Improved physicochemical and functional properties of dietary fiber from millet bran fermented by Bacillus natto

Food Chemistry 294 (2019) 79–86

Contents lists available at ScienceDirect

Food Chemistry journal homepage: www.elsevier.com/locate/foodchem

Improved physicochemical and functional properties of dietary fiber from millet bran fermented by Bacillus natto

T

⁎

Jiaxi Chu, Haizhen Zhao , Zhaoxin Lu, Fengxia Lu, Xiaomei Bie, Chong Zhang College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, PR China

A R T I C LE I N FO

A B S T R A C T

Keywords: Bacillus natto fermentation Foxtail millet bran Dietary fiber Physicochemical and functional properties Modification

Millet bran was fermented with Bacillus natto and the changes of structural, physicochemical and functional properties of its dietary fiber were investigated. Results showed that B. natto fermentation enhanced soluble DF content from 2.3% to 13.2%, and soluble DF/insoluble DF ratio from 3.1% to 19.9%. SEM and FTIR assay indicated that fermentation led to the degradation of cellulose and hemicellulose, thereby forming more porous and loose structure and polysaccharides. The binding capacities such as water and oil holding capacity, swelling capacity as well as cholesterol, bile salts, nitrite ion and glucose adsorption capacity were improved, while cation exchange capacity was not significantly changed. The total phenolic content and DPPH free radical scavenging capacity increased significantly. Overall, fermentation of millet bran by B. natto improved the structural and functional properties of its DF, which could be applied as a functional ingredient in food products.

1. Introduction Dietary fibers (DFs) are recognized as a group of carbohydrate polymers or oligomers that escape digestion in the small intestine, passing into the large intestine, where they are either partially or completely fermented by gut microbiota (Fuller, Tapsell, & Beck, 2018). According to the solubility, DF can be divided into water soluble DF (SDF) or insoluble DF (IDF). IDF consists mainly of cell wall components (e.g., cellulose, lignin, hemicellulose), while SDF consists of noncellulosic polysaccharides (e.g., pectin, gums, mucilage) (Dai & Chau, 2017). DF has attracted increasing interest due to its potential healthy and nutritious benefits. Studies had shown that diets high in DF were significantly associated with reduced risk of coronary heart disease, cardiovascular disease, diabetes and colon cancer (Threapleton et al., 2013, Elleuch et al., 2011). Supplementation with DF could improve the texture, color, flavor and taste of foods (Zheng & Li, 2018). Fortifying food with DF also could improve quality and shelf life (Bhise & Kaur, 2017). According to the literature reports, SDF was more bioactive than IDF due to its fermentability and viscosity (Ma & Mu, 2016), and ca 20–30% of human DF intake should come from soluble fiber (Elleuch et al., 2011). A good quality of DF was characterized with a high SDF

content. Many physical, chemical and biological treatments, such as extrusion, steam heat treatment, acidic hydrolysis, cellulase and xylanase hydrolysis, and microbial fermentation were developed to improve SDF content and its properties (Zhang, Wang, Cao, & Wang, 2018). It was obvious that microbial fermentation could be a potential method to produce a good quality DF with high SDF content and improved physicochemical and functional properties, such as water holding capacity (WHC), water swelling capacity (WSC), oil holding capacity (OHC) and anti-diabetic effect (Min et al., 2018; Cui, Gu, Zhang, Ou, & Wang, 2015). Millet bran, the by-product of millet processing industry, contains an abundance of nutritious components, especially dietary fiber. However, the low SDF content (1.75%) of millet bran DF limits its use (Zhu et al., 2018). Although there are some reports about the applications of millet bran and dietary fibers (Kang, Kou, Shen, Wang, & Cao, 2017; Palaniappan, Yuvaraj, Sonaimuthu, & Antony, 2017; Bijalwan, Ali, Kesarwani, Yadav, & Mazumder, 2018), information about the changes of structural, physicochemical and functional properties of DF from microbial fermented millet bran is lacking. The aim of this paper is to evaluate the two effects of microbial fermentation on millet bran: (1) the change of SDF content; (2) the changes of structural,

