil), were used as biopolymers matrices in the composite and single films. Calcium chloride dihydrate (Merck, Darmstadt, Germany) was used as crosslinking agent and glycerol (Synth, Diadema, Brazil) as plasticizer. Natamycin (Natamax ), kindly donated by Danisco (São Paulo, Brazil), was used as antimicrobial agent. Film preparation Alginate, pectin and alginate/pectin (1:1) films were made by casting in a two-stage crosslinking procedure. In the first stage, a film forming solution of biopolymer (1.5 g/100 ml) was prepared in 400 ml distilled water already containing 0.6 g glycerol/g biopolymer at room temperature. The solution was mechanically stirred at 900 rpm (Tecnal, TE-139, Piracicaba, Brazil) for about 1 h to ensure homogeneity. Afterwards, the temperature of the system was raised to 70ºC and a dilute aqueous calcium chloride solution (30 ml) was slowly added to the biopolymer solution at a flow rate of 1 ml/min delivered by a peristaltic pump (Masterflex C/L, model , Vernon Hills, USA) until a total amount of 0.05 g CaCl.H O/g biopolymers was transferred. Aliquots of the solution (50 ml) were poured into square plaxiglass frames (5 cm ) and dried in a convection oven (Fanem, model 099EV, Guarulhos, Brazil) at 40ºC for about 0 h. After detaching the resulting film from the support, the crosslinking was complemented in a second stage contact, by total immersion of the films in 50 ml of an aqueous calcium chloride solution (5% w/v) containing glycerol (3% v/v) for 0 min. The excess surface liquid was removed and the films were dried in a ventilated ambient for about 5 h, at room temperature. All films were conditioned at room temperature and 5% relative humidity inside desiccators for 3 days before submission to physical characterization. The active films were prepared as described previously using 4g natamycin/100g alginate added to the polymeric solution containing calcium chloride (first stage). The system was further stirred for another 10 minutes before casting. Film thickness (δ) The film thickness was controlled by pouring a constant mass (50 g) of the film forming solution over the support. Digital micrometer (Mitutoyo, MDC-5S, Naulcapan de Juárez, Mexico) was used to measure the thickness of conditioned films. Ten measurements were taken at random positions. Soluble matter in water (S w ) The soluble matter in water of the films was measured as proposed by Irissin-Mangata et al. [13]. The moisture weight fraction, ω, of the film was gravimetrically determined in a vacuum oven (Lab-Line, Squaroid, USA) at 105ºC for 4 h. Disks cut from the same film, were weighed and immersed in 50 ml of distilled water using a 50 ml beaker maintained under mild agitation (150 rpm) at 5ºC for 4 h (Shaker Bath Orbit, Lab-Line, USA). The final dry matter of the sample was determined in the same vacuum oven (105ºC/4 h). The fractional solubilized matter (S w ) was calculated as a function of the initial dry matter. Mechanical properties Tensile strength (TS) and elongation at break (TE) of the preconditioned films were determined at room temperature using a TA.XT (Stable Microsystems SMD, Surrey, UK) according to ASTM standard method D88 [14]. Films were cut into strips (10 x.54 cm) and mounted between the tensile grips of the instrument. The initial grip spacing and cross-head speed were set at 5 cm and 0.1 cm/s, respectively. A
3 microcomputer was used to record the stress strain curves. The tensile strength was expressed as the maximum force at break per initial transversal area of the film and the elongation as a percentage of the original length. Opacity (O p ) The opacity of the films was determined in triplicate using a Colorquest II colorimeter (Hunterlab, Virginia, USA) operating in the transmittance mode according to Hunterlab method [15]. Opacity was calculated by the equipment software, as the relationship among the opacity of each sample over the black standard and the opacity of each sample over the white standard. Natamycin migration test Square film samples (4 cm ) were immersed in a beaker containing 5 ml of distilled water under gentle agitation (150 rpm) in a shaker (Shaker Bath Orbit, Lab-Line, USA) at a temperature of 5 C. After a predetermined period of time, the film was quickly transferred to a second water container. This procedure was repeated from one beaker to another until no further release of natamycin could be detected. The natamicyn concentration in the beakers was determined with UV/VIS spectrophotometer (HP, model 8453, USA) over a wave length range of 90 to 350 nm. The natamycin concentration was obtained by measuring the amplitude of the peak at 317 nm. The accumulated mass of natamycin released, M t, was calculated and plotted as M t /M as a function of time, where M t /M is the fractional natamycin release. The mean film thickness was determined before and after each experiment. Diffusion coefficient determination Diffusion coefficients were determined from the data obtained using a relationship derived from the solution to Fick s Law for a flat plate [16]. Under the conditions of the experiments, and assuming a constant total film thickness, δ, the following equation (Eq. 1) can be adapted for the fractional natamycin release. π ( ) = Mt 8 1 D 1 exp n + 1 t (1) M π n= 0 (n + 1) δ where D is the average effective diffusivity of natamycin, assumed constant. For short contact times, when less than 60% of the solute mass is liberated, a simplified solution of Fick s Second Law can be used (Eq. ): M t M = 4 Dt δ π () Polymeric matrices are prone to undergo structure relaxation under the influence of the penetrating solvent or solute molecules and anomalous transport mechanisms can prevail for some situations. A common way to investigate the mechanism involved in the diffusion process for a planar system is by fitting