Edible Films from Methylcellulose and Nanoemulsions of Clove Bud

Article pubs.acs.org/JAFC

Edible Films from Methylcellulose and Nanoemulsions of Clove Bud (Syzygium aromaticum) and Oregano (Origanum vulgare) Essential Oils as Shelf Life Extenders for Sliced Bread Caio G. Otoni,† Silvania F. O. Pontes,§ Eber A. A. Medeiros, and Nilda de F. F. Soares* Laboratory of Food Packaging, Department of Food Technology, Federal University of Viçosa, Av. PH Rolfs s/n, Viçosa, MG 36570-900, Brazil ABSTRACT: Consumers are increasingly demanding foods with lower synthetic preservatives. Plant essential oils are natural compounds with remarkable antimicrobial properties and may be incorporated as emulsions into water-soluble polymers to form antimicrobial films. Coarse emulsions (diameters of 1.3−1.9 μm) and nanoemulsions (diameters of 180−250 nm) of clove bud (Syzygium aromaticum) and oregano (Origanum vulgare) essential oils were produced through low-speed mixing and ultrasonication, respectively. Methylcellulose was added for film-forming purposes. Both essential oils reduced the rigidity and increased the extensibility of the methylcellulose films, effects that were even more pronounced for nanodroplets. Both essential oils lessened the counts of yeasts and molds in sliced bread during 15 days, and droplet size reduction provided a further improvement in antimicrobial properties. Due to increased bioavailability, less preservative content might be used and still deliver the same antimicrobial efficiency if encapsulated in smaller particles. KEYWORDS: active packaging, edible film, nanoemulsion, essential oil, Syzygium aromaticum, Origanum vulgare, sliced bread

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INTRODUCTION As consumers increasingly demand foods with lower synthetic preservative contents but still safe to consume, novel preservation techniques are urged to be developed. Natural antimicrobials such as essential oils from plants have been exploited due to their availability and potential in replacing synthetic preservatives in an effort to match consumers’ requirements for natural products.1−3 Active packaging denotes a means of increasing the shelf life of foodstuffs without changing their fresh-like characteristics as thermal processing usually does,4 because active films,5−7 sachets,8−12 and coatings13−16 may carry and gradually release antimicrobials into food matrices. Essential oils from clove bud (Syzygium aromaticum) and oregano (Origanum vulgare) have been successfully incorporated into edible films and provided antimicrobial activity against several foodborne pathogenic and spoilage microorganisms.17−20 During the incorporation of nonpolar substances such as essential oils into water-soluble polymeric solutions, phase separation is likely to occur because stability is reached when the surface areas of the immiscible constituents are minimum. Such phase separation is undesirable as it leads to nonhomogeneous films. Adding a surfactant stabilizes oil-in-water emulsions and denotes a means of producing uniform films. The essential oil becomes the dispersed phase in the aqueous emulsion that is the film-forming solution. Another way of improving emulsion stability to aggregation and gravitational separation is by reducing droplet diameter to the nanoscale level, producing nanoemulsions,21,22 emulsions with droplets ranging in diameter from 20 to 500 nm.23,24 Nanoemulsions, because of their smaller droplets, also provide improved bioavailability of lipophilic bioactives.22,26 D-Limonene encapsulated in smaller droplets showed improved antimicrobial activities against Lactobacillus delbrueckii, Saccha© XXXX American Chemical Society

romyces cerevisiae, and Escherichia coli in pear and orange juices.27 Smaller droplets also presented higher bactericidal activity against E. coli in lemongrass essential oil−alginate nanoemulsions prepared through microfluidics.28 Pectin/ papaya puree/cinnamaldehyde nanoemulsion edible films were reported to have improved in vitro (i.e., in laboratory media) antimicrobial properties against E. coli, Salmonella enterica, Listeria monocytogenes, and Staphylococcus aureus when droplets were smaller.25 In this work, a disk inhibition test indicated that inhibition halo values were increased by >12 times by decreasing cinnamaldehyde (major constituent of cinnamon essential oil) droplet size from 272 to 41 nm. However, no previous works have reported the effect of droplet size on the in vivo (i.e., in a real food matrix) antimicrobial properties of essential oil-containing edible films. The present study aimed at producing clove bud or oregano essential oil-containing emulsified edible films in an effort to provide films with antimicrobial properties against spoilage fungi in bakery products, as well as evaluating the effect of the emulsification process on emulsion droplet size and size distribution and on films’ mechanical and antifungal properties.

