Abstract
Duck feet gelatin (DFG) films were prepared and applied to the packaging of cherry tomatoes. Cinnamon leaf oil (CLO) was incorporated into the DFG films at concentrations of 0.5, 1.0, and 1.5% to provide antimicrobial activity. The DFG films with 1.0% CLO incorporation exhibited the most desirable tensile strength (41.6 MPa) and elongation at break (18.5%). Regarding the antimicrobial activity, the DFG films containing CLO significantly inhibited the growth of foodborne pathogens. In addition, the DFG film with 1.0% CLO was employed in the coating and wrapping of cherry tomatoes inoculated with Salmonella typhimurium. The DFG film with 1.0% CLO incorporation reduced the population of the bacteria to below the detection limit. Moreover, the DFG film with CLO delayed the color change on cherry tomatoes. Overall, the DFG film with CLO enhanced the shelf life of cherry tomatoes and can be used as an antimicrobial packaging.
Keywords: Antimicrobial activity, Cherry tomato, Cinnamon leaf oil, Duck feet gelatin
Introduction
Petroleum-based film materials are widely used, but they are not biodegradable. With increasing need for eco-friendly packaging materials, biodegradable films have been developed to replace conventional plastic packaging materials. To prepare the biodegradable films, various film sources have been investigated with different strategies, such as using food processing by-products to overcome high cost [1]. In particular, edible films and coatings have been applied in food systems [2].
Gelatin is a major protein resource for edible films and is obtained from hydrolysis of collagen originating from skins and tendons of vertebrates and invertebrates [3]. Although a considerable amount of gelatin is supplied from porcine skin and bovine hides, poultry feet are also a collagen-rich material and can be used as a gelatin source [4]. Recently, chicken feet gelatin has been used for an edible film [5].
Duck meats are widely consumed in smoked, boiled, or roasted form and their processing generates by-products, such as duck feet. Thus, duck feet gelatin has been extracted to utilize the waste and its physiochemical properties have been reported [6], although duck feet gelatin films for food packaging have never been studied.
Essential oils have been incorporated into gelatin films and coatings to provide antimicrobial and antioxidant activities [7]. However, the addition of essential oils into gelatin films can alter the physical properties of the films because of the interactions between gelatin molecules and oils [8]. Among essential oils, cinnamon leaf oil has shown strong antibacterial activities against foodborne pathogens [9]. This activity is observed because the oil contains up to 95% eugenol followed by trans-cinnamaldehyde [10]. Compared to cinnamon bark oil, cinnamon leaf oil has been scarcely used in antimicrobial films for active packaging. It was reported that the chitosan-based films containing cinnamon leaf oil were prepared and applied to the coating of strawberries [11].
Center for Disease Control and Prevention (CDC) reports indicate that Salmonella typhimurium is one of the most frequently occurring pathogens in various foods [12]. Thus, control of S. typhimurium using essential oils has been studied for the preservation of meat, milk, fruit, and vegetables [13]. Cinnamon bark essential oil has been used to treat tomatoes inoculated with S. typhimurium, resulting in significant reduction of the pathogenic bacteria [14]. Recently, it was reported that zein coating with cinnamon oil effectively eliminated S. typhimurium from inoculated cherry tomatoes [15].
Till date, there have been no reports on duck feet gelatin (DFG) films or coating containing cinnamon leaf oil (CLO) applied to cherry tomatoes. Therefore, the present study aims to develop a DFG film containing CLO, characterize its physical properties, and evaluate antimicrobial activity in the packaging of cherry tomatoes. The results from this study could promote the possibility that DFG films with CLO could be used as a food packaging material.
Materials and methods
Materials
Duck feet and cherry tomatoes were obtained locally. CLO was obtained from Gooworl Co. (Daegu, Korea). The strains of Staphylococcus aureus (ATCC 10537 and KCTC 1621), Listeria monocytogenes (ATCC 19111 and ATCC 19115), S. typhimurium (ATCC 14028 and KCTC 2421), and Escherichia coli O157:H7 (ATCC 43889 and NCTC 12079) were used as major pathogenic bacteria in this study.