Abbreviations: DF, Dietary fiber; SDF, soluble dietary fiber; IDF, insoluble dietary fiber; WHC, water holding capacity; WSC, water swelling capacity; OHC, oil holding capacity; F-MBDF, fermented millet bran dietary fiber; UF-MBDF, unfermented millet bran dietary fiber; SEM, Scanning electron microscopy; CAC, cholesterol binding capacity; NIAC, nitrite ion adsorption capacity; CEC, cation exchange capacity; GAC, glucose-adsorption ability; TPC, total phenolic content; GAE, gallic acid equivalents ⁎ Corresponding author at: Weigang No. 1, Nanjing Agricultural University, Nanjing 210095, PR China. E-mail address: [email protected] (H. Zhao). https://doi.org/10.1016/j.foodchem.2019.05.035 Received 2 October 2018; Received in revised form 19 March 2019; Accepted 7 May 2019 Available online 08 May 2019 0308-8146/ © 2019 Elsevier Ltd. All rights reserved.

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

physicochemical and functional properties of millet bran dietary fiber. This study will provide an effective and novel method for obtaining functional dietary fibers.

DF were determined following the method of Xiong, Zuo, and Zhu (2005). 2.5. Scanning electron microscopy

2. Materials and method Scanning electron microscopy (SEM) was used to evaluate the effect of fermentation treatment on DFs structural characteristics. Dietary fiber samples were fixed in 3% glutaraldehyde in 2.0 M sodium phosphate buffer. After 2 h, samples were rinsed 3 times with the same buffer and dehydrated in a graded ethanol series (50%, 70%, 80%, 90%, 100%) for 15 min each and 100% ethanol three times for 30 min. After drying in a CO2 critical point drying, the fiber samples were placed on a specimen holder with the help of double-sided adhesive tapes and sputter-coated with gold powder. Samples were observed with an Environmental scanning electron microscope (XL-30ESEM, Philips, Holland) at an accelerating potential of 10 kV and high vacuum condition.

2.1. Materials Foxtail millet (Setaria italic) bran was purchased from Qinshui Country (Shanxi Province, China). Eggs and soybean oil were purchased locally. Cholesterol (≥99%) was provided by Sigma. Heat-stable alphaamylase (≥4000 U/g), neutral protease (> 50 U/mg), amyloglucosidase (> 100 U/mg), and sodium cholate (> 98%) were purchased from Aladdin Chemistry Co., Ltd. Other chemicals and reagents were analytical grade and obtained from Nanjing chemical reagents Co., Ltd (Nanjing, China). 2.2. Defatted millet bran preparation

2.6. Fourier-transformed infrared spectroscopy Millet bran was milled and passed through a 200 mesh sieve to obtain a fine powder. The fine powder was defatted three times with nhexane (1:2.5, g/ml) and dried in a fume hood. The dried defatted millet bran was kept at −20 °C for further use.

Fourier-transformed infrared spectroscopy (FT-IR) was performed using a NEXUS870 spectrometer (NICOLET, American). 1–2 mg DFs were thoroughly mixed with KBr (1:100, w/w) and pelletized. FT-IR spectra were recorded from 400 to 4000 cm−1 with 32 scans and a resolution of 4 cm−1.

2.3. Preparation of millet bran dietary fiber 2.3.1. Fermented millet bran preparation Millet bran was fermented with Bacillus natto, a Bacillus bacteria, previously kept in Enzyme Engineering lab of the Department of Bioengineering, Nanjing Agricultural University. Before use, Bacillus natto was revitalized in100 ml fresh seed medium, which with a volume of 1 L, included 10 g of peptone, 3 g of beef extract and 5 g of NaCl, with a neutral pH. The seed cultivation was incubated at 37 °C and 180 rpm in an incubator for 24 h. Cells were harvested by centrifugation and washed with physiological saline (0.9%), and then resuspended in the physiological saline to a concentration of 107–109 CFU/ml, which served as the inoculum for millet bran fermentation. Fermentation substrate was prepared with defatted millet bran (10 g), glucose (0.1 g) and NaCl (0.5 g) in 100 ml distilled water and sterilized by autoclaving at 115 °C for 20 min and cooled for inoculation. The sterilized fermentation substrate was started at 37 °C and 180 rpm by inoculating with 3% of B. natto inoculum concentration (approximately 106 CFU/ ml). After incubation for 47 h, the wet fermented millet bran was taken out and used for the preparation of dietary fiber.