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MATERIALS AND METHODS

Chemicals. Essential oils from clove bud and oregano were purchased from Ferquima Ltd.a. (Vargem Grande Paulista, Brazil). Potato dextrose agar (PDA) was obtained from Sigma-Aldrich So. (Milwaukee, WI, USA). Polyoxyethylene (20) sorbitan monooleate (Tween 80) was bought from Labsynth Ltd.a. (Diadema, Brazil). Methylcellulose was procured from Sigma-Aldrich Brasil Ltd.a. (São Received: March 2, 2014 Revised: May 2, 2014 Accepted: May 11, 2014

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dx.doi.org/10.1021/jf501055f | J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Journal of Agricultural and Food Chemistry

Article

five random positions with a digital micrometer from Mitutoyo Manufacturing (Tokyo, Japan). Films’ tensile strength (TS), elastic modulus (EM), and elongation at break (EB) were determined in a universal testing machine (model 3367) from Instron Corp. (Canton, MA, USA), fitted with a 1 kN load cell and set to stretch the film strips from an initial gauge length of 50 mm at 50 mm min−1. TS was calculated by dividing the highest load that a film strip withstood prior to breakage by its initial cross-sectional area. EM was given by the relationship between stress and strain at the initial slope of the chart. EB was calculated by dividing the deformation of a film strip right before breaking by its initial length and multiplying by 100 to be expressed as percentage. Bread Storage. Preservative-free bread slices (18.98 ± 0.95 g) were bought at a local bakery in Viçosa, MG, Brazil. They were placed, two by two, inside methylcellulose film/metalized polypropylene bags, which were sealed and stored at 25 ± 2 °C in an effort to simulate usual commercialization conditions of bakery products. The storage system with two slices also aimed at reproducing the typical distribution of sandwiches due to convenience reasons. Preservativefree slices packaged alongside essential oil-free films were used as control (C−). Bread slices with an added commercial antifungal comprising sorbic acid, calcium propionate, ethanol, and grain alcohol were packed likewise, except for the absence of the inner layer (methylcellulose film) of the package system (C+). This antifungal mixture is used in the sliced bread sold at the bakery, and this evaluation allowed the comparison of the shelf life extension provided by the films developed here and by the commercially applied preservation method that advertises a shelf life of 7 days for this product. Table 2 summarizes the components of each storage set.

Paulo, Brazil). Poly(ethylene glycol) (PEG) was obtained from Isofar Ltd.a. (Duque de Caxias, Brazil). Difco Laboratories (Detroit, MI, USA) supplied bacteriological peptone. Essential Oil Concentrations. The concentrations of clove bud and oregano essential oils to be incorporated into the antimicrobial films were determined by diffusion through solid medium in cavitycontaining plates29 against Aspergillus niger (ATCC 16404) and Penicillium sp. (ATCC 2147), common spoilage fungi in bakery products. Aliquots of 100 μL of fungal suspension ((8.0 ± 1.4) × 105 CFU mL−1) were spread onto solidified PDA in 90 mm diameter Petri dishes. A 6 mm diameter cavity was made in the PDA with a sterilized borer at the midpoint of each dish. Cavities were filled with 50 μL of essential oil aqueous solutions at concentrations of 40, 20, 10, 5, 2.5, 1.25, and 0 (control) mg mL−1. An aqueous stock solution comprising 4% (w/v) of clove bud or oregano essential oil, 1.6% (w/v) of Tween 80, and 0.2% (w/v) of PEG was 2 times serially diluted in sterilized distilled water to achieve the mentioned concentrations. Plates were sealed and incubated at 25 ± 2 °C for 5 days before inhibition haloes around cavities were measured to the nearest 0.01 mm with a digital caliper from Mitutoyo Manufacturing (Tokyo, Japan). Six plates were prepared for every essential oil concentration and fungus, three for each repetition. Emulsification. Coarse oil-in-water emulsions were formed by mixing clove bud or oregano essential oil (at the concentration determined in the previous item), 3% (w/v) of Tween 80, and doubledistilled water at 1000 rpm for 5 min. An ultrasonicator (model DES500) from Unique Group (Indaiatuba, Brazil) was used to prepare nanoemulsions by ultrasonicating the coarse emulsions at 20 kHz (frequency) and 400 W (nominal power input) for 10 min. Droplet Size and Polydispersity Index (PdI). The mean droplet diameter and the PdI were determined through light scattering in a Nanophox from Sypatec GmbH (Clausthal-Zellerfels, Germany) after emulsion samples had been diluted in double-distilled water to 1/10 of their initial concentration to avoid multiple scattering effect. Droplet size was indicated by the Z-average, which measures the scattering intensity-weighed mean diameter of the droplets present in an emulsion. Film Casting. To emulsions were added 2% (w/v) of methylcellulose, as the polymeric matrix, and 0.2% (w/v) of PEG, as a plasticizer to improve film handling. The resulting film-forming solution was gently homogenized for 30 min at 6 rpm, rested for 2 h to eliminate air bubbles, cast onto glass plates, and allowed to dry at 25 ± 2 °C overnight. Control films were produced likewise except for the essential oil concentration, which was zero for comparison purposes. Table 1 shows the compositions of all film-forming solutions. For

