Investigation of physicochemical and antioxidant properties of gelatin edible film mixed with blood orange (Citrus sinensis) peel extract

Food Packaging and Shelf Life 21 (2019) 100342

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Investigation of physicochemical and antioxidant properties of gelatin edible film mixed with blood orange (Citrus sinensis) peel extract

T

⁎

Mourad Jridia,b, , Soumaya Boughribaa, Ola Abdelhedia, Hend Nciria, Rim Nasria, Hela Kchaoua, Murat Kayac, Hichem Sebaib, Nacim Zouaria,d, Moncef Nasria a

Laboratory of Enzyme Engineering and Microbiology, Engineering National School of Sfax (ENIS), University of Sfax, Sfax, Tunisia Higher Institute of Biotechnology of Beja, University of Jendouba, Beja, Tunisia c Higher Institute of Applied Biology of Medenine, University of Gabes, Medenine, Tunisia d Department of Biotechnology and Molecular Biology, Faculty of Science and Letters Aksaray University, 68100, Aksaray, Turkey b

A R T I C LE I N FO

A B S T R A C T

Keywords: Grey triggerfish skin gelatin Blood orange (Citrus sinensis) peel Release kinetics of phenolic extract FTIR analysis Wetting and thermal properties

The present study aims at developing Grey triggerfish skin gelatin films containing phenolic extracts from blood orange (Citrus sinensis) peel, as an alternative for the existing synthetic packaging films. The effect of drying pretreatment on the phenolic compounds’ profile and antioxidant and antibacterial activities of the extracts was investigated. Physicochemical, thermal and mechanical properties of gelatin films incorporated with orange peel extract, at different concentrations and plasticized with glycerol were investigated. Films were also tested for their antioxidant capacity, monitored through the β-carotene bleaching, DPPH radical-scavenging and reducing power activities. Results showed that the fresh orange peel extract (FOPE) was more effective against all bacteria tested and exhibited higher antioxidant effect than the thermally-dried orange peel extract (DOPE). In addition, the LC-ESI-MS analysis showed that the quinic acid was the major compound among the total poly-phenols followed by rutin, trans-ferulic acid, naringenin and 4,5-di-O-caffeoylquinate. After its addition, FOPE modified the mechanical and thermal properties of gelatin films, which showed more deformable texture than the control gelatin film. This effect may be caused by the interactions between phenolic compounds of the extract and gelatin chains, as assessed by the Fourier Transform infrared (FTIR) analysis. The FOPE-added films presented higher antioxidant properties than the control. Furthermore, release kinetics of FOPE through gelatin film showed controlled quasi-Fickian diffusion. The overall results emphasized the potential use of phenolic compounds from blood orange by-products to produce bioactive films intended for food packaging.

1. Introduction Natural biopolymers are attracting the scientific attention, as they can be used to address environmental concerns and consumer demands (Niaounakis, 2015; Sangha, Ravichandran, Prithiviraj, Critchley, & Prithiviraj, 2010). These biopolymers can be derived from different origins, including polysaccharides, lipids or proteins (such as gelatin) (Abdelhedi et al., 2018; Arfat, Ahmed, Hiremath, Auras, & Joseph, 2017; Chiralt, González-Martínez, Vargas, & Atarés, 2018; Costa, Silva, & Boccaccini, 2018). Gelatin has valuable properties in pharmaceutical, medicinal and industrial applications due to its transparency, film-forming ability, and high barrier properties (Etxabide, Uranga, Guerrero, & de la Caba, 2017). In this context, edible gelatin-based coatings have been used to

preserve foods, including meat (Jridi et al., 2018) and fruits (Khan, ZillE-Huma, & Dangles, 2014), in order to extend their shelf-life and improve their quality and safety during storage. Moreover, gelatin-based films may be used as carriers of bioactive additives, to achieve active packaging functions and protect, consecutively, food products from oxidation and microbial spoilage, resulting in their quality preservation. The interactions between the bioactive and the gelatin polymer can provide its controlled release over the storage time. Among the most used functional molecules, emulsifiers, antioxidants and antimicrobials, are usaually used to achieve this goal (Adilah, Jamilah, Noranizan, & Hanani, 2018; Ramos, Valdés, Beltrán, & Garrigós, 2016; Santoro, Tatara, & Mikos, 2014). Due to safety concerns associated to synthetic active compounds, extensive research has been performed for the naturally-occuring molecules, where the most famous family is the

⁎ Corresponding author at: Laboratoire de Génie Enzymatique et de Microbiologie, Université de Sfax, Ecole Nationale d’Ingénieurs de Sfax, B.P. 1173-3038 Sfax, Tunisie. E-mail address: [email protected] (M. Jridi).

https://doi.org/10.1016/j.fpsl.2019.100342 Received 18 September 2018; Received in revised form 8 April 2019; Accepted 29 May 2019 2214-2894/ © 2019 Elsevier Ltd. All rights reserved.