Extraction of DFG
Duck feet were washed with tap water. Visible fat and non-collagenous proteins in the duck feet were manually separated, packed in a polyethylene bag, and kept at −20 °C until further use. Duck feet gelatin was prepared following the process of Park et al. [16] with minor modifications. Duck feet were soaked in 0.1 N hydrochloric acid (1:10, w/v) at 18 °C for 18 h, and then washed with tap water for 2 h. The swollen duck feet were homogenized in water (1:5, w/v) with a blender, and heat-treated at 95 °C for 2 h to extract the gelatin. After filtering the extracted gelatin with six-layered gauze, the filtrate was cooled at 20 °C for 30 min followed by removal of the fat layer. The extracted gelatin was kept at 18 °C for 5 h after which the fat layer was removed again. The gelatin solution was then frozen at −70 °C and freeze-dried. The yield of gelatin was approximately 15%. The powdered gelatin was kept at 4 °C prior to use.
SDS–PAGE analysis
Duck feet gelatin was dissolved in 5% SDS solution and mixed with sample buffer (2% SDS, 2% β-mercaptoethanol, 65.8 mM Tris–HCl, and 0.01% bromophenol blue). The sample was loaded and separated on a stacking gel (5%) and separating gel (7.5%). After electrophoresis, the gel was stained and then de-stained. Protein molecular weight markers (Bio-Rad Laboratories, Hercules, CA, USA) ranging from 20 to 250 kDa were used to estimate the molecular weight.
Analysis of the amino acid composition of DFG
The amino acids of DFG were analysed using liquid chromatography with Waters 510 pumps, a Waters 2487 UV detector, and a Waters 717 automatic sampler (Waters, Milford, MA, USA), with a Pico-Tag column (Waters). Each amino acid was identified and quantified by comparing retention time and peak area with an authentic standard mixture using Empower 2 software (Waters).
Preparation of DFG films
DFG (3 g, w/v), CLO (0.5, 1.0, and 1.5 g, w/v), and Tween-80 (25% of CLO, w/w) were dissolved in distilled water (100 mL) at 50 °C for 30 min. Amount of the CLO was 16.7, 33.3, and 50.0% relative to DFG (w/w), respectively. Homogenization of the mixture was achieved using a homogenizer (Ultra-Turrax T25, IKA, Staufan, Germany) at 10,000×g for 5 min followed by sonication for 8 min (Sonics and Materials, Inc., Newtown, CT, USA). After filtering the solution with six-layered gauze, the filtrate was kept at 60 °C for 30 min. Fructose as a plasticizer (1.2 g, w/v) was added into the film-forming solution. The DFG film was prepared by pouring the film-forming solution onto a Teflon-coated plate. After drying at 20 °C for 18 h, the film was preconditioned in a humidity chamber at 25 °C and 50% relative humidity (RH) to determine the film properties.
Determination of DFG film properties
The rectangular DFG films were prepared and the average of five thickness values taken at random locations was calculated using a micrometer (Mitutoyo, Tokyo, Japan). The mechanical properties of the DFG films were determined using a Testometric machine (M250-2.5 CT, Testometric Company Ltd., Lancashire, UK) equipped with a load cell of 100 N. Tensile strength (TS) and elongation at break (E) of the film samples (2.54 × 10 cm) were measured under the conditions of 5 cm of initial grip distance with 50 mm/min of cross-head speed. Five replicates were used for each film. The water vapor permeability (WVP) of the DFG films was evaluated using poly (methyl acrylate) cups with 18 mL distilled water [17]. The color of the DFG films are represented by L*, a*, b*, and total color difference (ΔE*) values using a colorimeter (CR-400, Minolta, Tokyo, Japan). For the opacity of DFG films, the films were cut into 10 × 25 mm and the absorbance at 600 nm was determined using a spectrophotometer (UV-2450, Shimadzu Corporation, Kyoto, Japan).