Table 2. Components Present (+) or Absent (−) in Each Sliced Bread Storage System

MCa (%)

PEGb (%)

CF RCF NCF ROF NOF

2.0 2.0 2.0 2.0 2.0

0.2 0.2 0.2 0.2 0.2

OEOc (%)

CBEOd (%) 4.0 4.0

4.0 4.0

Tween 80 (%)

emulsification

3.0 3.0 3.0 3.0 3.0

mixing mixing ultrasound mixing ultrasound

preservative

film

essential oil

emulsion

C− RC NC RO NO C+

− − − − − +

CF RCF NCF ROF NOF −

− clove bud clove bud oregano oregano −

− coarse nano coarse nano −

Microbiological Evaluation. Counts of yeasts and molds, microorganisms that are known to spoil bakery products in a short period of time, were monitored after 0, 5, 10, and 15 days of storage. Bread slices (25 ± 0.2 g) were randomly and aseptically sampled, diluted in 225 mL of 0.1% (w/v) bacteriological peptone solutions, and homogenized for 2 min in a stomacher from ITR Ltd.a. (Esteio, Brazil). Serial 10-fold dilutions (10−1−10−4) were prepared and inoculated in Petrifilm plates from 3 M do Brasil Ltd.a. (Sumaré, Brazil), specific for counting yeasts and molds. The plates were incubated at 25 ± 2 °C for 5 days before counts of yeasts and molds were reported as colony-forming units per gram of sliced bread, in a logarithm scale (log CFU g−1). Statistical Analysis. All data were submitted to one-way analysis of variance (ANOVA) followed by Tukey’s test at the 5% of probability level in statistical software (version 9.1) from SAS Institute Inc. (Cary, NC, USA).

Table 1. Compositions of Aqueous Film-Forming Solutions film

treatment

a

MC, methylcellulose. bPEG, poly(ethylene glycol). cOEO, oregano essential oil. dCBEO, clove bud essential oil.

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sliced bread shelf life evaluation, the films were cast directly onto the metalized layer of metalized polypropylene sheets, selected for their low gas transmission rates.11 Scanning Electron Microscopy (SEM). Films were characterized as to their morphologies through SEM images taken in a tabletop microscope (model TM3000) from Hitachi High Technologies America, Inc. (Schaumburg, IL, USA) operating with an accelerating voltage of 15 kV and at a magnification of 10000×. Mechanical Properties. At least seven films from each treatment were shaped into 100 mm × 25 mm test strips according to ASTM D882-12. Their thicknesses were measured to the nearest 0.001 mm in

