Article pubs.acs.org/JAFC
Characterization and Bioavailability of Tea Polyphenol Nanoliposome Prepared by Combining an Ethanol Injection Method with Dynamic High-Pressure Microfluidization Li-qiang Zou, Wei Liu,* Wei-lin Liu, Rui-hong Liang, Ti Li, Cheng-mei Liu,* Yan-lin Cao, Jing Niu, and Zhen Liu State Key Laboratory of Food Science and Technology, Nanchang University, No. 235 Nanjing East Road, Nanchang 330047, Jiangxi, China S Supporting Information *
ABSTRACT: Tea polyphenols are major polyphenolic substances found in green tea with various biological activities. To overcome their instability toward oxygen and alkaline environments, tea polyphenol nanoliposome (TPN) was prepared by combining an ethanol injection method with dynamic high-pressure microfluidization. Good physicochemical characterizations (entrapment efficiency = 78.5%, particle size = 66.8 nm, polydispersity index = 0.213, and zeta potential = −6.16 mv) of TPN were observed. Compared with tea polyphenol solution, TPN showed equivalent antioxidant activities, indicated by equal DPPH free radical scavenging and slightly lower ferric reducing activities and lower inhibitions against Staphylococcus aureus, Escerhichia coli, Salmonella typhimurium, and Listeria monocytogenes. In addition, a relatively good sustained release property was observed in TPN, with only 29.8% tea polyphenols released from nanoliposome after 24 h of incubation. Moreover, TPN improved the stability of tea polyphenol in alkaline solution. This study expects to provide theories and practice guides for further applications of TPN. KEYWORDS: tea polyphenols, nanoliposome, combining ethanol injection with DHPM, in vitro antioxidation, in vitro antibacterial activity, sustaining release, alkaline media stability
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INTRODUCTION Tea polyphenols, including flavanols, anthocyanins, flavonoids, and phenolic acids, are rich in green tea and have been demonstrated to possess several biological and pharmacological activities such as antioxidant, antibacterial, anticancer, and blood lipid lowering activities.1 Because of the various health attributes of tea polyphenols, they could be used in the food preparation and pharmaceutical industries.1 However, due to the oxidation sensitivity of tea polyphenols toward the external environment, their stability during processing and storage is reduced, which greatly limits their application.2 To overcome these disadvantages, extensive studies have been carried out to encapsulate tea polyphenols, such as nanoparticles,3 coprecipitation,4 coacervation core micelles,5 microparticles,6 and liposomes.2,7−9 The main objective of encapsulation is to protect the core material from adverse environmental conditions, thereby contributing to an increase in the shelf life of the product and promoting a controlled liberation of the encapsulation.10 However, the difference in wall material, encapsulation formation, and interaction between wall material and core material would result in a variation in entrapment efficiency and protected capacity of the core material. There are a wide variety of methods that can be used to produce tea polyphenol liposome. Gülseren et al.9 prepared tea polyphenol nanoliposomes using a one-stage high-pressure homogenizer. Gulseren and Corredig7 prepared tea polyphenol-bearing nanoliposome with high-pressure homogenization. Lu et al.2 prepared tea polyphenol nanoliposome by the thin film ultrasonic dispersion method. Ma et al.8 used a © 2014 American Chemical Society
reverse-phase evaporation method to prepare tea polyphenols and a vitamin E-loaded nanoscale complex liposome. Dynamic high-pressure microfluidization (DHPM) is an emerging technology, which uses the combined forces of high-velocity impact, high-frequency vibration, instantaneous pressure drop, intense shear, cavitation, and ultrahigh pressures of up to 200 MPa with a short treatment time (100 nm);7 TPN obtained by thin film ultrasonic dispersion method were 160.4 nm with a polydispersity index of 0.28;2 and the tea polyphenol nanoscale complex liposome showed 202.8 nm (mean sizes) and 0.296 (polydispersity index).8 In a preliminary experiment, a thin film dispersion method was also attempted to prepare tea polyphenol liposome, but it was difficult to wash membrane from the wall of the rotary flask and difficult to spontaneously form liposome when the tea polyphenol was 5 mg/mL. Hence, an ethanol injection method, without the membrane washing off process, was used to prepare tea polyphenol liposome. The mean particle size of tea polyphenol liposome prepared by the ethanol injection method was 496 nm, which was not in nanoscale. In our previous research, we also found that DHPM treatment containing strong mechanical forces could significantly reduce the particle size of liposome.12,24 In addition, the zeta potential of TPN under the optimum conditions was −6.16 mv (pH 6.0), which was lower than those of Gulseren and Corredig7 (−12 mv, pH 5.0) and Lu et al.2 (−67.2 mv, pH 6.62). Liposomes are mainly composed of cholesterol and phospholipids. The different value of zeta potential of liposome was probably attributed to variations in competence and property of phospholipids. There are two main viewpoints on whether the zeta potential value could directly decide its shelf life. The suspension with greater zeta potential is more likely to be stable, which was due to the charged particles repelling one another and thus overcoming the natural tendency to 936
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Figure 1. AFM micrograph of tea polyphenol nanoliposome.