2.7. Physiochemical and functional properties 2.7.1. Physicochemical properties Water holding capacity (WHC) and oil-binding capacity (OBC) of dietary fibers at different treatment time were estimated according to the method reported by Sangnark and Noomhorm (2003). Water swelling capacity (WSC) of dietary fibers at different treatment time was determined by the method reported by Zhang, Bai, and Zhang (2011). 2.7.2. Cholesterol adsorption capacity Cholesterol binding capacity (CAC) was determined by the method of Zhang, Huang, and Ou (2011). Egg yolk was used to replace cholesterol, as cholesterol was difficult to dissolve in water even after addition of emulsifiers. Fresh yolk was separated from fresh eggs and diluted 1:10 (v/v) with deionized water. Mixtures of 1.0 g DF with 25 ml diluted yolk were adjusted to pH 2.0 and 7.0, simulating gastric and intestinal environment, respectively, and incubated at 120 rpm and 37 °C in a shaking water-bath for different time. Diluted yolk (25 ml) was used as the blank. At the end of incubation, reaction mixture was centrifuged at 4000g for 20 min. 0.02 ml supernatant was used to determine the cholesterol concentration according to the o-phthalaldehyde method. Standard curve was generated using a standard cholesterol solution. The CAC was calculated as follows:

2.3.2. Dietary fiber extraction Dietary fiber from millet bran was prepared according to the method described by Zhu et al. (2018). 10 g fermented or unfermented defatted millet bran was suspended in 100 ml water. After adjusting the pH to 5.5, alpha-amylase (200 U/g) was added and the mixture was stirred gently at 95 °C for 1 h. The mixture was cooled and adjusted to pH 4.2, and amyloglucosidase was added. After incubation at 60 °C for 1 h, the reaction mixture was adjusted to pH 7.0, mixed with neutral protease (250 U/g) and incubated at 55 °C for 2 h. The mixture was heated in boiling water for 15 min to inactivate the enzymes and cooled to room temperature. The cooled mixture was precipitated with 4 vol of 95% ethanol overnight. The residue was collected and dried. DFs from B. natto fermented millet bran (F-MBDF) and unfermented millet bran (UF-MBDF) were obtained.

CAC =

(Cblank − Cd ) − (Cyolk − Cblank ) W

× 25

where Cyolk, Cblank, and Cd were the concentrations of cholesterol in the diluted yolk, the diluted yolk without DF, and the diluted yolk mixed with DF (mg/ml), respectively; 25 was the volume of the adsorption system (ml); and W was the dry weight of DF (g). The unit of CAC was mg/g dry DF. 2.7.3. Sodium cholate adsorption capacity Sodium cholate adsorption capacity (SCAC) was evaluated according to the method reported by Zhang et al. (2011). Briefly, standard sodium cholate solution (10 µmol/ml) was prepared with phosphate buffer solution (pH 6.9). 0.5 g dietary fiber was incubated at 37 °C for 1 h with 20 ml standard sodium cholate solution and centrifuged at 4000 rpm for 15 min. The residual sodium cholate concentration in

2.4. Chemical analysis Moisture, protein, ash and fat contents of dietary fibers were determined according to the standard methods of GB/T5009 (2016), and soluble, insoluble and total fiber contents were determined according to the AACCI method 32–07 (2000). Cellulose, hemicellulose and lignin of 80