Antimicrobial activity measurement of the DFG films
To assess the antimicrobial activity of the DFG films, disc agar diffusion tests were performed. E. coli O157:H7 (ATCC 43889 and NCTC 12079) and S. typhimurium (ATCC 14028 and KCTC 2421) were used as Gram-negative bacteria and cultured in Tryptic Soy Broth (TSB, Bacto/Difco, Becton–Dickinson, Sparks, MD, USA) at 37 °C for 18 h. Staphylococcus aureus (ATCC 10537 and KCTC 1621) and L. monocytogenes (ATCC 19111 and ATCC 19115) used as Gram-positive bacteria were cultured in Brain Heart Infusion broth (Bacto/Difco). The cocktail of each strain was streaked on Mueller–Hinton agar (Bacto/Difco). The solution of the DFG film containing CLO was prepared by dissolving the film in distilled water (0.25 g/mL). Dissolved film was then poured onto the discs (8 mm, diameter) and dried on a clean bench for 30 min. The dried disc was placed onto the inoculated medium and subsequently incubated at 37 °C for 18 h. Inhibition zone (diameter, mm) was determined with a Digimatic calliper (Mitutoyo Corp., Kawasaki, Japan).
Application of the DFG films to packaging of cherry tomatoes
Solutions of DFG and DFG containing 1.0% CLO (DFG–CLO) were prepared to study the coating of cherry tomatoes while DFG films were prepared to examine wrapping of cherry tomatoes. Cherry tomatoes (15 ± 1 g) uniform in size and maturity were prepared and stored at 4 ± 1 °C. Salmonella strains (ATCC 14028 and KCTC 2421) were cultured in 25 mL of TSB at 37 °C for 18 h with shaking (150 rpm) until reaching 7 log CFU/mL. The cocktail of strains was inoculated on cherry tomatoes by the dipping method and the tomatoes were dried at 20 °C for 30 min. The cherry tomatoes were then coated with the solution of DFG or DFG–CLO and left to dry on a clean bench for 1 h. For wrapping cherry tomatoes, the films with or without CLO were prepared one day prior to the experiment and heat-sealed in a pouch form. Three cherry tomatoes were wrapped in a pouch with the dimension (3.5 × 3.5 × 12 cm) and kept them in PET container at RH 70 ± 10% and 4 ± 1 °C for 10 days. For the microbial analysis, cherry tomatoes (15 g) were immersed in peptone water (135 mL) and shaken for 3 min. The homogenized samples were serially diluted, and 0.1 mL of the solution was spread on xylose lysine deoxycholate agar (Bacto/Difco) and incubated at 37 °C. After 24 h, colonies were counted as CFU/g.
To evaluate the quality changes in the cherry tomatoes during storage, the weight loss of the cherry tomatoes was measured by comparing with initial weight. In addition, the color change of the cherry tomatoes was measured. Ten fruits were used for color measurement. In particular, the effects of coating and wrapping with the DFG or DFG–CLO films were evaluated by a/b value.
Statistical analysis
One-way analysis of variance was performed to analyse the experimental data using SAS (SAS Institute Inc., Cary, NC, USA) with Duncan’s multiple range test. All experiments were repeated three times, except the physical properties of the films (n = 5). p < 0.05 was considered to be statistically significance.
Results and discussion
Molecular properties of DFG
The molecular weight profile of DFG was visualized on a SDS–PAGE gel (Fig. 1). DFG was mainly comprised of two different α-chains (α1, 120 kDa and α2, 140 kDa), β-chains (dimers of the α-chains; 230 kDa), and γ-chains (trimers of the α-chains; 280 kDa). The profile indicates a typical type I collagen, which consists of α-, β-, and γ-chains. However, Park et al. [16] identified the molecular weight profile of DFG extracted under different temperature and pressure conditions as having 120–130 kDa (α1 and α2) and 200 kDa (β-chain), which differs from our results. This difference might be explained by the fact that the molecular weight profile of gelatin is affected by the extraction conditions.