Figure 2. (a) DPPH free radical scavenging capacity and (b) ferric reducing/antioxidant power (FRAP) of tea polyphenol solution and nanoliposme at various concentrations.
aggregate.25 However, it was also deemed in some studies that even at low zeta potential values (i.e., close to 0), liposomes might remain stable.26 According to the research studies of Lu et al.2 and Makino et al.,26 it can be concluded that the zeta potential value was not a direct indicator of the stability of liposome. Consequently, the shelf life of liposome depended not just on its zeta potential value. In this work, two vital indicators of liposome (entrapment efficiency and particle size) indicated that DPHM combined with ethanol injection methods was suitable for preparing TPN. As presented in Figure 1, 1 μm × 1 μm scans were captured, showing the morphology of TPN was mainly spherical defined shapes (indicated by the arrows). TPNs maintained a spherical and well-defined shape (common characteristic of nanoliposome), which was in agreement with the morphology observed by transmission electron microscopy.2 According to AFM photographs, most of the TPN was well distributed, which is in agreement with a narrow size distribution obtained by DLS (shown in Figure S1 in the Supporting Information). Furthermore, the sizes of nanoliposomes obtained through AFM were close to mean sizes measured by a dynamic laser
light scattering method, which was consistent with results of Maherani et al.27 Nanoliposome is a new technology for the encapsulation and delivery of bioactive agents. It is generally acknowledged that the performance of bioactive agents could be enhanced by nanoliposomes, improving their solubility and bioavailability and in vitro and in vivo stability, as well as preventing their unwanted interactions with other molecules.28 In addition, their smaller mean diameters could be helpful in enhancing their bioavailability.12 This study examined how the bioactivity of TPN varied. In vitro antibacterial activity and in vitro antioxidant activity of TPN will be discussed in detail in the following text. In Vitro Antioxidation. To date, it is still not clear how the in vitro antioxidant activity of tea polyphenols after nanoliposome encapsulation changed. There are different types of antioxidant methods used to estimate in vitro antioxidant activity of tea polyphenols before and after nanoliposome encapsulation. The DPPH free radical scavenging capacity assay and ferric reducing/antioxidant power (FRAP) assay were chosen to represent organic solvent and aqueous phase environments, respectively. 937
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reducing/antioxidant power of TPN was significantly lower than that of tea polyphenol solution. The FRAP values of the tea polyphenol solution at 20, 30, 40, and 50 μg/mL were equivalent to 17.1 ± 2.0, 25.5 ± 2.5, 30.6 ± 1.8, and 37.6 ± 2.2 μg/mL gallic acid, respectively, which are higher FRAP values than those of TPN (12.0 ± 1.3, 18.7 ± 2.3, 21.9 ± 1.9, and 28.6 ± 2.4 μg/mL gallic acid, respectively). It was reported by some researchers that the antioxidant activity measured by the FRAP assay was reduced by many encapsulations (solid lipid matrix, chitosan microspheres, novel polymer−polyphenol beads).20,31,33 Patel et al.20 reported that the lower FRAP value of epigallocatechin gallate in the novel polymer−polyphenol beads at an initial stage of 2 h was probably hindered by bead encapsulation, compared with free epigallocatechin gallate. Weerakody et al.31 also found that the antioxidant activity by FRAP assay of lipoic acid encapsulated in chitosan microspheres was much lower than the same concentration of free lipoic acid, which was probably due to structural interaction between chitosan matrix and lipoic acid. Donsı ̀ et al.33 reported that the antioxidant activities by FRAP assay of the encapsulated resveratrol and curcumin in a solid lipid matrix were much lower than those of resveratrol and curcumin that were not encapsulated. In this study, the FRAP assay of tea polyphenol was decreased by nanoliposome encapsulation. This was probably due to the fact that most of the tea polyphenol was encapsulated in the nanoliposome aqueous phase. Therefore, donating electron capacity of tea polyphenol encapsulated in nanoliposome would be influenced by phospholipid bilayer membranes, which resulted in a low antioxidant activity that was evaluated by the FRAP value of TPN. In Vitro Antibacterial