RESULTS AND DISCUSSION Essential Oil Concentrations. Table 3 shows the inhibition halo values of Penicillium sp. and A. niger for each essential oil concentration. No inhibition halo was recorded at concentrations lower than 20 mg mL−1, regardless of the microorganisms and essential oil. The largest (p < 0.05) inhibition halo of A. niger and Penicillium sp. was provided by clove bud and oregano essential oils at 40 mg mL−1 (Table 3). Thus, 40 mg mL−1 was the concentration used for film B



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Table 3. Inhibition Haloes of Aspergillus niger or Penicillium sp. after 5 Days at 25 ± 2 °C, As Affected by Clove Bud or Oregano Essential Oil Concentration clove bud essential oil concn (mg mL−1) 40.0 20.0 10.0 5.00 2.50 1.25 0.00

Aspergillus niger 34.43 15.93 0.00 0.00 0.00 0.00 0.00

± ± ± ± ± ± ±

oregano essential oil

Penicillium sp.

2.10 a 10.20 b 0.00 c 0.00 c 0.00 c 0.00 c 0.00 c

30.71 13.10 0.00 0.00 0.00 0.00 0.00

± ± ± ± ± ± ±

Table 4. Droplet Diameters and Polydispersity Index (PdI) Values of Aqueous Coarse Emulsions and Nanoemulsions of Clove Bud and Oregano Essential Oils emulsion

droplet diametera (nm)

PdI

clove bud

coarse nano

1999.03 ± 1856.82 a 250.43 ± 100.67 b

0.863 0.162

oregano

coarse nano

1313.38 ± 1302.41 a 180.59 ± 84.76 b

0.983 0.220

29.24 15.85 0.00 0.00 0.00 0.00 0.00

± ± ± ± ± ± ±

1.20 a 12.44 b 0.00 c 0.00 c 0.00 c 0.00 c 0.00 c

Penicillium sp. 27.59 9.72 0.00 0.00 0.00 0.00 0.00

± ± ± ± ± ± ±

2.05 a 10.77 b 0.00 c 0.00 c 0.00 c 0.00 c 0.00 c

input of ultrasonication when compared to the low-speed mixing used in coarse emulsification, given that droplets tend to assume an equilibrium diameter as the energy input increases, leading to a more uniform emulsion having reduced PdI values.21,25 Scanning Electron Microscopy. SEM images aimed at confirming that droplet aggregation and coalescence did not take place during film drying and that droplet diameters remained stable in the final films. Figure 1 shows typical SEM micrographs of the methylcellulose films. As expected, the essential oil-free film showed a homogeneous surface without any droplets (Figure 1A). Contrastingly, droplets are easily

production. The antimicrobial activities of the essential oils from oregano and clove bud against several foodborne pathogenic and spoilage microorganisms, including fungi from Aspergillus and Penicillium genera, have been widely reported.11,30−34 Droplet Size and Polydispersity Index. The mean diameters and PdI values obtained for droplets of both clove bud and oregano essential oils in coarse emulsions and nanoemulsions are shown in Table 4. Coarse emulsions

essential oil

3.50 a 12.25 a 0.00 b 0.00 b 0.00 b 0.00 b 0.00 b

Aspergillus niger

Mean values ± standard deviations followed by different letters are significantly different (p < 0.05).

a

produced at low mixing speed had droplets with diameters of a couple of micrometers, which is in accordance with the values (1−20 μm) previously reported in the literature.21 The formation of a coarse emulsion prior to a high-energy process improves both droplet size reduction and polydispersity of the resulting emulsion.35 Coarse emulsion droplets were remarkably larger (p < 0.05) than those present in nanoemulsions (Table 4), regardless of the essential oil used. Droplet breakdown is a nonspontaneous process that requires enough energy input to enhance droplet interfacial area by overcoming its surface free energy,21 and the low-speed process used for coarse emulsion preparation did not provide the required energy to reduce droplet size to the nanoscale. Ultrasonication, however, created thoroughly disruptive forces resulting from an intense acoustic field, leading to rapid formation and collapse of microbubbles at the droplet interface.36 The collapse of microbubbles, known as cavitation, induced turbulence and shock waves that disrupted droplets to the nanoscale level.35,37,38 The type of essential oil did not affect (p > 0.05) droplet size either in coarse emulsions or in nanoemulsions (Table 4). Another remarkable difference between the coarse emulsions and nanoemulsions produced here was the PdI. Coarse emulsions had PdI values close to unity (Table 4), indicating a multimodal, wide droplet size distribution. Nanoemulsions, however, had a narrow size distribution as indicated by low PdI values. This difference is attributable to the increased energy