the early portion of the release curve (M t /M <0.60) to the following well-known Power Law Model (Eq. 3) [16]. M = M t kt n (3) where k is a kinetic constant, t is the release time and n is the diffusional exponent characteristic of the release mechanism. A value of n=0.5 confirms that Fickian (Case I) diffusion is observed and the release rate depends on t 0.5. A value of n=1 indicates Case II transport and the release rate is directly proportional to time. For values of 0.5<n<1.0, anomalous (non-fickian) transport is the predominating mechanism [17]. Statistical Analysis Analysis of Variance and Tukey Test were used to determine statistically significant differences (p<0.05) among averages, using the Software Statistica V RESULTS & DISCUSSION Since the incorporation of antimicrobials might influence the mechanical and barrier properties of the packaging, active films were submitted to the physical characterization procedures and the results compared to the values obtained for the natamycin-free film (control film). The values of thickness,
4 opacity, mechanical properties and soluble matter in water of single and composites alginate/pectin films are shown in Table 1. Table 1. Thickness (δ), soluble matter in water (S w ), tensile strength (TS), elongation at break (TE) and opacity (O p ) of films without natamycin (control films) and with natamycin (active films). Film δ (µm)** S w (%)* TS (MPa)** TE (%)** O p (%)* Pectin Control films 19 (0.9) c 4.53 (0.54) b (5.5) d 4.66 (0.44) b 4.55 (0.06) f Active films 0 (1.1) c 45.5 (1.79) a (5.93) e 4.75 (0.37) b (0.89) b Pec/Alg Control films 5 (3.1) b 16.9 (1.97) d (3.43) b 4.68 (0.53) b 7.85 (0.48) e Active films 5 (1.9) b 5.66 (4.76) b (7.08) c 4.81 (0.45) b 57.0 (0.86) a Alginate Control films 30 (.) a (1.) c 1.51 (3.7) a 6.59 (0.7) a 13.1 (0.06) d Active films 30 (.1) a (1.98) cd (4.99) b 6.84 (1.09) a (0.39) c Average (standard deviation) of three (*) and ten (**) experimental determinations. Average with the same letter, in the same column, indicate no significant difference (p <0.05). The results indicate that the thickness of the films did not significantly change with the presence of natamycin. However, the results also show that there was a significant increase of thickness when alginate was present in the formulation. This behavior may be associated to the differences of molecular mass of the biopolymers. According to Sriamornsak & Kennedy [3], the pectin films tend to be thinner than the alginate films because they achieve a more compact molecular arrangement, fact attributed to the lower molecular mass of the pectin in relation to the alginate. These authors obtained pectin films that were half as thick as the pure alginate films. The addition of the antimicrobial agent caused a great increase in the soluble matter in water (S w ) of both pectin and composite films, approximately 85% and 50%, respectively. This behavior may have been attributed to the release of natamycin while the films remained immersed in water under agitation during the analysis. This amount released was erroneously accounted as loss in film mass. The lower compatibility of natamycin with pectin might also have caused difficulties in crosslinking with calcium ions. When crosslinking is deficient, the diffusion of water through the chains is easier. Zactiti & Kieckbusch [8] produced alginate films and observed that the solubilized mass doubled after addition of the antimicrobial potassium sorbate. These authors attributed this behavior to the loss of the antimicrobial during the solubility tests in water since 95% of the sorbate release took place in the first 4 minutes of contact with water. The incorporation of natamycin also caused a significant reduction (p < 0.05) in the tensile strength (TS) compared to the control films. On the other hand, addition of natamycin in films did not affect the elongation at break (TE). Reduction in tensile strength may be attributed to modifications in the polymeric structure. According to Han [1], the loss of mechanical integrity may be caused by an excess of antimicrobial agent that cannot be properly incorporated to the biopolymer. Several studies on active films have reported a decrease in tensile strength with the addition of the antimicrobial agent, for example Pires et al. [1], who analyzed cellulose films with natamycin and Cha & Chinnan [18], who studied alginate films with nisin. Pranoto et al. [11] also evaluated the effects of added potassium sorbate or nisin on the mechanical properties of chitosan films and verified that there was a decrease in tensile strength with both agents. The results in Table 1 also show that tensile strength of the alginate films was significantly higher than the respective composite film and pectin film. According to Fang et al. [], alginates have a more linear and organized chain that allows a more efficient connection to the calcium ions. This more energetic crosslinking of the alginate provides an increase of the cohesive forces between the chains. Da Silva et al. [19] reported that alginate films have tensile strength twice as large as the pectin films. This behavior also was observed by Sriamornsak & Kennedy [3], that claimed alginate films were stronger and more flexible. Transparency is an important property of films intended for food packaging as its aspect could influence consumer acceptance of the product. The results in Table 1 indicate that the incorporation of natamycin into films caused an increase in the opacity of all film formulations. This may be related to the chemical structure of natamycin, which simultaneously includes a hydrophilic and a hydrophobic fraction in its molecule, giving it low water solubility. Yang & Paulson [0] have reported an increase in film opacity due to the addition of hydrophobic substances.