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2.4. Liquid chromatography-electrospray ionization mass spectrometry (LCESI-MS) analysis

phenolic compounds, largely present in plants. Citrus is among the most important fruit tree in the world, with an annual production up to 140 million tons in 2015 (FAOSTAT, 2018). Citrus sinensis represents the largest citrus cultivar group grown around the world, accounting for about 70% of the total annual production of Citrus species (Abbate et al., 2012). The citrus industry generated substantial quantities of peels and seed residues as by-products of orange juice processing, accounting for up to 50% of the total fruit weight (Balasundram, Sundram, & Samman, 2006). Considering the compositional profile of Citrus peels, their transformation into value-added products, like natural bioactive extracts rich in phenolic compounds, is a promising option with great economic and environmental perspectives (Laufenberg, Kunz, & Nystroem, 2003). In fact, recent studies have reported the efficiency of orange peel as an excellent source of phenolics and flavonoids (Ozturk, Parkinson, & Gonzalez-Miquel, 2018). Moreover, orange peels have been studied due to their numerous biological activities (Barrales et al., 2018; Devi et al., 2015; Lee, Lee, Lee, Baeg, & Shim, 2012; Ozturk et al., 2018). In this context, the aim of the present study is improve the biological properties of grey triggerfish skin gelatin films (GF) by the incorporation of phenolic extracts from blood orange (C. sinensis) peels. The phenolic profiles and antioxidant and antibacterial activities of the extracts were determined, as well as their effects on the physicochemical, structural, thermal, mechanical and biological properties of the resulting films were investigated.

Twenty mg of each extract powder were dissolved in 1 ml of 10% methanol, and then the mixture was filtered through a 0.45 μm membrane filter before injection into the HPLC system. Analysis was performed using a LC–MS-2020 quadrupole mass spectrometer analyzer (Shimadzu, Kyoto, Japan) equipped with an electro-spray ionization source (ESI) and operated in negative ionization mode. Mass spectrometer was coupled online with an ultra-fast liquid chromatography system consisted of LC-20AD XR binary pump system, SIL-20AC XR autosampler, CTO-20AC column oven and DGU-20A 3R degasser (Shimadzu, Kyoto, Japan). Spectra were monitored in mode SIM (Selected Ion Monitoring) and processed using Shimadzu LabSolutions LC–MS software. The mass spectrometer was operated in negative ion mode with a capillary voltage of −3.5 V, a nebulizing gas flow of 1.5 l/ min, a dry gas flow rate of 12 l/min, a dissolving line temperature of 250 °C, a block source temperature of 400 °C, and a voltage detector of 1.2 V. The spectra were fully scanned from 50 to 2000 Da. 2.5. Evaluation of antioxidant activities 2.5.1. Ferric (Fe3+) reducing power The ability of samples to reduce iron was determined according to the method of Yıldırım, Mavi, and Kara (2001). A volume of 0.5 ml of each sample or small pieces of each film (10 mg), was mixed with 1.25 ml of potassium phosphate buffer (0.2 M, pH 6.6) and 1.25 ml of 1% potassium ferricyanide solution. The reaction mixtures were incubated for 20 min at 50 °C. After incubation, 0.5 ml of 10% trichloroacetic acid (TCA) was added and the reaction mixtures were then centrifuged for 10 min at 3000 rpm. Finally, 1.25 ml of the supernatant solution from each sample mixture was added to 1.25 ml potassium phosphate buffer and 0.25 ml of 0.1% ferric chloride. The absorbance of the resulting solutions was measured at 700 nm after 10 min of incubation. Three replicates were done for each test sample.

2. Materials and methods 2.1. Extraction of gelatin from grey triggerfish Skin from grey triggerfish (Balistes capriscus) was obtained from the local fish market of Sfax City, Tunisia. Skin was cut into small pieces (1 cm × 1 cm) and then soaked in 0.05 M NaOH (1:10 w/v). The mixture was stirred for 2 h and the alkaline solution was changed every 30 min. The alkaline-treated skins were then washed with distilled water until a neutral pH was obtained, and then soaked in 100 mM glycin-HCl buffer (pH 2.0) with a solid/solvent ratio of 1:10 (w/v). Pepsin was then added (5 units of pepsin /g of skin), for collagen hydrolysis, as described in Jellouli et al. (2011). Grey triggerfish skin gelatin (G) obtained was freeze-dried and then used for films preparation.

2.5.2. Antioxidant assay using the β-carotene bleaching method The prevention of β-carotene from bleaching was determined according to the method of Koleva, van Beek, Linssen, de Groot, and Evstatieva (2002). First, the emulsion of β-carotene/linoleic acid was freshly prepared by dissolving 0.5 mg of β-carotene, 25 μl of linoleic acid and 200 μl of Tween 40 in 1 ml of chloroform. The chloroform was then completely evaporated under vacuum in a rotatory evaporator at 50 °C and then 100 ml of distilled water were added. In the reaction tube, 2.5 ml of the β-carotene/linoleic acid emulsion was mixed with 0.5 ml of each sample or small pieces of each film (10 mg). Control tubes were prepared under the same conditions by adding 0.5 ml of water to the emulsion. The absorbance of each test tube was measured at 470 nm twice, before and after incubation for 1 to 2 h at 50 °C. Tests were carried out in triplicate and the antioxidant activity was evaluated in terms of β-carotene bleaching inhibition using the following equation:

2.2. Preparation of blood orange powders and their ethanolic extracts Blood orange peels were collected on March 2018 from the area of Beja (Tunisia), washed and dried in a convection oven at 80 °C during 2 h (Polin A511088/AL/3125, Verona, Italy). The dried peels were ground in a spice grinder (Black & Decker CBG100S Smartgrind, Maryland, USA), sieved through 250 μm sieve and the obtained powder, referring to the dried blood orange peels powder was stored at 25 °C until use. The powder (25 g) was Soxhlet-extracted using 300 ml of ethanol during 6 h to obtain dried orange peel extract (DOPE). Similarly, fresh peels, without drying, were used to prepare a fresh orange peel extract (FOPE), with the same manner as DOPE. The solvent (ethanol) was then evaporated under vacuum and the residual solvent was removed by flushing with nitrogen. Thereafter, extracts were freeze-dried to obtain DOPE and FOPE powder, kept in the dark at 4 °C until analysis.