Activity of TPN. It was not clear how the in vitro antibacterial activity of tea polyphenol changed after nanoliposome encapsulation. To evaluate the variation in antibacterial activity of tea polyphenol after nanoliposome encapusulation, four common food pathogenic bacteria (S. aureus, E. coli, S. typhimurium, and L. monocytogenes) were used to determine the antimicrobial activities of tea polyphenol before and after encapsulation of nanoliposomes. The inhibition zones of tea polyphenol solution and nanoliposome are shown in Figure 3. The inhibition zones of tea polyphenol solution for S. aureus, E. coli, S. typhimurium, and L. monocytogenes were 21.3 ± 1.3, 19.7 ± 0.5, 19.7 ± 1.2, and 19.3 ± 0.9 mm, respectively, whereas TPN exhibited smaller inhibition zones for S. aureus, E. coli, S. typhimurium, and L.
The stable DPPH radical is a widely used scavenging model for evaluating the free radical scavenging ability of natural compounds. The effect of antioxidants on DPPH radical scavenging was attributed to their hydrogen-donating ability. It is shown in Figure 2a that both tea polyphenol solution and TPN had concentration-dependent antioxidant activities toward DPPH free radical scavenging capacity. No significant differences in DPPH free radical scavenging capacity of the same concentration of tea polyphenol were found before and after nanoliposome encapsulation. The DPPH scavenging activities of the tea polyphenol solution in 50, 75, 100, and 125 μg/mL were 37.7 ± 3.0, 55.2 ± 1.9, 70.2 ± 5.2, and 81.4 ± 4.0%, respectively, with an equal or higher DPPH scavenging power of TPN (36.2 ± 2.0, 48.4 ± 3.1, 64.5 ± 3.0, and 76.8 ± 2.8%, respectively). Alterations in DPPH radical scavenging activity of antioxidants were reported by other authors after gum arabic− maltodextrin particle,29 liposome,30 and placebo chitosan microsphere31 encapsulation. Peres et al.29 demonstrated that free catechin and gum arabic−maltodextrin particles loaded with catechin exhibited similar DPPH quenching abilities in all tested concentrations and deemed that the loading method preserved the original antioxidant properties of the catechin. Niu et al.30 reported that the DPPH radical scavenging activity of liposomal curcumin was higher than that of free curcumin. It was ascribed to the polarity of different environments. Curcumin is a hydrophobic core material, so it would be entrapped in the liposomal bilayer, the polarity of which is much lower than that of sodium phosphate buffer, and the DPPH molecule has a highly hydrophobic nature; it is likely that the DPPH radical is scavenged by curcumin inside liposome.30 Weerakody et al.31 reported that lipoic acid encapsulated in placebo chitosan microspheres exhibited lower DPPH radical scavenging activity as compared to free lipoic acid, which could be attributed to an incomplete extraction of the encapsulated lipoic acid due to structural interactions. In this work, nanoliposome encapsulation did not reduce the DPPH radical scavenging capacity of tea polyphenol. It was probably explained by the main reagent in the DPPH radical scavenging system being alcohol. Nanoliposome would be demulsified by high concentrations of alcohol. Tea polyphenol encapsulated in liposome aqueous phase was exposed homogeneously into the DPPH system, after alcohol demulsification. Therefore, compared with tea polyphenol solution, TPN exhibited an equal or lower DPPH radical scavenging activity. In our previous study, it was also found that the DPPH radical scavenging activity of vitamin C was not significantly altered by nanoliposome encapsulations.12 The FRAP assay was developed to measure reducing power in plasma,19 but the assay has been adapted to measure antioxidant activity of tea polyphenols.32 The FRAP assay is quick and simple to perform, and the reaction is reproducible and linearly related to the molar concentration of the antioxidant present.19 It is based on the reduction, which is monitored by measuring the change of absorbance at 593 nm. At low pH, a colorless ferric complex (Fe3+−tripyridyltriazine) changes to a blue ferrous complex (Fe2+−tripyridyltriazine) by the action of electron-donating antioxidants.19 Figure 2b shows that both tea polyphenol solution and TPN have concentration-dependent antioxidant activity toward ferric reducing/ antioxidant assay. Nevertheless, the ferric reducing/antioxidant power of tea polyphenol was reduced by nanoliposome encapsulations. In the current study, we found that the ferric