Figure 1. Typical SEM micrographs of methylcellulose films (A) with added clove bud or oregano coarse emulsions (B and D, respectively) or nanoemulsions (C and E, respectively). C



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Table 5. Mechanical Properties of Methylcellulose Films Incorporated or Not with Clove Bud or Oregano Essential Oil Coarse Emulsions or Nanoemulsions essential oil

a

emulsion

TSa (MPa)

EMa (MPa)

EBa (%)

5.40 ± 1.13 a

118.86 ± 24.53 a

20.46 ± 2.71 a

clove bud

coarse nano

6.07 ± 1.11 a 6.11 ± 1.26 a

53.97 ± 8.71 b 56.79 ± 16.58 b

40.29 ± 4.53 b 56.61 ± 5.59 c

oregano

coarse nano

8.05 ± 1.45 a 7.61 ± 1.32 a

104.21 ± 4.15 a 72.94 ± 10.97 b

34.08 ± 5.17 b 54.77 ± 1.66 c

Mean values ± standard deviations followed by different letters within the same column are significantly different (p < 0.05).

observed in the emulsified films. Methylcellulose films with added coarse emulsions (Figure 1B,D) presented much larger droplets and a more heterogeneous size distribution profile than films with added nanoemulsions (Figure 1C,E), regardless of essential oil type. This validates the droplet diameter and PdI values obtained through light scattering (Table 4) and also indicates that the emulsion remained stable with regard to droplet diameter during film polymerization at the tested conditions. Mechanical Properties. The mechanical attributes tensile strength (TS), elastic modulus (EM), and elongation at break (EB) of the films produced here are summarized in Table 5. The essential oils added to methylcellulose films had a plasticizing effect, as suggested by reduced (p < 0.05) EM and increased (p < 0.05) EB when compared to those of essential oil-free films. However, TS was not affected (p > 0.05) by the addition of essential oils. Similarly to our results, essential oils have been widely reported to weaken the intermolecular interactions between polymeric chains, resulting in less rigid and more extensible and flexible films.19,39−44 The reduction in droplet size led to an even more remarkable plasticizing effect, because smaller droplets increased (p < 0.05) the EB and reduced (p < 0.05) the EM of the methylcellulose films. The addition of clove bud essential oil nanodroplets provided almost a 3-fold increase in EB and a 2-fold decrease in EM when compared to control films. Oregano essential oil showed a similar behavior. Microbiological Evaluation. The counts of yeasts and molds throughout the storage of sliced bread are illustrated in Figure 2. At the very beginning of the storage period, the counts of yeasts and molds did not differ (p > 0.05) among the different treatments because no time was available for microbial development, even in C− in which neither synthetic preservatives nor antimicrobial films had been used. As expected, there was a trend of increasing counts of yeasts and molds during storage, regardless of treatment. Different storage conditions (Table 2), however, led to different survival patterns. After 5 days, the counts in all treatments were not different (p > 0.05), except in slices packaged alongside clove bud nanoemulsion films (NC), which showed counts lower (p < 0.05) than the other treatments. The synthetic antifungal present in C+ worked just as well as the antimicrobial films until day 5, but the emulsified films were more efficient (p < 0.05) in lessening microbial growth at all further analysis times. At 10 days of storage, the essential oil-free treatments (C− and C+) allowed greater (p < 0.05) growth of yeasts and molds when compared to the treatments that included antimicrobial films. This suggests that neither the essential oil-free film (C−) nor the synthetic preservative (C+) was effective in preventing microbial development after 10 days of storage at 25 ± 2 °C,