Fig. 1.
Molecular weight profile of DFG on a SDS–PAGE. Lane (1) Prestained molecualr marker, (2) DFG
The major amino acids of collagen are glycine, alanine, proline, and hydroxyproline, regardless of gelatin sources. The amino acid composition of DFG is represented in Table 1. The glycine content in the DFG was 32.8%, almost one-third of total amino acid contents, and glycine is known to play an important role in the tight helix structure of collagen [18]. The glycine content of DFG is similar to those of chicken feet gelatin (33.6%) and tilapia scale gelatin (34.9%) [4, 19]. In addition, tryptophan was not detected in the DFG, which is in good agreement with the reports of chicken feet gelatin [20] and tilapia scale gelatin [19].
Table 1.
Amino acid composition of DFG
| Amino acid | % |
|---|---|
| Aspartic acid | 4.60 |
| Glutamic acid | 7.29 |
| Threonine | 2.01 |
| Serine | 2.87 |
| Glycine | 32.84 |
| Alanine | 11.06 |
| Cysteine | 0.06 |
| Valine | 1.75 |
| Methionine | 0.87 |
| Isoleucine | 1.18 |
| Leucine | 2.53 |
| Phenylalanine | 1.65 |
| Tyrosine | 0.47 |
| Lysine | 3.04 |
| Histidine | 1.18 |
| Arginine | 4.86 |
| Proline | 12.09 |
| Hydroxyproline | 9.65 |
| Total | 100 |
Physical and optical properties of DFG films
The physical properties of DFG films with and without added CLO are shown in Table 2. The prepared DFG film was brittle without a plasticizer. When fructose was used in the DFG film, TS (52.3 MPa) and E (15.5%) were obtained (Table 2). The thickness of DFG films was ranged from 69 to 90 μm and increased a little by the addition of CLO. Lee et al. (2016) [17] also found an increase in film thickness of skate skin gelatin films by the incorporation of thyme essential oil. The hydrophobic interactions between gelatin molecules and essential oils might cause rearrangement of gelatin molecules, consequently affecting film thickness.
Table 2.
Physical properties of the DFG films containing CLO
| CLO (%) | Thickness (μm) | Tensile strength (MPa) | Elongation (%) | WVP (×10−9 g/m s Pa) |
|---|---|---|---|---|
| 0 | 69.20 ± 2.68d,1) | 52.31 ± 1.47a | 15.52 ± 0.64c | 2.14 ± 0.01b |
| 0.5 | 76.20 ± 1.30c | 42.11 ± 0.54b | 24.70 ± 0.90a | 2.08 ± 0.09b |
| 1.0 | 85.40 ± 2.61b | 41.56 ± 0.35b | 18.47 ± 0.03b | 2.15 ± 0.02b |
| 1.5 | 90.40 ± 3.65a | 37.28 ± 0.32c | 12.88 ± 1.03d | 2.95 ± 0.09a |
1)Values are mean ± SD (n = 5). Any means in the same column followed by different letters are significantly (p < 0.05) different by Duncan’s multiple range test
The TS of DFG films varied from 37.3 to 52.3 MPa. The control film had the highest TS value (52.3 MPa), whereas TS of DFG films incorporated with CLO were lower. In most cases, the addition of essential oils to gelatin films has been reported to cause decreases in TS. Wu et al. [21] reported the decrease of TS in the gelatin film incorporated with cinnamon oil nanoliposome. Martucci et al. [22] also suggested that the TS of gelatin film containing lavender oil decreased with increasing concentration of the oil. The reason for this trend might be explained by the change in the molecular interactions among gelatin molecules in the film being affected by the addition of essential oil, resulting in a decrease of TS in the films containing essential oil [23].
