Intelligent and active composite films based on furcellaran: Structural characterization, antioxidant and antimicrobial activities

Food Packaging and Shelf Life 22 (2019) 100405

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Intelligent and active composite films based on furcellaran: Structural characterization, antioxidant and antimicrobial activities

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Ewelina Jamróza, Piotr Kulawikb, Pavel Kopelc,d, Radka Balkováe, David Hynekc,d, ⁎ Zuzana Bytesnikovac,d, Milica Gagicc, Vedran Milosavljevicc,d, Vojtech Adamc,d, a

Institute of Chemistry, University of Agriculture, Balicka Street 122, PL-30-149 Cracow, Poland Department of Animal Products Processing, University of Agriculture, Balicka Street 122, PL-30-149 Cracow, Poland c Department of Chemistry and Biochemistry, Faculty of AgriSciences, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic d Central European Institute of Technology, Brno University of Technology, Purkynova 123, CZ-612 00 Brno, Czech Republic e Institute of Materials Chemistry, Faculty of Chemistry, Brno University of Technology, Purkynova 118, CZ-612 00 Brno, Czech Republic b

A R T I C LE I N FO

A B S T R A C T

Keywords: Furcellaran Tea extracts Nanoparticles Antioxidant Antimicrobial Food packaging

Intelligent and active films were prepared using furcellaran (FUR). The FUR films were modified with various antibacterial material including natural extracts from green tea (GTE) and yerba mate (YM) and synthetized selenium (SeNPs) and zinc oxide (ZnONPs) nanoparticles. The bionanocomposite films were characterized by Xray diffraction, SEM, TGA and UV–vis spectroscopy. The structural characteristics confirmed successfully formation of FUR films in the presence of tea extracts and NPs. SEM analysis showed smooth and compact surface morphology for FUR, YM and GTE films. Structure of composite films with NPs becomes less homogeneous, with some aggregations or agglomerates of NPs. The addition of both NPs into the films increases their thermal stability, while the incorporation of ZnONPs and YM increased UV-light barrier properties. Films presented different physical properties depending on the composition of the active compounds. The addition of ZnONPs caused the reduction in solubility of prepared films. On the other side, FUR films with the tea extracts show great antioxidant activity based on the ABTS test (inhibition of 37.3% for YM films and of 67.6% for GTE films). However, the FUR films with SeNPs had the highest antimicrobial activity against S. aureus, MRSA and E.coli, with inhibition zone diameters of 21.8 mm, 26.6 mm and 26.7 mm, respectively. The carp spoilage test was done to evaluate possible application of the films as intelligent packages, and color change indicated the film could be used as a sensor in the food industry. The results indicate that composite films based on FUR can be used as smart packaging showing good antioxidant and antimicrobial properties for food packaging applications.

1. Introduction Smart packaging, including intelligent and active materials, offers safe and improved quality of packaged food products. Active packaging is defined as package system that incorporates various antimicrobial or antioxidant compounds. Such compounds can be release on the surface or absorb into the packaged food to extend the shelf-life or to improve the condition of the packaged food (EC Regulation No 450/2009). Active packages usually improve the antimicrobial and/or antioxidant properties resulting in shelf-life extension of the packed food product. Meanwhile, the intelligent packaging is a material that monitors the packaged food or the environment surrounding the food. Intelligent packaging includes packaging indicators, which usually provide

qualitative information through visual colorimetric changes. These indicators can be included into packaging material or attached to the inside or outside of the packaging (Yoshida, Maciel, Mendonca, & Franco, 2014). The challenge is to develop active materials that prolong the shelf life of food (active packaging) and transmit the information about quality of the food product (intelligent packaging) at the same time (Realini & Marcos, 2014). Due to the “clean label” trend, natural components, such as plant extracts and or essential oils, become the main replacements for synthetic adjectives in active materials (Asioli et al., 2017; Poojary et al., 2017). Addition of natural components to films prepared from natural products (furcellaran, chitosan, alginate or cellulose) improves the antimicrobial/antioxidant properties of films and their use in food

⁎ Corresponding author at: Department of Chemistry and Biochemistry, Faculty of AgriSciences, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic. E-mail address: [email protected] (V. Adam).

https://doi.org/10.1016/j.fpsl.2019.100405 Received 21 December 2018; Received in revised form 21 September 2019; Accepted 26 September 2019 2214-2894/ © 2019 Elsevier Ltd. All rights reserved.