Figure 3. Antimicrobial activities (mm of zone inhibition) of tea polyphenol solution and nanoliposme. 938
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monocytogenes (14.0 ± 0.2, 11.7 ± 0.5, 12.3 ± 1.3, and 12.8 ± 1.0 mm, respectively). The minimum inhibitory concentrations of tea polyphenol solution for S. aureus, E. coli, S. typhimurium, and L. monocytogenes were 0.078, 0.312, 0.078, and 0.039 mg/ mL, respectively, and minimum bactericidal concentrations were 0.312, 0.312, 0.312, and 0.312 mg/mL, respectively. Compared with tea polyphenol solution, TPN exhibited higher minimum inhibitory concentrations (1.25, 1.25, 1.25, and 0.625 mg/mL, respectively) and minimum bactericidal concentrations (2.5, >2.5, 2.5, and 2.5 mg/mL, respectively). It could be concluded from the above that the antibacterial activity of tea polyphenol was decreased by nanoliposome encapsulation. Low antibacterial activity of tea polyphenol nanoliposome in this work could be explained by the photograph of tea polyphenol solution and TPN incubated in a broth for 24 h (Figure S2 in the Supporting Information). With the concentration increasing from 0.078 to 2.5 mg/mL, the color of both tea polyphenol solution and nanolipsome in the broth became deeper and deeper. However, the color of tea polyphenol solution in the broth was much deeper than that of TPN in broth. Red sediments were found in tea polyphenol solution in the broth, and they became larger with increasing concentration (indicated by the arrows). Red circles were also formed on the walls of the test tube, which was due to the red sediments in the broth. However, no red sediments and circles were observed in all various concentrations of TPN samples. The cause for the sediment phenomenon could be probably attributed to the tea polyphenol. Catechins as the main components in tea polyphenol would react with proteins present in the broth and form various complexes with protein, thus resulting in the formation of sediments.34 TPN possessing high entrapment efficiency (78.5%) could prevent tea polyphenol incorporated into the aqueous cores from being released into the broth, interacting with proteins in the broth solution and forming sediments. Tea polyphenol solution could interact with the protein (in the broth) and form sediment, but there were large portions of antibacterial compositions still in the broth. The nonencapsulated portion of tea polyphenol in nanoliposome would also interact with protein, but the nonencapsulated portion in nanoliposome was too small to form obvious sediment. In addition, the content of encapsulated tea polyphenol released from nanoliposome during 24 h of incubation in broth was very low, which was also confirmed by the following sustained release profiles of TPN. Resident antibacterial ingredients remaining in broth in the TPN sample were much lower than that in the control group (tea polyphenol solution). Consequently, liposomal encapsulation could reduce the antibacterial activity of tea polyphenols. There have been some reports on encapsulation technologies that could alter the antibacterial activity of biological agents, but there were no uniform viewpoints on how the antibacterial activity of biological agents varied after encapsulation. According to previous papers, there were no consensus opinions on whether encapsulation technology could enhance or reduce the antibacterial activity of biological substances.21,22 In Liolios et al.’s21 study, all tested compounds from the essential oil presented enhanced antimicrobial activity after the liposomal encapsulation, even only 4.16% entrapment efficiency. According to Liolios et al.,21 the dramatically increased antimicrobial activity by liposomal encapsulation was probably due to PC−liposomes interacting with cells in many ways (intermembrane transfer, contact release, absorption, fusion, phagocytosis); the mechanism of interaction