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

evaluated according to previous method (Saiga, Tanabe, & Nishimura, 2003). The DPPH solution in ethanol (0.2 mmol/L) was prepared freshly, and incubated with sample solution at room temperature for 30 min, and then the absorbance at 517 nm was measured (AS). A blank control absorbance (AB) was measured with equal volume ethanol to replace sample and a solvent control absorbance (AC) was measured with equal volume ethanol to replace DPPH solution. Free radical scavenging activity was calculated using the following formula:

supernatant was determined by furfural colorimetric method. Standard curve was plotted using standard sodium cholate solution. Sodium cholate adsorption capacity was calculated according to the difference in original and residual bile salt concentrations. The unit of SCAC was mmol/g dry DF. 2.7.4. Nitrite ion adsorption capacity Nitrite ion adsorption capacity (NIAC) of UF-MBDF and F-MBDF was determined according to the reported method (Zhu, Du, & Xu, 2015) with slight modification. Briefly, dried DFs (0.5 g) were mixed with 100 ml 1 μmol/L NaNO2 solution in a 250 ml conical flask. The pH was adjusted to 2.0 and 7.0, simulating gastric and intestinal environment, respectively. The mixture was incubated at 37 °C for certain time with continuously magnetic stirring. Samples were taken for the measurement of residual concentration of nitrite ion. NIAC was expressed as follows:

NIAC =

A − AC ⎞ DPPH scavenging rate(%) = ⎛1 − S × 100 AB − AC ⎠ ⎝ ⎜

⎟

2.9. Statistical analyses Each experiment was carried out in triplicate. Statistical analyses were performed with SPSS Version 16.0 software (Chicago, IL, USA). Differences among samples were determined by one-way ANOVA. The data were expressed as the mean ± standard deviation. P < 0.05 was considered to be statistically significant.

(C1 − C2) × M ×V m

where C1 and C2 was the concentration of NaNO2 solution before and after adsorption, µmol/L, M was the relative molecular weight of NaNO2, m was the weight of dietary fiber, g; V was the total volume of treated sample, L.

3. Results and discussion 3.1. Proximate composition

2.7.5. Glucose adsorption capacity The assay was conducted following the procedure by Kabir et al. (2014) with slight modifications. Briefly, the glucose-adsorption capacity (GAC) (μmol/g) was measured by mixing dietary fiber (0.1 g) with 20 ml glucose solution at 37 °C for 2 h. Then the mixture was centrifuged at 4000 rpm for 20 min. Glucose concentration in the supernatant was assayed using DNS reagent-based colorimetric assay. Glucose adsorption capacity was recorded as μmol/g dry matter.

The chemical composition of the fibers of F-MBDF and UF-MBDF is shown in Table 1. Significant differences were observed between the contents of proteins, fats and total dietary fiber in the two extracted dietary fibers, while the contents of ash and moisture were not obviously different (P > 0.05). F-MBDF exhibited significantly lower protein content (2.1%) than UF-MBDF (4.3%), probably due to the degradation of protein by B. natto during the millet bran fermentation process. Total DF content of F-MBDF was higher than that of UF-MBDF, indicating the increase of fiber purity by fermentation. F-MBDF exhibited significantly lower IDF content (66.5%), but higher SDF content (13.2%), than UF -MBDF with 73.4% and 2.3% for IDF and SDF, respectively. SDF/IDF ratio increased from 3.1% to 19.9%. The change of SDF/IDF ratio was attributed to the partial solubilization and depolymerization of hemicellulose and insoluble pectic substances (Marconi, Ruggeri, Cappelloni, Leonardi, & Carnovale, 2000). This could be demonstrated from the significantly reduced content of cellulose, hemicellulose and lignin (17.3% to 14.3%, 47.3% to 44.4% and 8.8% to 7.9%, respectively) after B. natto fermentation (Table 1). This indicated that fermentation could enhance SDF content. Dietary fiber containing more than 10% SDF is regarded as a characteristic of high quality dietary fiber (Qiu et al., 2010). SDF helps to lower blood cholesterol and control blood glucose. So fermentation could improve the quality of millet bran dietary fiber. Furthermore, the purity of F-MBDF and UF-