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on the properties of FUR films. Therefore the aim of our study was to prepare simple intelligent or/and active bionanocomposite films using acceptable by consumers and non-toxic compounds including FUR, GTEand YM extracts or nanoparticles (SeNPs and ZnONPs). Due to our study is focused on physical, bioactive and intelligent properties of FUR films prepared in multiple combination of tea extracts and NPs. NPs were selected due to their potential bioactive properties and low toxicity. By the addition of tea extracts, we wanted to enhance their bioactive properties using a well-known, safe, cheap and acceptable by the consumer’s natural compounds. We have also chosen tea extracts due to the presence of their pigments which allowed the color change in different pH.

preservation and packaging. Using of films prepared from mentioned natural products represent a promising candidate for the safe and controlled foodstuff packaging due to excellent biocompatibility, biodegradability, low density, high loading capacity, high colloidal stability and the absence of toxicity (Fang, Zhao, Warner, & Johnson, 2017). Furcellaran (FUR) represents excellent natural derived material which can be used for the preparation of new generation of antimicrobial or antioxidant biofilms. FUR is a sulphated, negative charged polysaccharide obtained from Furcellaria lumbricalis. It is composed from the fragment of (1 → 3) β-D-galactopyranose with a sulphate group at C-4 and (1 → 4) 3,6-anhydro-α-D-galactopyranose (Laos, Brownsey, & Ring, 2007). Furcellaran is approved by the European Commission (2011) as the food additive with the number E 407. This polysaccharide easily interacts with starch, gelatin and essential oils creating active biopolymer films (Jamroz, Konieczna-Molende, & Para, 2017). The properties of biopolymer films can be improved by the addition of active ingredients such as plant extracts, essential oils or nanomaterials (Jamroz, Juszczak, & Kucharek, 2018). The incorporation of nanoparticles (NPs) into biofilms is a promising method for food preservation. From a wide group of NPs, The Food and Drug Administration (FDA) of USA considered ZnO as healthy safe material (21CFR182.8991). ZnO NPs exhibits ordered crystalline structure, large specific surface area, UV barrier and thermo-mechanical properties, which makes them a possible functional nanofillers in biopolymers films (Arfat, Benjakul, Prodpran, Sumpavapol, & Songtipya, 2014; Ejaz, Arfat, Mulla, & Ahmed, 2018). On the other side the selenium nanoparticles (SeNPs) are second type of NPs with good potential to be used as nanofillers due to their excellent antimicrobial, free radical scavenging properties, lower toxicity, higher biological activity and good bioavailability compared to another selenium compounds (Nonsuwan, Puthong, Palaga, & Muangsin, 2018). However, comparing with ZnO NPs the use of SeNPs as antimicrobial material in food preservation is still under consideration. On the other side the application of ZnO and Se-NPs in animal production has been already reported, indicating the absence of toxicity when they are administered in higher doses to animals (Kim et al., 2014; Zhang, Wang, Yan, & Zhang, 2005). Therefore, it is important to reduce the levels of used NPs to the minimum, while maintaining their bioactive properties. One of the possibly approach is to use combination of well-studied and acceptable by the consumers natural plant extracts with NPs, which can further enhance the bioactive properties of the films allowing reducing of the final concentration of NPs in the film. This can have the important role in the minimizing of the NPs potential toxicity. On the other side, it is well known that tea extracts exhibit antioxidant activity, which could extend the shelf-life of foods (Yang, Lee, Won, & Bin Song, 2016). The application of tea extracts especially become valuable knowing that green tea (Camellia sinensis L.) is one of the most important crops used within beverage industry. Its global production is estimated as above 5.3 million tons produced on over 3.5 million ha of land. Green tea, produced from fresh unfermented tea leaves accounts for around 15% of global tea production. The benefits of green tea come from phenolic compounds, which had strong antioxidant and antimicrobial activity (Karak et al., 2017; Weerawatanakorn et al., 2015; Zhang et al., 2019). Similarly as the green tea, yerba mate (Ilex paraguariensis A. St. Hil.) is a plant that naturally grows in Brazil, Argentina, Uruguay and Paraguay (Bracesco, Sanchez, Contreras, Menini, & Gugliucci, 2011). Yerba mate is source of bioactive compounds, such as phenolics or methylxanthines. Usually, it is consumed for its wellknown health benefits and strong antioxidant properties (Arrieta, Peponi, Lopez, & Fernandez-Garcia, 2018; Gómez-Juaristi, MartínezLópez, Sarria, Bravo, & Mateos, 2018; Riachi et al., 2018). Both green tea (GTE) and yerba mate (YM) extracts have been reported as good pH indicators in FUR films, showing distinct color change of films when subjected to various pH (Jamróz, Kulawik, Guzik, & Duda, 2019). Due to and to the best of our knowledge, there is no report on the combined effect of green tea or yerba mate extracts and nanoparticles