depends on the cell type (cell wall/membrane composition), as well as the liposome membrane physicochemical characteristics; the use of liposomal formulation improves the cellular transport and releases the active component inside the cell. However, Wattanasatcha et al.22 reported that minimum inhibitory concentration and minimum bactericidal concentration of P. aeruginosa were increased by nanosphere encapuslation, which means that the action of thymol toward this bacterial strain is somewhat retarded when the material is encapsulated. Wattanasatcha et al.22 deemed that it was probably due to the ethylcellulose/methylcellulose shell being nondegradable under the experimental condition, and it is speculated that diffusion of the hydrophobic thymol molecules from the spheres is prior to their action on the bacteria. In the present study, we found that nanoliposome encapuslation reduced the antibacterial activity of tea polyphenols. This was probably due to the high viscidity, which made it difficult for tea polyphenols to diffuse into the agar. In addition, slight amounts of tea polyphenols released from the nanolipsome after encapuslation also result in lower antibacterial activity. In Vitro Drug Release of TPN. Liposomes have the property of prolonging the residence time of the drugs in the blood, releasing the drugs slowly in vivo. An in vitro release model in this work was expected to partly reflect properties of prolonging the residence time in vivo of liposome, which was an important factor of liposome potential applications. The in vitro drug release profiles of tea polyphenol solution and TPN were obtained and are shown in Figure 4. Rapid tea polyphenol
Figure 4. In vitro release of tea polyphenol from tea polyphenol solution and nanoliposme.
diffusion was observed in tea polyphenol solution before 2 h, and nearly 70% of tea polyphenol diffuses across the dialysis membrane. After that, the tea polyphenol diffusion rate from tea polyphenol solution dropped, and reached a maximum content of 92.6 ± 3.8% at 12 h. This was similar to Zhou et al.’s5 result that 81% of tea polyphenol solution diffused across the dialysis membrane after 4 h and reached a maximum content (near 95%) at 12 h. Compared with tea polyphenol solution, nanoliposome obviously slowed the release of tea polyphenol. TPNs had a continued release rate, with only 6.4 ± 1.9% of tea polyphenol released in 2 h and reaching a maximum content of 23.9 ± 4.5% in 12 h. Then they exhibited a very slow release of 29.8 ± 3.7% after 24 h. It could be concluded from the above that TPN has a sustained release profile. There were some reports that encapsulation methods or carrier systems such as nanoliposomes prepared by the thin film ultrasonic dispersion method,2 chitosan-coated nanoparticles,3 939
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high-pressure antisolvent coprecipitation,4 and complex coacervation core micelles5 could enhance the sustained release profile of tea polyphenols. Various carrier systems exhibited different sustained release capacities of tea polyphenols. In the Lu et al.2 study, TPN also exhibited a sustained profile, but the sustained capacity was lower than that in this work. The sustained release rate reached nearly 25% after 2 h, and within 12 h, the cumulative release increased to about 70%.2 The burst effect of tea polyphenols from chitosan-coated tea polyphenols nanoparticles was observed in 6 h, in which 30−40% of the drug was released from nanoparticles.3 Sosa et al.’s4 results showed that green tea encapsulation using high-pressure antisolvent coprecipitation exhibited a release of nearly 30% of the drug in 20 h, and no significant release was observed from 20 to 90 h. Zhou et al.5 demonstrated that complex coacervation core micelles had a sustained release capacity, and the complex coacervation core micelles continuously released tea polyphenol, until it was completely released at 14 h (97%). In this work, the sustained release behavior of nanoliposomes is presumably due to the high probability of tea polyphenols being incorporated into the aqueous cores inside the bilayers, which overcomes a burst release, whereas the variant sustained capacity of liposomes was probably attributed to their difference in entrapment efficiency, encapsulation method, and membrane structure. Stability under Alkaline Solution. Tea catechins incubating at slightly alkaline pH, similar to the small intestine, showed a rapid decline in the concentrations of tea catechins,35 and their half-life was significantly reduced by alkaline media.36 Consequently, the stability experiment of TPN under alkaline pH (pH 7.4), which mimics the environment present in the intestinal tract or other fluids such as plasma, is necessary to carry out. Tea polyphenols are easily oxidized, which is due to their abundance of various sensitive ingredients such as chemically unstable catechins and theaflavins. Tea catechins readily undergo oxidation and form quinone oxidized products,16 