β-carotene bleaching inhibition (%) = [1− (OD0 − ODt)/(OD0’− ODt’)] × 100

2.3. Total phenolic and flavonoid contents

Where OD0 and ODt are the absorbance of the test sample measured before and after incubation, respectively, and OD0’ and ODt’ are the absorbance of the control measured before and after incubation, respectively.

Total phenolic and flavonoid contents were measured in orange peel extracts as previously described (Dewanto, Wu, Adom, & Liu, 2002; Sun, Ricardo-da-Silva, & Spranger, 1998). Total phenolics content was expressed as mg gallic acid equivalents (GAE)/g of extract. Flavonoids content was expressed as mg quercetin equivalents (QE)/g of extract.

2.5.3. Free radical scavenging activity on 1,1-diphenyl-2-picrylhydrazyl (DPPH%) The DPPH%-radical scavenging activity was determined as described previously by Bersuder, Hole, and Smith (1998). A volume of 500 μl of sample or small pieces of each film (10 mg) were allowed to react with 2

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125 μl of 0.02% DPPH% solution (in ethanol) and 375 μl of ethanol. Blank tube was prepared in the same way, but with substituting the sample by distilled water. The reaction mixtures were incubated for 60 min in dark at room temperature and the reduction of DPPH% radical was measured at 517 nm. The test was carried out in triplicate and the DPPH%-radical scavenging activity was calculated as follows:

10 mg/ml) were dispersed in FFS and mixed at 25 °C until complete solubility. Films were obtained by casting 25 ml of FFS on Petri dishes (12 cm × 12 cm), dried at 25 °C at a relative humidity (RH) of 50% and then peeled off manually. Prior to characterization, all films were kept at 25 °C and 50% RH for at least 14 days. The thickness of films was measured using a digital thickness gauge (Schmidt, Control instrument). Ten random locations (from the center and close to the perimeter) were taken from each film sample, and the average was used in the calculations of transparency and mechanical properties.

Scavenging activity (%) = [(ODC + ODB − ODS)/ODC] × 100 Where ODC, ODB and ODS represent the absorbance of the control, the blank and the sample reaction solution, respectively.

2.7.2. Color, light transmission and transparency Color of the film samples was determined using a chromameter (CR200, Minolta, Japan) and expressed as L* (lightness/brightness), a* (redness/greenness) and b* (yellowness/blueness) values. The barrier properties of films against ultraviolet (UV) and visible light were measured at wavelengths ranged between 200 and 800 nm, using a UV–vis spectrophotometer. The transparency value of the film was calculated by the following equation:

2.5.4. Lipid peroxidation inhibition The inhibition of in vitro lipid peroxidation of each sample was determined by assessing their ability to inhibit the oxidation of linoleic acid in an emulsified model system. Briefly, the sample at different concentrations were dissolved in 2.5 ml of 50 mM phosphate buffer (pH = 7.0) and added to a 2.5 ml of 50 mM linoleic acid in ethanol (95%). The final volume was then adjusted to 6.25 ml with distilled water. The obtained mixture was incubated in a 10 ml tube with silicon rubber caps at 45 °C for 8 days in dark and the degree of oxidation was evaluated by measuring the ferric thiocyanate values. An aliquot of reaction mixture (0.1 ml) was mixed with 4.7 ml of 75% ethanol followed by the addition of 0.1 ml of 30% ammonium thiocyanate and 0.1 ml of 20 mM ferrous chloride solution in 3.5% HCl. After stirring for 3 min, the degree of color development was measured at 500 nm. αtocopherol was used as reference and control reaction was conducted without sample. The percentage of oxidation inhibition was expressed as follows:

Transparency value = − log T600/e where T600 is the fractional transmittance value at 600 nm and e is the film thickness (mm). The greater transparency value represents the lower transparency of the film. 2.7.3. Fourier transform infrared spectroscopy Fourier transform infrared (FTIR) spectra of different films were determined using a PerkinElmer infrared spectrometer equipped with an attenuated total reflection (ATR) accessory. Films were analyzed with a 32 scans per minute at a resolution of 4 cm−1 in the wavenumber region between 400 cm−1 and 4000 cm−1.

Lipid peroxidation inhibition (%) = [1 – (ODS / ODNC)] × 100 Where ODS and ODNC represent the absorbance of the sample and the negative control tubes, respectively.