2. Materials and methods 2.1. Materials The chemicals and the solvents including ZnONPs were provided by Sigma-Aldrich (St. Louis, MO, USA) in ACS purity. The other materials used were: FUR (Est-Agar AS, Karla village, Estonia), the composition of FUR was: carbohydrates 79.61%; protein 1.18%; fat 0.24%; green tea (Yunnan, China) and yerba mate Amanda (type Despalada, La Cachuera SA, Argentina). Millipore Direct-Q 3UV purification system (EMD Millipore, MO, USA) was used for purification of water employed for all measurements. 2.2. Synthesis of selenium nanoparticles (SeNPs) The SeNPs were prepared according to the previously published papers (Hegerova et al., 2017; Jamroz, Kopel et al., 2018). 0.105 g of Na2Se03.5H2O was dissolved in 80 mL water. 110 μl of 3-mercaptopropionic acid (MPA) was added dropwise and then the pH 7 of the solution was adjusted with 1 M NaOH. The mixture was stirred for 2 h until a slightly orange colour was obtained. Then 10 ml of 1% carboxymethylcellulose was added and water up to 100 ml. 2.3. GTE and YM extraction Green tea and yerba mate water extract solutions were prepared by mixing dried leaves with distilled water (1 g/100 ml H2O) controlled at 90o C for 20 min. The water extracts were filtered and used in films production. The yield of YM and GTE was 13.79% ± 0.58 and 30.2% ± 1.1, respectively. 2.4. Preparation of composite films The FUR films are consisted of furcellaran (1 wt. %), glycerol as plasticizer (0.5 wt.%) and distilled water (98.5 wt.%). The films with GTE and YM had the same concentration of FUR and glycerol except of 10 and 20 wt. % of water was replaced with the extracts. The films with NPs, had the same concentration of FUR and glycerol except of 1 wt. % of water was replaced with solution of each NPs. The solution was mixed with constant stirring at 40 °C for 30 min. Further, the film forming solutions were poured into polyester Petri dishes (Φ =90 mm) then dried for 2 d under fume hood at room temperature. 2.5. Characterization of composite films 2.5.1. Particles size analysis and ζ-potential Size and ζ-potential of FUR, GTE, YM, SeNPs and ZnONPs were measured by Zetasizer Nano ZS (Malvern, UK), with the detection angle of 173o. Each value was obtained as an average from three runs with at least 20 measurements. 2.5.2. Scanning electron microscopy (SEM) MIRA3 LMU instrument (Tescan, Brno, Czech Republic) was used. 2

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2.5.10. Application of the colorimetric films 2.5.10.1. Color changes of the film in acidic and alkaline environments. The changes of the composite film color in different pH solutions were tested according the methodology shown by MedinaJaramillo, Ochoa-Yepes, Bernal, and Fama (2017). 20% GTE and 20% YM composite film (2 x 2 cm) were placed into 10 ml of acidic (pH 3.0) or alkaline solutions (pH 12.0). Changes in the visual color of tested films were recorded with a camera (Canon EOS 1300D).

The SEM was fitted with In-Beam SE detector. A beam current of approximately 1.0 nA was used with accelerating 15,000 V. 2.5.3. X-ray diffraction (XRD) XRD analysis was performed on MiniFlex 600, Rigaku diffractometer using Cu Kα at 40 V and 15 A. Diffraction data from 2 to 80° were obtained using continuous scanning at a speed of 10o/min and step 0.3°.

2.5.10.2. Fish freshness determination. The color changes of the film during fish spoilage were prepared according the published methodology (Baek & Song, 2018) with modifications. Briefly, fresh common carp (Cyprinus carpio) fillets was purchased from the local market. Each fish sample was placed at the bottom of sealable bag. The 20% GTE, 20% YM and 20% GTE + ZnONPs films were cut into squares and used as indicator for monitoring the freshness of fish. The fish samples were divided into three groups depending on the package method: (i) the first group was packed into sterile PET trays with cover, and the film indicators were attached to the inside of the cover and additionally directly onto the surface filet. (ii) The second group of fillets were placed into PPE bags and vacuum packed, with the film indicator attached into the headspace of the package and additionally directly onto the surface of the fillet. (iii) The third group of fillets was placed in sealed PPE bags in air atmosphere with the film indicator placed at the headspace of the package. The prepared samples were stored at room temperature for 72 h, and the film color was measured through the bag.

2.5.4. Thermogravimetric analysis (TGA) Thermal stability of the samples was analyzed using a thermogravimetric analyzer (Q500, TA Instrument). The heating rate was 10 °C/min from the room temperature to 1000 °C under nitrogen atmosphere (N2, flow rate of 60 mL/min). 2.5.5. UV–Vis absorption spectra measurement (UV–vis) UV–Vis spectra of FUR, FUR-ZnONPs, FUR-SeNPs, FUR-YM, FURYM + SeNPs, FUR-YM + ZnONPs, FUR-GTE, FUR-GTE + SeNPs, FURGTE + ZnONPs colloid solutions were obtained on UV-5500 spectrophotometer (Metash. Shanghai, China). 2.5.6. Measurement of film thickness Film thickness measurement was performed on a Mitotuyo 7327 (Kawasaki, Japan) at five random locations on each film. Average value of these estimations was used as the film thickness. 2.5.7. Water content and solubility The water content and solubility of film samples in water was done according to the published methods of Kavoosi, Rahmatollahi, Mohammad Mahdi Dadfar, and Mohammadi Purfard (2014) and Souza et al. (2017) with modifications. Briefly, three randomly selected 3 x 3 cm squares of each film type were weighed, dried in oven at 70 °C for 24 h and weighed again. Further, each film was immersed into 30 ml of Milli-Q water, covered and stored for 24 h at 25 ± 2 °C. Afterwards, the films were dried again in an oven at 70 °C for 24 h and weighed. The analysis was performed in triplicate.