The DFG films incorporated with 0.5 and 1.0% CLO had higher E values than the control film, whereas the DFG films with 1.5% CLO had a lower E value (Table 2). Similarly, Ahmad et al. [24] reported that the E value in the gelatin film containing bergamot oil increased up to a specific concentration of oil and thereafter decreased. These results suggest that the compatibility between gelatin and essential oil is important with regard to the physical properties of the films, and addition of an excessive amount of oil can cause a heterogeneous film structure, affecting the E value.
The WVP value was the lowest for the DFG film with 0.5% CLO, 2.08 × 10−9 g/m s Pa (Table 2). However, there was no significant difference between the DFG films and DFG films with CLO, except the film with 1.5% CLO, which has the highest WVP, 2.95 × 10−9 g/m s Pa. Teixeira et al. [25] found that the WVP values of the gelatin films incorporated with garlic or organum oil were not statistical different from the control films. Martucci et al. [22] also found that the WVP of gelatin films incorporated with oregano oil was not changed. Similar results for the gelatin films incorporated with bergamot oil were obtained by Ahmad et al. [24]. In general, the hydrophobicity of films is increased by the addition of essential oil, and the incorporation of hydrophobic oils into hydrophilic gelatin molecules usually decreases WVP [26]. However, this trend was not observed in this study.
The optical properties of the DFG films are shown in Table 3. The addition of CLO to DFG films caused increases in the yellowness (b*) and the total color value (ΔE*) of the films and decrease in the redness (a*). The opacity values were decreased by the incorporation of CLO. In particular, the DFG film with 1.0% CLO had the lowest value. Thus, the DFG films with 1% CLO can be used as a see-through packaging material. Lee et al. [5] also reported that the opacity of chicken gelatin film was lowered with the addition of 1.0% clove oil. Based on the mechanical and optical properties of DFG films with CLO, the DFG film with 1.0% CLO was used for the packaging of cherry tomatoes.
Table 3.
Optical properties of the DFG films containing CLO
| CLO (%) | L* | a* | b* | ΔE* | Opacity |
|---|---|---|---|---|---|
| 0 | 96.24 ± 0.01b,1) | −1.28 ± 0.02a | 7.60 ± 0.01d | – | 2.86 ± 0.07a |
| 0.5 | 96.37 ± 0.02a | −1.93 ± 0.03b | 9.23 ± 0.01c | 1.76 ± 0.01c | 1.66 ± 0.04b |
| 1.0 | 96.26 ± 0.03b | −2.92 ± 0.01c | 10.84 ± 0.02b | 3.62 ± 0.01b | 0.37 ± 0.04d |
| 1.5 | 96.13 ± 0.06c | −3.62 ± 0.02d | 12.93 ± 0.03a | 5.81 ± 0.01a | 0.50 ± 0.02c |
1)Values are mean ± SD (n = 5). Any means in the same column followed by different letters are significantly (p < 0.05) different by Duncan’s multiple range test
Antimicrobial activity of the DFG films
The antimicrobial activities of the DFG films were tested against S. typhimurium, E. coli O157:H7, L. monocytogenes, and S. aureus by the agar diffusion method (Table 4). The DFG film without CLO did not inhibit the growth of bacterial pathogens, whereas the inhibition zone increased proportionally to the increase of CLO concentration. In addition, the antimicrobial activities were more effective against S. aureus and L. monocytogenes than S. typhimurium and E. coli O157:H7 due to extra lipopolysaccharide in outer membrane of Gram-negative bacteria. The antimicrobial activity of CLO is attributed to eugenol, which disrupts the membrane structure of S. typhimurium [27]. CLO also contains trans-cinnamaldehyde that inhibits ATPase, resulting in the inhibition of APT synthesis thus killing the bacteria [28]. Recently, it was reported that zein films with eugenol incorporated had antimicrobial activity against Bacillus cereus and Salmonella enterica [29]. Based on these results, the DFG films with CLO can be used as an active packaging with antimicrobial activity.