5 Diffusion coefficients of natamycin from single and composite films were estimated by adjusting the experimental points to Equation 1 using 15 terms in the summation. Initial experimental data (M t /M < 0.6) were also adjusted to the diffusion model for short contact times (semi-infinite solid model) using Equation. These values, the correlation coefficient as well the time of equilibrium found for each situation studied are shown in Table. Table. Time to equilibration (t), diffusion coefficients (D), diffusion exponent (n) and diffusional constant (k) of pectin, alginate and composite films containing natamycin Film t (h) D 1 (cm /s) R 1 D (cm /s) R n k (s -1 ) Pectin Pec/Alg Alginate Diffusion coefficient and correlation coefficient found from Equation 1. Diffusion coefficient and correlation coefficient found from Equation. Comparing the times to equilibration results (t), it can be observed that natamycin release was slower in single alginate films. Pectin films reached equilibrium in approximately 30 hours, while this period increased to 70 hours for composite films and over 800 hours for alginate films. These results reinforce the hypothesis that natamycin presents higher compatibility with alginate than with pectin. The rapid release of natamycin from pectin films also explains the high soluble matter in water value observed in Table 1. As expected, the diffusivity coefficients decreased significantly when alginate was added to the formulation. The largest difference in results between the two fitting approaches used (D 1 and D ), was observed with the pectin film, which indicates that the diffusion is more influenced by swelling. Bajpai et al. [1] produced alginate and pectin beads crosslinked with calcium and studied the release of potassium nitrate in water. The authors observed that the release rate increased with an increase in the pectin concentration. This behavior was attributed to the higher hydrophilicity of pectin, which causes relaxation of the chains, resulting in faster release of the active agent. The films with higher proportions of alginate also had a higher degree of crosslinking and created difficulties for natamycin mobility. Zactiti & Kieckbusch [8] observed that the diffusivity of potassium sorbate in water decreased when the concentration of calcium used in the crosslinking of alginate films was increased. Although the diffusivity was higher for pectin films, the observed values were low compared to other results on release of antimicrobial agents. For example, values found in the literature for potassium sorbate, lisosyme and sorbic acid diffusivities are in the order of 10-8 cm /s [9,, 3]. Diffusion exponents for the Power Law Model (Equation 3) were obtained by plotting ln (M t /M ) versus ln (t). The diffusional exponent (n) was calculated from the angular coefficients and the diffusional constant (k) was obtained from the linear coefficients of the fitting line. As shown in Table, all formulations presented a diffusional exponent (n) between 0.5 and 1, which are characteristic of anomalous diffusion, a mechanism in which the diffusion rate of the solvent and the relaxation of the polymeric chains are of the same order of magnitude. The deviation from Fickian behavior indicates that the polymer relaxation phenomenon is more prominent and may affect the release of natamycin during the first moments of the process [17]. An anomalous diffusion mechanism was also observed by Zactiti & Kiecbusch [8] for alginate films with potassium sorbate. Flores et al. [4] and Ozdemir and Floros [] also observed deviations from ideal Fickian behavior during release of potassium sorbate from starch and protein films, respectively. CONCLUSION The incorporation of natamycin as an antimicrobial agent affected tensile strength and, particularly, the opacity of active films. When pectin was used as a biopolymer, the results revealed that natamycin was not homogenously incorporated into the structure, which caused its rapid release as well as high water solubility values. Composite films tended to present intermediary properties when compared to both simple films. The diffusion coefficient obtained by adjusting the experimental data to Fick s second law varied from to cm /s. The good compatibility of natamycin with alginate, the low diffusion coefficient and the excellent physical properties indicate that this film has great potential for use in antimicrobial packaging.