2.5.11. The statistical analysis Statistica v13.0 software (Statsoft, Tulsa, USA) was used. To establish significant differences a three-way ANOVA with type of extract, extract concentration and type of nanoparticles used as independent variables with Tukey post-hoc test was employed for determination of differences between means. The probability value used for discarding null hypothesis was p < 0.05. 3. Results and discussion

2.5.8. Surface color measurement Film color was determined using the CIE Lab scale, using the Konica Minolta CR 200 Chromameter (Osaka, Japan). Each film type was analyzed using three different repetitions; with three measurements taken from each repetition (nine measurements for each film type were done). Standard white plate was used as a background. Total color difference (ΔE) was calculated using the formula provided by Mehdizadeh, Tajik, Razavi Rohani, and Oromiehie (2012).

3.1. Size distribution and ζ-potential measurement The size distribution of SeNPs and ZnONPs in solution was determined through DLS method, which gives more exact information about the distribution of hydrodynamic sizes of NPs irrespective of being mono or poly-crystalline (Hajji et al., 2017). The hydrodynamic diameters of SeNPs and ZnONPs were app. 80 and 90 nm, respectively. The average ζ-potential of FUR, GTE, YM, SeNPs and ZnONPs was -35.6, -28.3, -15.1, 12.2 and 19.3 mV, respectively. It is expected that NPs with a positive charge will interact strongly with the negatively charged biopolymer (Oun & Rhim, 2017). Regarding this fact and our previous experiences (Jamroz, Kopel et al., 2018), we selected FUR for further experiments. The FUR films were translucent and flexible while the films with extracts were transparent and showed the characteristic color given by each extract (GTE-light brown; YM- green color). Under the influence of ZnONPs white color, the films become white, nontranslucent. The incorporation of ZnONPs into GTE and YM films caused lack of transparency, but films keep flexibility. The solution of SeNPs had orange color and incorporation this type of NPs into films did not cause differences in the appearance of the film.

2.5.9. Bioactivities assay 2.5.9.1. ABTS radical scavenging activity. The ABTS assay was performed according to Barton (2010) with modifications. Briefly, ABTS aqueous solution (7 mM) was mixed with sodium persulfate (2.45 mM in the final solution) and left in the dark for 16 h. Such prepared solution was diluted with ethanol to the point, in which absorbance of the solution at 734 nm was approx. 0.7. Then, 2940 μl of diluted ABTS solution was mixed with 60 μL of film extract, stirred and incubated for 10 min at 30 °C. The absorbance was taken at 734 nm and compared to the blank. The results were expressed as the % of radical scavenging effect. The analysis of antioxidant assays was performed in six independent measurements for each sample.

3.2. Morphological characterization 2.5.9.2. Antimicrobial test. S. aureus (NCTC 8511), E. coli (NCTC 13216) and MRSA (ST239:SCCmec IIIA) bacterial strains were received from the Czech Collection of Microorganisms (Faculty of Science, Masaryk University, Brno, Czech Republic). The size of inhibition zones was determined according to the published method (Jamroz, Kopel et al., 2018).

SEM of the surface and cross-sectional section of the composite films can be seen in Fig. 1A and B, respectively. The FUR films showed a compact, non-porous, homogenous structure without phase separation. The good interaction between FUR and YM or GTE is observed, as evidenced by homogenous structure. This good interaction is due to 3

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Fig. 1. Microscopic appearance of composite films at (A) surface and (B) cross-section.

FUR + GTE or YM and FUR + SeNPs did not show diffraction peaks. All samples are amorphous as they show amorphous halo with a maximum at 20.1° 2Θ and a low intensity area at 6.1 a 30.6° 2Θ (Fig. 2A). The nanocomposite films with ZnONPs exhibited characteristic peaks at 2Θ of 32°, 34.4°, 36.2°, 47.5°, and 56.5°, which belong to (100), (002), (101), (102), and (110) planes (Fig. 2B). Similar results were also observed in nanocomposite films with ZnONPs (Kanmani & Rhim, 2014; Oun & Rhim, 2017).

hydrophilic character of these extracts. The results further show that the morphology is quite different from FUR films due to the presence of both types of nanoparticles. The incorporation of SeNPs imparted a rough surface structure in FUR films. On the other hand, the microstructure images showed that adding ZnONPs into FUR films caused homogeneous structure in which nanoparticles were incorporated in the matrix. Similar surface morphology of nanocomposite films was observed when Gracilaria vermiculophylla films were reinforced with ZnONPs (Baek & Song, 2018). Structure of GTE + ZnONPs composite films becomes less homogeneous with some aggregations or agglomerates of ZnONPs. This was mainly due to weaker interaction between FUR, GTE extract and ZnONPs. The same case was observed in YM + SeNPs composite films. The incorporation ZnONPs into YM films, and SeNPs into GTE films imparted a rough surface structure (Fig. 1A). Cross section analyses showed regular and homogenous structure of F (Fig. 1B). On the cross-section of the films with SeNPs or ZnONPs it is possible to see the presence of dispersed nanoparticles. Moreover, nanocomposite films showed smooth surfaces (Fig. 1B).