2.7.6. Cation exchange capacity Cation exchange capacity (CEC) was measured by treating DFs with hydrochloric acid (Carvalho et al., 2009). Dried DFs were mixed with 10 ml of 0.1 mol/L hydrochloric acid for 2, 4, 6, 8, 10 and 24 h to convert dietary fiber’s functional cation groups into their acidic forms, then filtered. The residual was washed with deionized water until the filtrate was free from Cl− (verified using10% AgNO3 solution) and mixed with 25 ml of 0.3 mol/L NaCl solution thoroughly, then titrated with 0.01 mol/L NaOH with phenolphthalein as indicator. CEC was expressed as the consumed mole number of 0.1 mol/L NaOH per gram of dietary fiber at pH 7.0. 2.8. Assays for antioxidant properties of DFs 2.8.1. Extraction of antioxidant substances 3.0 g dietary fiber was extracted with 80% methanol (30 ml) by a magnetic stirring for 2 h and centrifuged at 4000 rpm for 20 min. The supernatant was transferred to a clonical vial and filled up to 100 ml with 80% methanol, and then stored at 4 °C for further study.

Table 1 Chemical composition of UF-MBDF and F-MBDF.

2.8.2. Total phenolic content (TPC) The TPC of dietary fiber was determined using the Folin-Ciocalteu reagent-based colorimetric assay (Lamuela-Raventós, Singleton, & Orthofer, 1998). Briefly, 1 ml diluted methanol extract was incubated with 5 ml Folin-Ciocalteu reagent and 4 ml of 7.5% (w/v) Na2CO3 at room temperature and darkness for 2 h. Then the absorbance was measured at 760 nm. Gallic acid standards at 0, 10, 20, 30, 40 and 50 μg/ml were treated as above to develop the standard curve. Phenolic content was expressed as gallic acid equivalents (GAE) and recorded as mg/g dry matter.

Components

UF-MBDF

F-MBDF

Protein (%) Ash (%) Moisture (%) Fat (%) Total DF (%) IDF (%) SDF (%) Cellulose (%) Hemicellulose (%) Lignin (%)

4.3 ± 0.2b 6.3 ± 0.5a 4.1 ± 0.3a 3.6 ± 0.3b 75.6 ± 0.2a 73.4 ± 0.1b 2.3 ± 0.1a 17.3 ± 0.2b 47.3 ± 0.2b 8.8 ± 0.1b

2.1 ± 0.0a 5.7 ± 0.2a 4.2 ± 0.2a 2.9 ± 0.3a 79.7 ± 0.3a 66.5 ± 0.3a 13.2 ± 0.2b 14.3 ± 0.1a 44.4 ± 1.0a 7.9 ± 0.2a

UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from Bacillus natto fermented millet bran; IDF, water insoluble dietary fiber; SDF, water soluble dietary fiber. Each value was expressed as the mean ± SD (n = 3). a,bDifferent small letters within a row mean significant difference (P < 0.05).

2.8.3. Determination of DPPH free radical scavenging capacity DPPH free radical scavenging capacity of millet bran DF was 81

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

Fig. 1. Scanning electronic micrograph for UF-MBDF and F-MBDF (A and B were the images of UF-MBDF at magnifications of 300× and 1000×. C and D were the images of F-MBDF at magnifications of 300× and 1000×). UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from B. natto fermented millet bran.

MBDF was comparable to that from rice bran (74.1–76.8 g/100 g) (Wen, Niu, Zhang, Zhao, & Xiong, 2017), indicating that they could be used as a functional ingredient. 3.2. SEM SEM micrographs of DFs from fermented and unfermented millet bran were magnified 300 and 1000 times. As reported in Fig. 1, the microstructure of UF-MBDF showed irregular shape flakes of uneven size and dense surface (Fig. 1A and B), with some small particles on the surface. After B. natto fermentation, the structure of F-MBDF became more loosen and porous, forming a honeycomb structure (Fig. 1C and D). It is likely that this structural characteristic contributes to the adsorption properties of DF such as water holding capacity, oil-holding capacity and cholesterol binding capacity (Zheng, Li, Xu, Gao, & Niu, 2018). Therefore, DFs from B. natto fermented millet bran had better physicochemical and functional properties than those from unfermented millet bran.