Table 4.
Antimicrobial activities of the DFG films against pathogenic bacteria
| CLO (%) | Inhibition zone (mm) | |||
|---|---|---|---|---|
| E. coli O157:H7 | S. typhimurium | S. aureus | L. monocytogenes | |
| 0 | 0 | 0 | 0 | 0 |
| 0.5 | 12.64 ± 0.37c,1) | 11.36 ± 0.98c | 15.91 ± 0.26c | 23.07 ± 0.25c |
| 1.0 | 22.75 ± 1.15b | 21.01 ± 0.93b | 28.18 ± 0.34b | 27.36 ± 2.25b |
| 1.5 | 28.60 ± 0.30a | 26.70 ± 1.70a | 37.39 ± 2.93a | 33.68 ± 1.98a |
1)Values are mean ± SD (n = 5). Any means in the same column followed by different letters are significantly (p < 0.05) different by Duncan’s multiple range test
Application of the DFG films to packaging of cherry tomatoes
The DFG film with 1.0% CLO incorporated (DFG–CLO) was used for both the coating and wrapping of cherry tomatoes. The microbial analysis of the cherry tomatoes coated and wrapped with the DFG film and DFG–CLO was evaluated during storage (Fig. 2). The initial population of S. typhimurium on the samples was 5.28 log CFU/g right after inoculation. The population of S. typhimurium in the control samples reached 2.5 log CFU/g on the 5th day, and it was 2.2 log CFU/g on the 10th day of storage. Similarly, the populations of S. typhimurium in the cherry tomatoes coated and wrapped with the DFG film were 2.1 and 1.8 log CFU/g on the 5th and 10th days, respectively. In contrast, the populations of S. typhimurium in the cherry tomatoes coated and wrapped with DFG–CLO had decreased to below the detection limit (1.0 log CFU/g) on the 3rd day of storage. These results clearly indicate that DFG–CLO effectively reduced the population of S. typhimurium inoculated on the samples. Similar to our results, Yun et al. [15] reported a decrease in the population of S. typhimurium on cherry tomatoes using zein coating incorporated with cinnamon bark oil.
Fig. 2.
Changes in the population of Salmonella typhimurium on the cherry tomatoes coated and wrapped with DFG films during storage. Filled circle control, open circle coating with DFG, inverted triangle coating with DFG containing CLO, triangle wrapping with DFG film, square wrapping with DFG film containing CLO
The weight loss in the cherry tomatoes showed a gradual increase during 10 days of storage. The weight losses of the cherry tomatoes coated and wrapped with the DFG and DFG–CLO films were slightly lower than those of the control samples. However, there were no significant differences between the DFG film and the DFG–CLO. These results are similar with the report of Yun et al. [15], where there was no improvement in weight loss by zein coating with cinnamon oil or mustard oil.
Regarding the color change of cherry tomatoes during storage, the cherry tomatoes wrapped with the DFG–CLO had a higher L value than other samples (data not shown). The color change of the cherry tomatoes during storage can be compared as a/b value. An a/b value in the range of 0.95–1.2 is accepted as a ripe fruit. In this study, the color a/b values of the cherry tomatoes coated with the DFG films were not different from those of the control (0.9–1.1). In contrast, the color a/b value of the cherry tomatoes wrapped with the DFG–CLO had a lower value of 0.8, which indicates a significant difference from other treatments. These color a/b values suggest that the wrapping of the cherry tomatoes with the DFG film with CLO can retard ripening during storage. Similarly, it was reported that zein coating of tomatoes and cherry tomatoes also retards ripening [15, 30].
In conclusion, the DFG film containing CLO effectively inhibited the growth of S. typhimurium inoculated on cherry tomatoes during storage compared to the control. In addition, the DFG film containing CLO reduced the color change on cherry tomatoes. Therefore, the DFG film incorporated with CLO developed in this study can be used as a new packaging material to enhance the microbial safety of cherry tomatoes.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
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