3.4. TGA analysis Thermogravimetric curves of FUR films and selected composite films are shown in Fig. 3A, B and C. Derivative curves were used to evaluate characteristic data, the minima to separate particular decomposition steps and maxima to evaluate temperature of the fastest rate (Td) of particular decomposition step (Δw). Data evaluated from the curves obtained under nitrogen atmosphere are shown in Suppl. Table 1. The films decomposed in five or six steps (very tiny or closely adjacent decomposition steps) were not distinguished but merged. Six decomposition steps of FUR films are marked by horizontal lines in Fig. 3A (five decomposition steps in N2 and six in air). In the first step, low-molecular substance evaporated at 45–74 °C from all films under 4.2–7.0 % in N2 and of 3.7–5.7% in air. The step is mostly associated

3.3. XRD analyses XRD results of the FUR and composite films with SeNPs and/or ZnONPs are shown in Figs. 2A and B, respectively. The neat FUR,

Fig. 2. XRD patterns of furcellaran and composite films with (A) SeNPs and/or (B) ZnONPs. 4

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Fig. 3. Thermo gravimetric curves of (A) furcellaran films, (B) furcellaran composite films with GTE, and (C) 20 YM composite films with nanoparticles obtained in N2 and air with marking of six decomposition steps. UV–vis absorption spectra of composite film with (D) YM and/or (E) GTE.

with the loss of free water adsorbed in the film (Arfat et al., 2014). The most of the films mass decomposed until 400 °C during the next three decomposition steps (steps 2, 3 and 4). These are attributed to decomposition of carbohydrates. Similar to carrageenan, the initial weight loss of FUR that occurs below 100 oC is associated with the evaporation of water and solvent, which are trapped into polymer chain. In the temperature range 210 to 280 oC, weight loss of FUR can be attributed to the distribution of the -OSO3- groups. However, degradation above 280 oC is associated with fragmentation of the carbohydrate backbone (Liew, Loh, Ahmad, Lim, & Wan Daud, 2017). The last decomposition step (5) ran in a wide temperature range (usually to 900 °C) in N2. However, the decomposition was completed in two steps (5 and 6) at 600 °C in the air. The steps are attributed to decomposition of aromatic hydrocarbons such as lignin and inorganic substances (Martone et al., 2009). Residue varied from 4.2 to 8.5% in N2 and from 5.3 to 10.0% in air. The content increased with addition of extracts and ZnONPs especially in the air. One of the reasons may be oxidation and incorporation of nanoparticles (Oun & Rhim, 2017). In the case of FUR film, the steps 1–4 are identical regardless of purge gas (Fig. 3B). The second step belongs to release of bound water and decomposition of FUR itself (Δw is about 15% considering the weight of the film after preparation). Further steps (3–4) are considered decomposition of glycerol and other part of FUR, respectively. The first steep part of the step 3 is attributed to decomposition of glycerol-rich phase. Burning occurred very probably during the fifth step in air and decomposition of inorganic materials such as carbonates occurred during the sixth step in air (Fig. 3B). Both types of nanoparticles increased Td of decomposition steps 2–4 especially in air and thus thermal stability of FUR film. Similar results have been reported for chitosan-based films containing ZnONPs (Sanuja, Agalya, & Umapathy, 2015). The steps 1–4 are nearly identical regardless of the purge gas; Td of the step 5 is lower for SeNPs in N2 but higher for ZnONPs together with residue. Decomposition temperatures of the step 5 and 6 in air are always higher and varied in Δw. Residue is nearly twice for ZnONPs. The addition of GTE to the FUR film led to the slight increase of Td of the steps 2–3 in N2 and of the steps 3–4 in air (Fig. 3B), i.e. thermal stability is higher. There is no difference in decomposition curves of

10% GTE and 20% GTE in particular purge gas except Td of the step 5 in N2 that decreased by about 250 °C. The addition of nanoparticles increased Δw of the step 2 and increased Td of the step 5 and in case of 20% GTE in N2. It is missing the steep decomposition step of glycerolrich phase. In air, Td of the step 5 decreased for 10% GTE + ZnONPs all Td increased for 20% GTE + ZnONPs. The addition of 10% of YM led to higher weight loss of the step 2 in N2 and to less weight loss of the steps 2, 3 and 5 in air and the step 5 in N2 together with decrease of Td of this step. The addition of 20% of YM led also to the increase of Td of the steps 2 and 3 in both purge gases and to lower Td of the step 5 by 240 °C in N2 with respect to FUR film. Decomposition steps 1–4 are the same regardless of the purge gas for each type of the film. The same situation can be applied for the addition of nanoparticles to 10% YM that increased thermal stability in N2 but decreased it in air and increased residue (higher content is for ZnO in both purge gases). Nanoparticles caused lower weight loss of the steps 2 and 4 and higher one for the step 3 in N2 and higher weight loss of the steps 3 and 4 in air. The addition of nanoparticles to 20% YM led to decrease of thermal stability (Fig. 3C) because Td of the step 2 decreased together with higher weight loss in this step especially for the films with ZnONPs in both purge gases. Nanoparticles increased Td of the step 5 in air and Td of the steps 4 and 5 in N2. It seems that GTE did not react with FUR, i.e. decomposition curves are the same in both purge gases but YM probably did. The great difference in decomposition curves may be to a certain extent caused by higher content of bound water in 10% YM with respect to FUR film and 20% YM (Suppl. Table 2). Nanoparticles increased thermal stability: ZnONPs more in N2 in both extracts, SeNPs were more active in air. There is nearly no difference between 10% GTE and 20% GTE except films with ZnONPs (higher thermal stability is for 20% GTE composite films) and decomposition of aromatic hydrocarbons and inorganic substances – the temperature is higher for 20% of extracts in N2. In case of YM films, thermal stability is slightly higher for 20% YM composite films in both purge gases. The films with ZnONPs exhibited increased thermal stability. Such trend was already observed with various biopolymerZnONPs composite films (Arfat et al., 2014; Oun & Rhim, 2017).