6 Acknowledgments The authors acknowledge The State of São Paulo Research Foundation FAPESP for financial support (Proc. 008/5830-9). REFERENCES [1] Han J.H Antimicrobial food packaging. Food Technology, 54(3), 56-65, [] Fang Y., Al-Assaf S., Phillips G.O., Nishinari K., Funami T. & Williams P.A Binding behavior of calcium to polyuronates: Comparison of pectin with alginate. Carbohydrate Polymers, 7(), [3] Sriamornsak P. & Kennedy R.A Swelling and diffusion studies of calcium polysaccharide gels intended for film coating. International Journal of Pharmaceutics, 358(1-), [4] Gigli J., Garnier C. & Piazza L Rheological behaviour of low-methoxyl pectin gels over an extended frequency window. Food Hydrocolloids, 3(5), [5] Limjaroen P., Ryser E., Lockhart H. & Harte B Development of a food packaging coating material with antimicrobial properties. Journal of plastic film and sheeting, 19(), [6] Chen G-Q., Lu F-P. & Du L-X Natamycin production by Streptomyces gilvosporeus based on statistical optimization, Journal of Agricultural and Food Chemistry, 56(13), [7] Ozdemir M. & Floros J.D Analysis and modeling of potassium sorbate diffusion through edible whey protein films, Journal of Food Engineering, 47(), [8] Zactiti E.M. & Kieckbusch T.G Release of potassium sorbate from active films of sodium alginate crosslinked with calcium chloride, Packaging Technology and Science, (6), [9] Buonocore G.G., Del Nobile M.A., Panizza A. & Corbo M.R A general approach to describe the antimicrobial release from highly swellable films intended for food packaging applications, Journal of Controlled Release, 90(1), [10] Franssen L.R., Rumsey T.R. & Krochta J.M Whey protein film composition effects on potassium sorbate and natamycin diffusion, Journal of Food Science, 69(5), [11] Pranoto Y., Salokhe V.M. & Rakshit S.K Physical and antibacterial properties of alginate-based edible film incorporated with garlic oil, Food Research International, 38(3), [1] Pires A.C.S., Soares N.F.F., Andrade N.J., Silva L.H.M., Camilloto G.P. & Bernardes P.C Development and evaluation of active packaging for sliced mozzarela preservation, Packaging Technology and Science, 1(7), [13] Irissin-Mangata J., Bauduin G., Boutevin B. & Gontard N New plasticizers for wheat gluten films, European Polymer Journal, 37(8), [14] ASTM Tensile properties of thin plastic sheeting. Annual Book of ASTM Standards, American Society for Testing and Materials, Philadelphia, D 88. [15] Sobral P.J.A. & Habitante A.M.Q.B Phase transitions of pigskin gelatin, Food Hidrocolloids, 15(4-6), [16] Crank J The Mathematics of Diffusion, ed., Clarendon Press, Oxford. [17] Siepmann J. & Peppas N.A Modeling of drug release from delivery systems based on hydroxypropyl methylcellulose (HPMC), Advanced Drug Delivery Reviews, 48(-3), [18] Cha D.S. & Chinnan M.S Biopolymer-based antimicrobial packaging: A review, Critical Reviews in Food Science and Nutrition, 44(4), [19] Da Silva M.A., Bierhalz A.C.K. & Kieckbusch T.G Alginate and pectin composite films crosslinked with Ca + ions: Effect of the plasticizer concentration, Carbohydrate Polymers, 77(4), [0] Yang L. & Paulson A.T Effects of lipids on mechanical and moisture barrier properties of edible gellan film, Food Research International, 33(7), [1] Bajpai J., Bajpai A.K. & Mishra S Dynamics of controlled release of potassium nitrate from a highly swelling binary biopolymeric blend of alginate and pectin, Journal of Macromolecular Science, 43(1), [] Ozdemir M. & Floros J.D Analysis and modeling of potassium sorbate diffusion through edible whey protein films, Journal of Food Engineering, 47(), [3] Redl A., Gontard N. & Guilbert S Determination of sorbic acid diffusivity in edible wheat gluten and lipid based films, Journal of Food Science, 61(1), [4] Flores S., Conte A., Campos C., Gerschenson L. & Del Nobile M Mass transport properties of tapiocabased active edible films, Journal of Food Engineering, 81(3),
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