and their oxidation products are a brown color possessing a peak area at 430 nm.23 Therefore, the stability of tea polyphenol solutions and tea polyphenol encapsulated in nanoliposome could be measured by the absorbance of oxidation products. Changes in absorbance at 430 nm of 200 μg/mL tea polyphenol solution and tea polyphenol in nanoliposome in PBS (50 mM 7.4) were recorded with increasing time from 0 to 24 h. The variations in absorbance and color of tea polyphenol solution and TPN are shown in Figure 5. Both tea polyphenol solution and TPN at 0 h showed low absorbance at 430 nm (0.083 ± 0.01 and 0.062 ± 0.01), and then the absorbance increased to 1.304 ± 0.075 and 0.827 ± 0.068, respectively, at 24 h, whereas the absorbance of TPN at the same incubation time was much lower than that of tea polyphenol solution. For example, after incubation for 4 h, the absorbances at 430 nm of tea polyphenol solution and TPN were 0.613 ± 0.061 and 0.357 ± 0.044, respectively. In addition, the absorbance differences between the two samples were increasing. The difference was 0.138 at 1 h and increased to 0.477 at 24 h. In addition, we could observe that both tea polyphenol solution and TPN became browner over time. The brown color of tea polyphenol solution at the same incubation time was much darker than that of TPN. This was consistent with absorbance alteration. Both absorbance and color alteration reflected that nanoliposome encapsulation could decrease the degradation rate of tea polyphenol and improve the stability of tea
Figure 5. Stability profiles of tea polyphenol solution and nanoliposome in 50 mM potassium hydrogenphosphate buffer, pH 7.4 (37 °C), at an initial concentration of 200 μg/mL. (Inset) Photograph of tea polyphenol solution and nanoliposome incubated at 50 mM potassium hydrogenphosphate buffer, pH 7.4 (37 °C), for a set period.
polyphenols in an alkaline solution. This was similar to Fang et al.’s15 report that liposomes could provide stable retention of epigallocatechin gallate in the medium. Encapsulation of tea catechins in chitosan−tripolyphosphate nanoparticles enhanced their stability in potassium hydrogen phosphate buffer (pH 7.4), which was also observed.16 Several factors, including pH, oxygen level, and concentration of epigallocatechin gallate, could affect the stability of epigallocatechin gallate.37 It was reported that tea catechins became much less stable38 and tea polyphenol became more sensitive to degradation with reducing concentrations37 and when the pH increased from an acid pH to an alkaline pH. In this work, nanoliposome encapsulations’ ability to protect tea polyphenols was probably attributed to hindering two important factors (oxygen levels and concentration of tea polyphenol), which could obviously affect the stability of tea polyphenols. Tea polyphenols encapsulated in nanoliposome were isolated with extra membrane environments, so little oxygen could interact with tea polyphenol. In addition, due to the slow release ratio of tea polyphenols, the concentration of tea polyphenols in nanoliposome might remain at a high value and the degradation rate of tea polyphenols was much slower than that of tea polyphenol solution. In this study, the stability of tea polyphenols against alkaline media was significantly improved by nanoliposome using a combination ethanol injection method with DHPM. Although the antioxidant and antimicrobial activities of TPN were not improved after encapsulation of polyphenol in the liposome, the sustaining property was obviously enhanced.
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ASSOCIATED CONTENT
S Supporting Information *
Particle size distribution of tea polyphenol nanoliposome; photograph of tea polyphenol solution and tea polyphenol nanoliposome incubated in broth for 24 h. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Authors
*(W.L.) Phone: +86 791 88305872 (8106). Fax: +86 791 88334509. E-mail:
[email protected]. *(C.L.) Fax: +86-791-8334509. E-mail: liuchengmei@aliyun. com. 940
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Funding
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This study was supported financially by the National Natural Science Foundation of China (No. 21266021) and the Research Program of State Key Laboratory of Food Science and Technology, Nanchang University (No. SKLF-ZZB201311). Notes
The authors declare no competing financial interest.
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