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for the films incorporated with SeNPs, all the other composite films resulted in stronger yellow appearance. These changes can be attributed to the inner color of GTE and YM. The addition of ZnONPs into FUR films also resulted in increased yellowness. The similar results were observed by other authors (Baek & Song, 2018; Kanmani & Rhim, 2014). The presence of YM and GTE alone produced a* values varying between -1.27 - 2.13 and -0.24 - 0.83. The addition of ZnONPs into FUR films had significant influence on all color parameters; however the most significant changes were observed when GTE and ZnONPs were incorporated together. There were no significant differences between control films and films with SeNPs alone. Addition of YM decreased significantly the L values indicating tendency towards darkness. The addition of YM, GTE and ZnONPs caused a change in both redness and yellowness. Besides films with SeNPs, the value of ΔE in each case increased compared with the control film. Values of ΔE above 3 indicate that the color differences are very distinct and could be seen by an inexperienced observer (Tiwari, Muthukumarappan, O’Donnell, & Cullen, 2008). Among the extracts, films with YM had higher values of ΔE then films with GTE. The changes in color can be attributed to presence of different polyphenolic compounds and chlorophyll (Medina-Jaramillo et al., 2017). The addition of ZnONPs into film matrix often results in significant color changes (Baek & Song, 2018; Kanmani & Rhim, 2014) which is in accordance with findings in this study, since the highest ΔE was observed in films with both extracts and ZnONPs.

3.5. UV–vis analysis There is no absorption band in spectrum of FUR films formed with YM and/or GTE (Fig. 3D and E, respectively). The SeNPs (< 100 nm) show no characteristic absorption peak (λmax) in the UV–vis region (200–800 nm) (Hien et al., 2018; Lin & Wang, 2005). Metal oxides exhibit barrier properties against UV-B and UV-A, thus, they are very often used as ultraviolet light-blocking compounds. Films with ZnONPs exhibited excellent ultraviolet blocking effect. The UV–vis absorption spectra for films with ZnONPs showed an adsorption maximum at 366 nm. These results agree well with those found in other publications (Arfat et al., 2014; Baek & Song, 2018). The composite films with YM showed a peak at 324 nm. YM + ZnONPs composite films had the absorption band at 360 nm which was attributed to the presence of ZnONPs (Lizundia, Urruchi, Vilas, & Leon, 2016) and YM. UV light can lead to undesired reactions such as lipid oxidation, loss of nutrients and discoloration, therefore, the protection from light is very important function for food packaging film (Nouri, Yaraki, Ghorbanpour, Agarwal, & Gupta, 2018). 3.6. Characterization of films The addition of extracts and nanoparticles together into FUR films resulted in significant differences in film thickness as shown in Suppl. Table 2. No differences in thickness were found between FUR films incorporated without and with different concentration of YM and GTE. Moreover, the addition of ZnONPs and SeNPs only did not change significantly the average thickness of the films. On the other hand, incorporation of YM and ZnONPs showed the most significant increase compared to the control film. An increase in thickness could be due to disruption in the order structure of FUR by the presence of extract compounds, since similar results were obtained in other studies which incorporated mango peel extract and epigagallocatechin gallate into gelatine films (Adilah, Jamilaha, Noranizan, & Hanani, 2018; Nilsuwan, Benjakul, & Prodpran, 2018). Moreover, the increase in the thickness was connected to higher content of solids in composite films with NPs (Oun & Rhim, 2017). The increase in thickness of films containing YM with SeNPs or ZnONPs was probably caused by reduction of the ordered alignment in film matrix, which can be indicated in results showed in Suppl. Table 2. The results of solubility showed that control, GTE, GTE + SeNPs, YM, YM + SeNPs and SeNPs films were completely dissolved in water. Solubility of films is an important parameter affecting its possible practical application in food industry as complete solubility significantly limits the use of a film as food products coating (Esteghlal, Niakousari, & Hosseini, 2018). Food products usually contain high water content, which would result in dissolution of the film and removal of its barrier properties. Therefore, the addition of ZnONPs improved the FUR films quality by decreasing its solubility to the level of 70.6 ± 2.0%. The decrease in solubility of FUR films with ZnONPs indicates the increased cohesiveness of the biopolymer matrix. The presence of ZnONPs in film leads to the formation hydrogen bonds between nanoparticles and FUR. Consequently, it reduces the interaction between film matrix and water molecules, which is in agreement with the observations of other authors (Baek & Song, 2018; Kotharangannagari & Krishnan, 2016). The complete solubility behavior of films with GTE and YM extracts is probably due to the more hydrophilic structure of FUR and GTE or YM, making the films more accessible to water. The water content of composite films was greatly influenced by the addition of YM + ZnONPs, with the lowest water content observed in the films with ZnONPs (Suppl. Table 2). This is because the addition of ZnONPs increases the film network’s integrity (Baek & Song, 2018). The incorporation of SeNPs at the 10 and 20% of GTE into FUR films significantly increased the water content of composite films. The values of L, a*, b* and ΔE are shown in Suppl. Table 3. The control film had slightly yellow appearance (positive b* value). Except