Fig. 2. FTIR spectra of UF-MBDF and F-MBDF. UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from B. natto fermented millet bran.

while some characteristic bands changed in absorbance and/or wavenumbers. Both displayed a broad, intense band at about 3400 cm−1, which was attributed to the stretching vibration of OeH, originating mainly from cellulose and hemicelluloses. After fermentation, the band shifted from 3300 cm−1 to 3412 cm−1 , probably due to the increase of

3.3. FT-IR The FT-IR spectra for UF-MBDF and F-MBDF are shown in Fig. 2. The FT-IR spectra of F-MBDF and UF-MBDF were in general similar 82

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

3.4.2. Adsorption capacity of dietary fibers for cholesterol, bile acid salts and glucose Fig. 3D shows the adsorbed cholesterol amount of the two millet bran dietary fibers at pH 2.0 and pH 7.0 (simulating gastric and intestinal environment). The highest CAC values of F-MBDF could reach 14.3 mg/g (pH 7.0) and 9.2 mg/g (pH 2.0) at 2.0 h, and so were the UFMBDF, 5.6 mg/g (pH 7.0) and 1.4 mg/g (pH 2.0), respectively. It was obvious that the CAC values at pH 7.0 were higher than those at pH 2.0, suggesting the CAC of MBDFs was stronger in simulated intestinal environment than in simulated gastric environment. Our results were in agreement with the results of Zhang et al. (2011), who found that wheat bran DF showed a lower cholesterol binding capacity (2.2 mg/g) at pH 2.0 than at pH 7.0 (3.5 mg/g). Furthermore, the CAC of F-MBDF was far higher than that of UF-MBDF, perhaps due to the increased SDF content. The higher the SDF content was, the stronger the serum cholesterol capacity lowering effect became (Chen, Ye, Yin, & Zhang, 2014). In addition, F-MBDF showed a higher CAC than that of DFs from wheat bran (3.5 mg/g at pH 7.0 and 2.2 mg/g at pH 2.0) and soybean hull (7.4 mg/g at pH 7.0 and 5.9 mg/g at pH 2.0) (Zhang et al., 2011), suggesting it could be used as a functional ingredient to lower cholesterol content in vivo. The evaluation of sodium cholate adsorption capacity (SCAC) was very important for dietary fiber to assess its cholesterol-lowering ability. Results in Table 2 showed that the SCAC of F-MBDF (105.6 μmol/g) was significantly higher than that of UF-MBDF (75.1 μmol/g) (P < 0.05), probably due to the increase of SDF content caused by fermentation. Zhang et al. (2011) also found that the adsorption capacities of the IDFs from wheat bran and soybean-seed hull for cholesterol and sodium cholate significantly increased when SDF from apple peels (20% of total concentration) was mixed with them. Furthermore, the SCAC vaules of F-MBDF and UF-MBDF were higher than that of DFs from wheat bran (3.2 mg/g) and soybean hull (3.5 mg/ g). The capacity of dietary fiber to adsorb glucose can delay or reduce the glucose digestion and absorption in the gastrointestinal tract, which play an important role in reducing blood sugar. As shown in Table 2, fermentation could significantly improve the GAC of F-MBDF (P < 0.05). The GAC of F-MBDF was 3.38 mmol/g, which was 1.39 times as much as in UF-MBDF. The increased GAC of the F-MBDF might be due to its increased surface area or porosity for glucose adsorption (Qi et al., 2016). The adsorption capacities of MBDFs to glucose were higher than those of carrot pomace IDF (2.63 mmol/g) (Yu, Bei, Zhao, Li, & Cheng, 2018) and oat IDF (0.43–0.91 mmol/g) (Chen, Gao, Yang, & Gao, 2013), while lower than that of SDF prepared from tomato peels which varied from 1.03 to 2.10 mg/mg (Niu, Li, Xia, Hou, & Xu, 2018).