2.7.4. Mechanical properties Tensile strength (TS) and elongation at break (EAB) point of film samples were determined using a texture analyzer (Lloyd Instrument, Hampshire, UK). Rectangular film samples (5 cm × 2.5 cm) were prepared using a precision standard cutter (Thwing-Albert JDC Precision Sample Cutter, USA) in order to get pieces with an accurate width and parallel sides throughout the entire length. The film samples were clamped and deformed under tensile loading using a 300 N load cell with a speed of 50 mm/min, until films’ breaking. TS (MPa) and EAB (%) were determined from the stress-strain curves, analyzed six times for each film sample.

2.6. Antibacterial activity 2.6.1. Microbial strains Seven Gram-negative and Gram-positive pathogenic bacteria strains were used for the assessment of antibacterial activity in the extracts: Micrococcus luteus (ATCC 4698), Staphylococcus aureus (ATCC 25923), Bacillus cereus (ATCC 11778) Pseudomonas aeruginosa (ATCC 27853), Salmonella enterica (ATCC 43972), Listeria monocytogenes (ATCC 19117) and Enterobacter sp. 2.6.2. Agar diffusion method The antibacterial activity assay was performed referring to the method described by vanden Berghe and Vlietinck (1991). Microorganism’s culture suspensions (200 μl), containing 106 colony forming units (CFU/ml) of bacteria cells, were spread on the surface of LuriaBertani (LB) agar medium. Then, 60 μl of each extract (5 and 10 mg/ml) were loaded into wells punched in the agar layer. Before incubation, all plates were stored in the dark at 4 °C for 2 h, to allow the diffusion of the extract. At the end of the incubation time, the antibacterial activity was detected by the presence of measurable clear inhibition zone around the well. Negative control was prepared using sterile water. Antimicrobial activity was evaluated by measuring the growth inhibition zone (diameter expressed in millimeters) present around the well.

2.7.5. Thermal properties Prior to experiments, samples were kept at 25 °C and 0% RH (silica gel) for 48 h to obtain the maximum dehydrated film samples. Conditioned films (5 mg) were then hermetically sealed in specific aluminum pans (PerkinElmer®) and scanned using a differential scanning calorimeter DSC (Mettler Toledo Star). DSC measurements were carried twice for each film. 2.7.6. Contact angle measurements and surface properties of films Surface wettability of films was evaluated from the contact angle measurements between films surface and water, using a goniometer (Krüss Drop Shape Analyzer, Germany) equipped with image analysis software (Krüss Advance, version 1.4.1.2) and via the sessile drop method, as described by Karbowiak, Debeaufort, Champion, and Voilley (2006).

2.7. Film preparation and characterization 2.7.1. Film preparation and thickness To prepare film-forming solution (FFS), grey triggerfish skin gelatin was dissolved in distilled water to achieve a final concentration of 3% (w/v). As plasticizer, glycerol was added to the gelatin solution at a level of 15% (w/w) and then gently mixed at 40 °C for 30 min to ensure total homogenization. For the bioactive films, selected FOPE (5 or

2.7.7. Release of FOPE The maximal extract (FOPE) absorbance value was determined from the absorbance spectrum of the pure extract in water/ethanol solution. To assess FOPE release through the gelatin film, a film sample of about 200 mg (˜5 × 5 cm2) was fully immersed in 100 ml of distilled water/ 3

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Table 1 Yield and chemical characteristics of FOPE and DOPE.

DOPE FOPE

Extraction yielda

Total phenolic content

31.2 ± 0.24 25.3 ± 0.07

8.68 ± 0.87 10.07 ± 0.62

*

Table 2 LC-ESI-MS analysis of the DOPE and FOPE. Flavonoids content

**

a

Compounds

b

Retention time (min)

Formula

5.57 ± 0.09 6.30 ± 0.42 1 2 3 4 5 6 7

FOPE and DOPE represent fresh and dried orange peel extracts, respectively. a g/100 g of dried mass. * mg gallic acid equivalents (GAE)/g of extract. ** mg quercetin equivalents (QE)/g of extract.

ethanol (1:1, v/v) solution, under a constant rotation speed of 50 rpm at room temperature (25 ± 1 °C) during 96 h. The amount of the extract released in the liquid medium was determined at regular intervals of time by UV–vis spectrophotometer.

8 9 10

2.8. Statistical analysis

11

All analytical results were expressed in mean ± standard deviation (SD). One-way analysis of variance was conducted using SPSS software, ver. 17.0. A difference was considered statistically significant at p < 0.05.

12 13 14 15 16 17 18

3. Results and discussion 3.1. Effect of blood orange peel drying pretreatment on the physic-chemical and biological properties of the extracts

Quinic acid Protocatchuic acid Caffeic acid Epicatechin* p-coumaric acid trans-frulic acid Hyperoside (quercetin-3-ogalactoside* Rutin* Luteolin-7-Oglucoside* 3,4-di-Ocaffeoyquinic acid Apegenin-7-Oglucoside* 4,5-di-Ocaffeoyquinic acid Quercetin Naringenin* Apegenin* Luteolin* Cirsiliol* Cirsilineol*

Mass (g/ mol)