3.7. Bioactivities assay The antioxidant activity of FUR films formulated with GTE or YM and nanoparticles is presented in Fig. 4A. The FUR film and FUR films with nanoparticles show no antioxidant activity, whereas the films containing GTE and YM extracts exhibited increased ABTS activity with the increase dependent on the extract content regardless of its type. Among the extracts, the FUR films with 20% GTE had the greatest ABTS radical scavenging activities. Moreover, GTE had greater antioxidant activity than YM. These results are in agreement with (Gerolis, Lameiras, Krambrock, & Neves, 2017), who reported that GTE had the higher antioxidant activity then YM (ABTS+ test). The antioxidant activity of YM depends on phenolic and flavonoid content (Gullon et al., 2018). According to Gerolis et al., GTE had higher content of phenols and flavonoids than YM, which explains its higher antioxidant activity (Gerolis et al., 2017). The addition of SeNPs did not significantly affect the antioxidant activity of films with GTE and YM. However, the addition of ZnONPs caused significant decrease in antioxidant properties of FUR films with 20% GTE and YM. The obtained results are surprising since other studies indicate that both SeNPs and ZnONPs exhibit antioxidant activity (Cai et al., 2018; Chen, Yue, Jiang, Liu, & Xia, 2018; Soren et al., 2018). The results of antimicrobial activities of composite films are shown in Fig. 4B. All films, except for those with addition of SeNPs, showed the highest activity towards Gram-positive bacteria (S. aureus) compared with Gram-negative bacteria (E. coli). It might be possible that the cationic metallic nanoparticles, such as SeNPs, have a higher affinity for Gram-negative bacteria (more negative surface charge) than Gram-positive bacteria (less negative surface charge) (Oun & Rhim, 2017). The strongest antimicrobial activity of tested films was related to the presence of SeNPs within the matrix (Fig. 4B), which is not surprising since biofilms with SeNPs have been previously reported to have antimicrobial activity (Jamroz, Kopel et al., 2018). Films with ZnONPs were more effective against Gram-positive bacteria. More complex cell wall structure of Gram-negative bacteria might be more difficult for ZnO penetration into the cells (Ma & Zhang, 2009). Tea polyphenols and flavonoids from GTE have previously shown antimicrobial effects against many food spoilage microorganisms (Graham, 1992; Perumalla & Hettiarachchy, 2011; Wu et al., 2007), which is in accordance with results presented herein, since films with both GTE and YM formed 6

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Fig. 4. (A) Antioxidant activity of composite films with furcellaran. (B) Antimicrobial activities of composite films with furcellaran, expressed as inhibition zone diameter (mm).

Since both YM and GTE water extracts are rich in chlorogenic acid (Heck & De Mejia, 2007; Jeszka-Skowron, Krawczyk, & ZgołaGrześkowiak, 2015), these compounds are possibly responsible for the color differences observed in this study. In each type of films with 10 or 20% extracts, the color changes were observed, however the color differences were more pronounced in samples with higher extract concentration (data not shown). Simply, the visual measurement can be used to detect pH changes in food products. All the color changes were detectable with the naked eye. Our research on color changes of the films at an appropriate pH can simulate changes that may occur during food storage. Further research directions should include the use of intelligent films as packaging to monitor changes during food product storage. Intelligent packaging systems attached as labels on the packaging material could offer possibilities to monitor freshness of product. During the food spoilage process numerous volatile compounds are produced, which affect the pH of both the product as well as its environment. In case of fish products, proteolytic bacteria cause the increase in total volatile basic nitrogen (TVB-N) compounds, which mostly consists of trimethylamine, dimethylamine and ammonia (Aghaei, Emadzadeh, Ghorani, & Kadkhodaee, 2018). This in turn can cause the increase of pH of the surrounding atmosphere. Since films with SeNPs and GTE or YM gave the same visual effects as films with GTE or YM alone and the 20% YM + ZnONPs film behaved exactly like 20% YM, only the three films were chosen as sensors for monitoring the quality of stored fish.: 20% YM, 20% GTE and 20% GTE + ZnONPs. The most notable differences could be observed for films with 20% YM alone. After 72 h the color of the film was changed from light green to black when film was placed on the package of PET trays and sealable