Figure 2. Counts of yeasts and molds in bread slices containing (C+) or not (C−) synthetic antifungal and packaged alongside methylcellulose films incorporated with clove bud and oregano essential oils coarse emulsions (RC and RO, respectively) or nanoemulsions (NC and NO, respectively), throughout 15 days of storage at 25 ± 2 °C. In the table, different letters within the same column indicate different means (p < 0.05).

conditions that simulate conventional commercialization practices of bakery products. At 15 days of storage, C− bread showed the greatest (p < 0.05) count of yeasts and molds, followed by C+ and then antimicrobial film-containing treatments. This corroborates the hypothesis that clove bud and oregano essential oils are effective in lessening microbial development in food matrices, even when compared to the commercial antimicrobial technique currently used (C+). Overall, clove bud and oregano essential oils within the same droplet diameter range displayed similar (p > 0.05) antimicrobial activities against yeasts and molds, although clove bud nanodroplets were more effective (p < 0.05) than oregano nanodroplets at days 10 and 15. The antifungal activities of clove bud and oregano essential oils are related to their major phenolic constituents eugenol and carvacrol (Figure 3), respectively.45 These phenols interact with and alter the

Figure 3. Chemical structures of eugenol (A) and carvacrol (B). D



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permeability of cell membranes, leading to leakage of cell contents, which are essential to microorganism survival.46 The similarity observed here is also attributable to the presence of hydroxyl groups (Figure 3) and delocalized electrons.47,48 The delocalized electrons allow proton release from the hydroxyl groups in a way that the proton gradient through cell membrane is reduced. The reduced proton gradient, along with the resulting depletion of the ATP pool, kills microbial cells.45 Droplet size reduction from a few micrometers to a few hundreds of nanometers improved (p < 0.05) the antimicrobial properties of the clove bud essential oil-containing films (Figure 2). Although this difference was not significant (p > 0.05) for oregano essential oil, there is a clear trend of decreasing the counts of yeasts and molds by smaller droplets. This observation is attributable to the increased bioavailability of nonpolar bioactive compounds encapsulated in smaller droplets, which possess a higher surface-to-volume ratio and are able to more easily penetrate cell membranes.22,26 This improvement in antimicrobial properties of nanoemulsified films provided by reduced droplet diameters had already been reported for cinnamaldehyde emulsions, but in laboratory medium.25 In summary, emulsion films were successfully produced with plant essential oils that displayed antimicrobial activity against spoilage fungi in bakery products. Ultrasonication was effective in reducing droplet diameter and in narrowing droplet size distribution. Both essential oils acted as plasticizers in methylcellulose films, as well as provided them with antimicrobial activity against yeasts and molds in sliced bread. Droplet size reduction was shown to increase both plasticizing and antimicrobial behaviors of essential oils. The antimicrobial films developed here improved sliced bread shelf life, even when compared to the commercial antifungal agent that is currently used in bakeries. The improvement of antimicrobial properties of an essential oil simply by reducing its droplet size has clear implications for food preservation, as lower preservative contents may be used to deliver the same antimicrobial efficiency if encapsulated in smaller particles. Future works are needed to validate the efficiency of the system proposed here in prolonging the shelf life of different food products and to study its impacts on product acceptance by consumers as well as to assess the feasibility of scaling up this system to a large-scale food production scenario.

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This work was supported by the National Council for Scientific and Technological Development/CNPq (Grant 800184/20114). Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED PDA, potato dextrose agar; PdI, polydispersity index; SEM, scanning electron microscopy; TS, tensile strength; EM, elastic modulus; EB, elongation at break; CFU, colony-forming units; PEG, poly(ethylene glycol)

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*(N.F.F.S.) Phone: +55 31 3891 1796. E-mail: nfsoares@ufv. br. Present Addresses †

(C.G.O.) National Nanotechnology Laboratory for Agribusiness, EMBRAPA-CNPDIA, Rua XV de Novembro 1452, São Carlos, SP 13560-970, Brazil, and PPG-CEM, Department of Materials Engineering, Federal University of São Carlos, Rod. Washington Luis, km 235, São Carlos, SP 13565-905, Brazil. § (S.F.O.P.) Department of Rural and Animal Technology, Southwest Bahia State University, Praça Primavera 40, Itapetinga, BA 45700-000, Brazil. E



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