Concentration (μg/g extract) DOPE

FOPE

2.308 8.159 16.658 18.85 22.877 24.906 25.92

C7H12O6 C7H6O4 C9H8O4 C15H14O6 C9H8O3 C10H10O4 C21H20O12

192 154 180 290 164 194 464

3813.55 9.89 4.01 – 0.69 74.52 16.21

4759.31 28.33 4.18 0.74 19.59 78.09 15.33

25.233 26.142

C27H30O16 C21H20O11

610 448

108.25 2.18

108.70 1.40

26.763

C25H24O12

516

1.56

50.45

28.11

C21H20O10

432

3.21

2.15

28.634

C25H24O12

516

27.48

20.75

33.403 35.374 35.976 36.402 36.759 40.066

C15H10O7 C15H12O5 C15H10O5 C15H10O6 C17H14O7 C18H16O7

302 272 270 286 330 344

4.05 47.71 0.11 6.96 8.50 1.4

25.49 41.71 0.26 7.80 30.43 2.65

a The numbering refers to elution order of compounds from an Aquasil C18 column. b Identification was confirmed using 32 authentic commercial standards. * Flavonoids. FOPE and DOPE represent the extracts from fresh and dried orange peel, respectively.

The extraction yields, the total phenolic and flavonoid contents are shown in Table 1. The extraction yield of the DOPE, prepared from the dried blood orange peels, was of 31.2% (w/w), which was significantly higher than that prepared from fresh peels (FOPE) (25.3%). Phenolic compounds are primarily responsible for antioxidant properties and several research have been developed to find natural antioxidants in cheap plant raw materials (Lachos-Perez et al., 2018). Results of Table 1 showed that there was a significant difference between the total phenolic contents in both extracts, which were of about 8.68 and 10.07 mg GAE/g of DOPE and FOPE, respectively. In addition, the flavonoid content in DOPE was about 5.57 mg QE/g of extract, which was lower than that of FOPE (6.30 mg QE/g of extract), indicating that the drying pretreatment of orange peels before the extraction may affect the phenolics’ concentration. These results are in agreement with those of M’hiri, Ioannou, Mihoubi Boudhrioua, and Ghoul (2015) who showed that microwave, ultrasound or thermal heat flow pretreatments made flavonoids unstable and easily degradable. Espinosa-Pardo, Nakajima, Macedo, Macedo, and Martínez (2017) extracted phenolic compounds from orange processing by-products by supercritical CO2 using ethanol as co-solvent and they found that the total phenolic compounds content was about 0.57 mg GAE/g of dry peel. In another work, Hegde, Agrawal, and Gupta (2015) used 50% (v/ v) aqueous methanol and acidified aqueous methanol to extract polyphenolic compounds from orange peel, and reported total phenolic compounds content ranged from 1.4 to 2.6 mg GAE/ g. On the other hand, Hayat et al. (2010) and Ahmad and Langrish (2012) demonstrated that drying peels at medium temperatures facilitate the release of phenolic compounds during extraction, while the use of temperatures up to 80 °C will accelerate their degradation (M’hiri et al., 2015). Orange peels are composed from a variety of polyphenols that include anthocyanins, flavonoids, tannins and procyanidins (Karoui & Marzouk, 2013). Table 2 shows the results of LC-ESI-MS analysis of DOPE and FOPE. Data revealed that the quinic acid was the major compound among the total polyphenols (4759.31 and 3813.55 μg/g of FOPE and DOPE, respectively), followed by rutin (about 108 μg/g in both extracts), trans-ferulic acid (78.09 and 74.52 μg/g extract for FOPE and DOPE, respectively), naringenin (41.71 and 47.71 μg/g of FOPE

and DOPE, respectively) and 4,5-di-O-caffeoylquinic acid (20.75 and 27.48 μg/g of FOPE and DOPE, respectively). However, FOPE contained higher contents in 3,4-di-O-caffeoyquinic acid, cirsiliol, protocatchuic acid, quercetin, and p-coumaric acid, compared to DOPE. The comparison between the compositions of the two extracts prepared with orange peel markedly showed that the drying step affected the concentrations of some phenolic compounds. Ozturk et al. (2018) and Lachos-Perez et al. (2018) reported, similarly, the presence of phenolic acids including gallic acid, p-coumaric acid, ferulic acid, caffeic acid, trans-cinnamic acid, flavone and thymol in orange peel extract. Additionally, it has been reported that quantitative determination of gallic acid, ferulic acid and p-coumaric acid are the most abundant phenolic compounds in Citrus aurantium peel (Karoui & Marzouk, 2013). However, among the identified flavonoids, hesperidin was the most abundant, corresponding to the typical flavonoid composition of citrus peel (Rafiq et al., 2016). Commonly, several authors have agreed that the highest contents of phenolic acids in citrus peels are the caffeic, ferulic, coumaric and sinapic acids (Rafiq et al., 2016; Robbins, 2003). The obtained phenolic profiles expected an important antioxidant potency of both extracts. In fact, the hydroxyl groups (eOH) in quinic acid, found the major compound in FOPE and DOPE, is capable to prevent or slow-down the oxidation processes, besides its antiviral, antibacterial and antifungal activities. The antioxidant activities of the orange peel extracts were investigated by using four methods: DPPH% radical-scavenging, Fe3+ reducing power, antioxidant assay using the β-carotene/linoleate model system and lipid oxidation inhibition activities (Fig. 1). The results of the scavenging effect of extracts on DPPH% radicals (Fig. 1A) showed an increased activity with a dose-dependent manner, with no significant difference between both extracts above 3 mg/ml. The IC50 values of FOPE and DOPE were about 0.7 and 1.05 mg/ml, respectively, which were comparable to that obtained by Barrales et al. (2018) for orange peel extract (IC50 = 11.18 μg/ml). The ferric 4