significant inhibition zone against E. coli and S. aureus. The antimicrobial activity of YM extracts is correlated with the presence of compounds derived from chlorogenic acid (Martin et al., 2013). All films without SeNPs showed lack of activity against MRSA; however films with SeNPs showed inhibition zone ranging from 20.1 to 26.5 mm regardless of the presence of extract (Fig. 4B). 3.8. Intelligent material An intelligent packaging may contain smart devices (labels or tags) that are capable of collecting the information about properties of packaged foods. A smart packaging is able to monitor the quality of food products, for example changes in pH (Ma, Ren, Gu, & Wang, 2017). Fig. 5A and B present the photos of the responses of the composite films (20% of GTE and YM) assayed in different pH solutions (pH 3.0 and pH 12.0). The color of the films changed immediately after being placed in both solutions. All the films turned white when exposed to acid (pH 3.0). However, they became orange in an alkaline environment (pH 12.0). Although chlorophyll is not soluble in water, the study by (Wang, Park, Chung, Baik, & Park, 2004), showed that part of the chlorophyll from tea leaves can be found in tea infusions. According to Medina et al., chlorophyll content can be responsible for color changes of films with tea extracts (Medina-Jaramillo et al., 2017). On the other side chlorophyll in acidic environment degrades into more yellow or olive green pigments (Andrés-Bello, Barreto-Palacios, GarcíaSegovia, Mir-Bel, & Martínez-Monzó, 2013), which was not observed in this study. Previously, chlorogenic acid has been proposed as a possible compound responsible for darkening of GTE films in alkali environment (Jamróz, Kulawik, Krzyściak, Talaga-Ćwiertnia, & Juszczak, 2019). 7

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Fig. 5. Colorimetric response of composite films with (A) 20% YM and/or (B) 20% GTE at different pH values.

Fig. 6. Photographs of intelligent film during monitoring of fish spoilage (in package PPE bags, packed in vacuum).

PPE bags (Fig. 6). As can be seen from the figures those changes are clearly visible by a naked eye and the color change progressed with storage time. A FUR + GTE film was not used for further testing, as the color changes were barely visible. When film was placed directly onto the fish surface, the color change did not occur. This was to be expected, since the pH changes of the fish muscle during storage is very low and usually does not exceed 0.2 (Simeonidou, Govaris, & Vareltzis, 1997). Therefore the volatile compounds have to be released into the atmosphere of the product before they can react fully with the intelligent film. This is in accordance with the results obtained from the films placed inside the vacuum-packed carp fillets, which also exhibited low and not homogenous color change (Fig. 7). The intelligent pH indicators which are currently employed involve the use of anthocyanins (Zhai et al., 2017). However, to the best of our knowledge, YM extract, which does not contain anthocyanins, has not been used for this purpose.

4. Conclusions The composite films based on FUR and FUR with various combinations of GTE, YM, SeNPs and ZnONPs were successfully prepared by solution casting method. We found that nanoparticles directly increased the thermal stability: ZnONPs more in N2, while SeNPs were more active in air. There is nearly no difference between 10% GTE and 20% GTE composite films except those with ZnONPs. In case of YM composite films, thermal stability is slightly higher for 20% of YM. The composite films with ZnONPs and YM could be used as biodegradable UV-barrier, antimicrobial materials and as indicators of food quality as intelligent materials. The films with SeNPs showed enhanced antimicrobial activity against E. coli, S. aureus and MRSA, while the addition of GTE, as active agent highly improved the antioxidant effects to the composite films. Therefore, the combination of GTE and SeNPs incorporated into the FUR results in obtaining films with both potent antimicrobial and antioxidant activity. As expected, the differences 8

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Fig. 7. Photographs of intelligent film in during monitoring of fish spoilage (in sterile PET trays with cover).

between films with both extracts and both NPs allowed obtaining materials with different properties (color, solubility etc.). This fact is interesting from the practical point of view as one can expect different applications for each type of film. The obtained results suggest that FUR films with YM extract have the potential to be used as intelligent packing material.

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Declaration of Competing Interest The authors of this study declare that they have no conflicts of interest pertaining to the funding sources or to the materials presented in this study. Acknowledgements This work was financially supported by CEITEC 2020 (LQ1601), Internal Grant Agency of Mendel University (IGA 20/2017) and by EFRR project "Multidisciplinary research to increase application potential of nanomaterials in agricultural practice" (No. CZ.02.1.01/0.0/ 0.0/16_025/0007314). Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.fpsl.2019.100405. References Adilah, A. N., Jamilaha, B., Noranizan, M. A., & Hanani, Z. A. N. (2018). Utilization of mango peel extracts on the biodegradable films for active packaging. Food Packaging and Shelf Life, 16, 1–7. Aghaei, Z., Emadzadeh, B., Ghorani, B., & Kadkhodaee, R. (2018). Cellulose acetate

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