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Fig. 1. Antioxidant activities of extracts. (A) DPPH%-scavenging activity (%); (B) Fe3+ reducing antioxidant power (OD 700 nm); (C) β-carotene bleaching inhibition (%); (D) Lipid oxidation inhibition (%).

reducing power measures the reducing ability of Fe3+ ions, giving idea about the electron donation ability (Khantaphant & Benjakul, 2008). The Fe3+ reducing power of extracts at different concentrations is presented in Fig. 1B. Based on absorbance values, the activity increased with increasing concentration between the range of 0.1 and 5 mg/ml extracts. FOPE was more effective than DOPE, reaching a maximal absorbance value of 1.2 at 5 mg/ml. In a similar study, Atrooz (2009) demonstrated that the seed extract of C. sinensis exhibited antioxidant activity using reducing power and DPPH% radical-scavenging assays. Furthermore, the antioxidant activity of extracts was determined as % of β-carotene bleaching inhibition in an emulsified linoleic acid model system (Fig. 1C). From the obtained results, it can be clearly observed that FOPE prevented more effectively the β-carotene from bleaching than DOPE, by donating hydrogen atoms to the hydroxyl radicals of the oxidized linoleic acid. Indeed, the IC50 values of FOPE and DOPE were about 0.95 and 2.12 mg/ml, respectively. Moreover, FOPE and DOPE showed an important ability of linoleic acid protection against oxidation, which increased with increasing the extract’s concentration (Fig. 1D). During the first 4 incubation days, FOPE showed higher linoleic acid protection activity than DOPE, while their activities remained similar after 6 days. In this context, Oboh and Ademosun (2012) reported that the phenolic extract from citrus peel showed radical DPPH% scavenging activity, %OH scavenging activity, Fe2+ chelating power and lipid peroxidation inhibition in pancreas, with respective IC50 values of 1, 4, 0.48 and 0.143 mg/ml. Previous works reported positive correlation between the total phenolic contents and antioxidant activities in plant extracts (Shofinita, Feng, & Langrish, 2015; Skotti, Anastasaki, Kanellou, Polissiou, & Tarantilis, 2014). In this regard, Karoui and Marzouk (2013) found that rutin and naringenin dominate the list of identified flavonoids in Tunisian bitter orange (C. aurantium L.) extracts, known by various beneficial biological activities to the human health. In addition, Zang et al. (2000) demonstrated the direct effect of p-coumaric acid in reducing

free radicals, lowering cholesterol level, and inhibiting the low-density lipoprotein cholesterol oxidation. On the other hand, ferulic acid demonstrated anticancer and antidiabetic activities and protective capacity from cardiovascular diseases (Srinivasan, Sudheer, & Menon, 2007). On the other hand, the antimicrobial activities of the extracts (5 and 10 mg/ml) against seven Gram-positive and Gram-negative bacteria strains were evaluated by determining the inhibition zones (mm) on solid medium (Table 3). The extracts presented an interesting antibacterial potential against all investigated micro-organisms. In fact, the values of the inhibition zones of the tested strains varied between 9.0 (P. aeruginosa) and 39.5 mm (S. enterica). S. aureus was the most sensitive strain against the effect of FOPE (36.0 mm) and DOPE (37.5 mm). Overall, data demonstrated that FOPE was more effective than DOPE against all Gram-positive and Gram-negative bacteria tested. Naila, Table 3 Antimicrobial activities of DOPE and FOPE against Gram-positive and Gramnegative bacteria strains. Strains

Inhibition zone diameters (mm) FOPE (5 mg/ml)

M. luteus Enterobacter sp. S. aureus P. aeruginosa B. cereus L. monocytogenes S. enterica

29.0 25.0 29.0 17.0 26.0 31.0 26.5

± ± ± ± ± ± ±

0.5 1.5 1.5 1.5 2.0 1.5 1.0

FOPE (10 mg/ml) b b b a b a b

34.0 30.0 36.0 19.0 32.0 33.5 39.5

± ± ± ± ± ± ±

1.5 0.2 1.0 1.0 2.0 2.0 1.0

a a a a a a a

DOPE (5 mg/ml)

DOPE (10 mg/ml)

23.0 ± 1.0 a 26.5 ± 2.0 a 25.0 ± 0.5 b 9.0 ± 1.0 a 24.0 ± 2.0 a 26.5 ± 2.0 a 25 ± 1.0 a

24.5 28.0 37.5 12.0 27.0 28.0 23.5

± ± ± ± ± ± ±

0.5 2.0 2.0 1.5 1.5 0.5 2.0

a a a a a a a

FOPE and DOPE represent extract from fresh and dried orange peel, respectively. Different letters in the same line within different concentrations indicate significant difference (p < 0.05). 5

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(amide II) at 1490 cm−1, and CeN stretching (amide III) at 1041 cm−1 (Uranga et al., 2018). The main absorption bands of glycerol appear at the 900–1050 cm−1 region and they are related to the vibrations of CeC and CeO bands (Uranga et al., 2018). Phenolic compounds showed diverse absorption bands due to the presence of a carboxylic group at about 1600–1700 cm−1, which cause a modification of the gelatin amide I band, and the absorption bands of the hydroxyl groups. Additionally, increasing FOPE concentration led to changes in the bands’ position of amide I and amide II, as shown in Table 5. This might be due to the promotion of the cross-linking reaction between gelatin, glycerol and phenolic acids. In this context, Uranga et al. (2018) reported the interactions between amine groups of fish gelatin and carboxylic group of gallic acid, through the FTIR analysis.

Table 4 Thickness and thermal and mechanical properties of films. Tg (°C) GF GF-FOPE (5 mg/ ml) GF-FOPE (10 mg/ ml)

Thickness (μm) a

69.59 70.25

76.26 ± 0.01 75.09 ± 0.21

71.90

76.36 ± 0.31

b

a

TS (MPa)

EAB (%)

6.23 ± 0.25 6.53 ± 0.12

a

6.15 ± 0.40

a

a

10.97 ± 1.10 15.36 ± 2.19

c

20.25 ± 0.56

a

b

TS: Tensile strength; EAB: Elongation at break. GF and FOPE indicate gelatin film and fresh orange peel extract. All measurements were performed at 25 °C and RH = 50%. Different letters in the same column indicate significant difference (p < 0.05).

Nadia, and Zahoor (2014) showed that nanoparticles, synthesized by mixing silver nitrate solution with C. sinesis extract, displayed great antibacterial activity against B. subtilis, S. aureus and E. coli. It is worth pointing out that orange peel extracts contain compounds (phenolics and flavonoids) with good antioxidant and antibacterial activities and having wide spectra of action, either by interrupting the oxidation reaction with different ways, or by inhibiting the growth of a great number of food spoilage bacteria. Of particular, FOPE was found more effective than DOPE, which promotes its use as a bioactive molecule to be incorporated in food packaging materials, e.g. the grey triggerfish skin gelatin in this study.

3.2.2. Color, light transmission and transparency of films Color and light transmission parameters of films are presented in Table 6. Results showed that the incorporation of FOPE significantly affected the color of the film surface (p < 0.05), by decreading L* values and inceasing a* and b* values. In fact, the addition of FOPE at 5 or 10 mg/ml significantly (p < 0.05) reduced film lightness from 90.57 to 85.02 and 62.65, respectively. High b* values of films indicated that they got yellow color after FOPE addition. These variations of films’ color are mainly caused by the natural coloured pigments present in the extract (orange color). In this context, Adilah et al. (2018) reported that films incorporated with mango peel extract showed yellowish color, comparing to control gelatin film. The incorporation of the extract in FG did not markedly changed the transmittance values in the UV–vis light region, showing a slight increment of these values for visible light between 400 and 600 nm (Table 6). Results of films’ opacity showed that GF was the lightest, while the incorporation of FOPE increased the darkness of gelatin film, due to the orange-colored pigments in the extract that absorb at this visible range, affecting therefore the opacity of the FOPE-added films (Bonilla & Sobral, 2016).

3.2. Films characterization 3.2.1. Mechanical, thermal, surface and structural properties Results of thickness, tensile strength (TS), and elongation at break (EAB) of triggerfish gelatin films (GF), incorporated or not with FOPE are shown in Table 4. No significant variations in thickness and TS values between all films were observed (p ≥ 0.05). However, the incorporation of 10 mg/ml FOPE in the gelatin film increased twice the elongation at break (20.25 ± 0.56%), compared to the control GF (10.97 ± 1.10%). In the same context, Bitencourt, Fávaro-Trindade, Sobral, and Carvalho (2014) showed a significant increase in EAB after the incorporation of diverse concentrations of ethanolic extract of Curcuma in gelatin based films. Similarly, Bonilla and Sobral (2016) demonstrated that the incorporation of cinnamon and guarana extracts increased the EAB, two folds, when compared to control gelatin film. Changes may be due to the interactions between the phenolic compounds (present in the extract) and gelatin poly-peptides. On the other hand, the addition of the extract increased slightly the glass transition temperature (Tg) of the gelatin film to reach 70.25 and 71.90 °C, after the addition of 5 and 10 mg/ml FOPE (Table 4), mainly due to the intermolecular interactions between gelatin and phenolic compounds/ floavonoids. DSC results indicated also that gelatin, glycerol and orange peel extract were completely miscible, as revealed by the unique endothermic peak recorded in the thermograms. The surface-tension characterization through the measurement of contact angle (θ), between water and films’ surface, is one of the key properties of packaging materials, giving idea about their wettability. Fig. 2 shows the water contact angle (WCA) value through 60 s. Although the initial WCA value of GF was found to be slightly higher than those of films incorporated with FOPE, all values indicated about the hydrophobic character of films’ surface, as the WCA values were higher than 90° in all the samples. In addition, after 60 s of water drop deposition, the WCA values decreased in the GF, compared to the values at t = 0 s, while this decrease was significantly reduced after FOPE addition, indicating the enhancement of films’ resistance against wettability. For better understanding the structure of the films, FTIR analysis was carried out to analyze the interactions among the components of the film (Table 5). The most characteristic bands of gelatin film are related to C]O stretching (amide I) at 1658 cm−1, NeH bending

3.2.3. Antioxidant activity of films Antioxidant packaging are the most favorite categories among active packaging thanks to their promising role in extending food products shelf-life (Benbettaïeb, Chambin, Karbowiak, & Debeaufort, 2016; Bonilla & Sobral, 2016; Jridi et al., 2014, 2013). The antioxidant power of the different films was measured using three tests and the results are presented in Table 6. The control GF (without FOPE) showed the lowest antioxidant activities (0.12, 12.68% and 20.35% for reducing power, βcarotene bleaching inhibition and DPPH radical-scavenging activities, respectively). Whatever the test used, the increase of FOPE concentration significantly increased the antioxidant activity (p < 0.05). In fact, FG incorporated with 10 mg/ml FOPE, showed the highest reducing power, β-carotene bleaching inhibition and DPPH radical-scavenging activities, which were of 1.38, 95.76% and 99.7%, respectively. These results were not surprising as FOPE has demonstrated its in vitro antioxidant potential as an hydrogen/electron donating agent or by chelating metals, resulting therefore in the interruption of the oxidation chain reaction. The comparison between the antioxidant activities of the FOPEadded films and the free extract showed that the bioactivity of the extract decreased following its incorporation in the film matrix. This could be explained by the cross-linking of phenolics and flavonoids in the film forming gelatin network. 3.2.4. Release behavior of FOPE The release kinetic of substances encapsulated in biomaterials is a crucial parameter that must be controlled in industrial applications, as it gives idea about the time attributed to completely deliver the bioactive substance across the film (Benbettaïeb et al., 2016). To better understand the mechanism of release of orange peel extract, the kinetics of release of FOPE from FG was carried out and results are 6

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Fig. 2. Shape behavior (t = 0 s) and kinetics of water droplets deposited on the surface of films as a function of time; measurements were done at 25 °C and RH = 50%.

Table 5 Fourier Transform infrared spectra (FTIR) of composite films. Wavenumbers (cm−1)

Amide A

Amide B

Amide I

Amide II

Amide III

GF GF-FOPE (5 mg/ml) GF-FOPE (10 mg/ml)

3297 3269 3278

2996 2991 2968

1658 1652 1655

1490 1458 1478

1041 1040 1040

GF: Gelatin film, FOPE indicates extract from fresh orange peel.

presented in Fig. 3. During the first 24 h, the release of extract from the gelatin film network began slowly, which could be due to the interaction between amine groups of fish gelatin and carboxylic group of gallic acid resulting in great bounding affinity between the bioactives and the gelatin polymer. Then, the release speed increased between 24 and 36 h of reaction, showing a sustained drug release profile with a quasiFickian diffusion mechanism (n-value less than 0.5). This mechanism indicated that gelatin was hydrated, swelled and then the drug diffused through the swollen matrix system. Thereafter, beyond 72 h, the release reached a stability stage, which slowed down the kinetic release.

Fig. 3. Cumulative release of FOPE from the gelatin film matrix. The non-added gelatin film (FG) was used as control.

films demonstrated the presence of interactions between the gelatin film and the phenolic molecules. These interactions affected FOPE release kinetic, which was prolonged up to 96 h. Overall, this work gives a new strategy of Citrus peel utilization through development of edible packaging with good biological properties.

4. Conclusion The present research studied the effect of drying on the quality of blood orange peel extracts and underlined the successful addition of the active extract in Grey triggerfish gelatin film. Physicochemical, mechanical and antioxidant properties of the FOPE-added films were significantly enhanced, compared to FG. Structural and thermal analysis of

Declaration of interest The authors declare no conflicts of interest. The authors alone are

Table 6 Light transmission, opacity, color, and antioxidant properties of films.

Wavelength (nm)

Opacity Color

Antioxidant activities

200 280 350 400 500 600 700 800 L* a* b* Reducing power (A700) β-carotene bleaching inhibition (%) DPPH radical-scavenging activity (%)

GF

GF-FOPE (5 mg/ml)

GF-FOPE (10 mg/ml)

0.01 0.01 28.36 49.7 69.4 82.6 88.4 90.5 1.09 90.57 ± 0.26 a −0.36 ± 0.01 c 0.35 ± 0.03 c 0.12 ± 0.01 c 12.68 ± 1.68 c 20.35 ± 0.20 c

0.01 0.00 26.32 48.6 67.3 80.2 89.5 90.4 1.28 85.02 ± 0.10 b 6.26 ± 0.52 b 2.10 ± 0.11 a 0.89 ± 0.11 b 67.95 ± 3.65 b 76.9 ± 2.35 b

0.01 0.01 25.25 49.2 68.1 80.0 89.6 90.6 1.27 62.65 ± 0.05 c 8.32 ± 0.10 a 3.68 ± 0.23 a 1.38 ± 0.11 a 95.76 ± 0.19 a 99.7 ± 1.74 a

Values of light transmission were measured at 25 °C and RH of 50% and expressed in %. Different letters in the same line indicate significant difference (p < 0.05). Opacity = -log (Transmission) / Thickness. GF: Gelatin film, FOPE: extract from fresh orange peel. 7

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responsible for the content and writing of this paper.

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