free –OH produced from the hydrolysis of cellulose and hemicellulose due to the fermentation process. The strong bands about 2930 cm−1 were representative of CeH vibrations from some methyl groups of polysaccharides and carbonyl groups (Sivam, Sun-Waterhouse, & Perera, 2013). The band around 1653 cm−1 represented the characteristic absorption of C]O bond for uronic acid. The weak peak about 1516 cm−1 was characteristic bending or stretching of aromatic hydrocarbons of lignin (Ma, Lu, & Cao, 2015). This band intensity became weaker after B. natto fermentation, indicating the structure of lignin linked to hemicellulose was changed when the hemicellulose was hydrolyzed during fermentation. A group of weak bands around 1200–1400 cm−1 were assigned to the bending vibrations of CeH group. The bands at 1000–1200 cm−1 corresponded to CeO stretching vibrations, which might be CeOeH and CeOeC of sugar ring in cellulose and hemicelluloses. The weak band at 881 cm−1 was the deformation vibration of βeCeH, which was the characteristic band of βglycosidic linkages (Ma & Mu, 2016).

3.4. Physiochemical and functional properties 3.4.1. Water holding capacity, water swelling capacity and oil holding capacity The WHC of dietary fiber was also closely related to the ratio of SDF to IDF, particle size, surface property and source. As shown in Fig. 3A, the WHC of dietary fibers increased with time extending, and up the highest at 2 h, which was 3.3 g/g and 4.4 g/g for UF-MBDF and FMBDF, respectively. The WHC of F-MBDF was higher than that of UFMBDF at all treated time, probably due to the increased content of SDF and the honeycomb structure (Zheng & Li, 2018). Yalegama, Karunaratne, Sivakanesan, and Jayasekara (2013) found that dietary fiber bearing good WHC was also due to the hydrophilic groups of polysaccharides. Dietary fibers with high WHC could be used as functional ingredient to avoid synaeresis and modify the viscosity and texture of some formulated food (Elleuch et al., 2011). Fig. 3B shows the WSC of UF-MBDF and F-MBDF at different treatment time. The maximal WSC of UF-MBDF and F-MBDF was 2.0 ml/g and 3.5 ml/g, respectively. With time extending, WSC increased up to maximum at 2 h, then decrease slightly. It was reported that high SDF content and more porous structure contributed to the swelling of dietary fiber exposed to water (Zheng & Li, 2018). FT-IR results also demonstrated that the linkages of cellulose and hemicellulose was broken (Cheng et al., 2017) during fermentation, exposing more hydrogen bonds and dipole forms, which also helped to the high WSC. The ability of dietary fiber to retain oil is important in food applications, for example, in preventing fat losses upon cooking and also in nutrition where the ability to adsorb or bind bile acids and increase their excretion is associated with plasma cholesterol reduction (Tosh & Yada, 2010). Fig. 3C shows the OHC of dietary fiber from fermented and unfermented millet bran at different treatment time. Both dietary fiber presented same trend. With time extending, OHC increased up to the maximum at 1.5 h, which was 2.2 g/g and 3.3 g/g for UF-MBDF and F-MBDF, respectively, then remained unchanged. The OHC of F-MBDF was stronger than that of UF-MBDF, probably due to the porous and loosen structure (seen SEM Figures). Increased SDF content in F-MBDF might be another reason for high OHC. DF components, such as arabinoxylan, pectin, arabinogalactan might contribute to adsorb and scavenge saturated and unsaturated lipid materials due to their strong affinity to lipid materials (Devi, Vijayabharathi, Sathyabama, Malleshi, & Priyadarisini, 2014). The high OHC was an important characteristic of dietary fiber since this capacity might interfere with the intestinal absorption of a dietary lipid, thereby contributing to the control of body weight and abnormal blood lipid profiles (Carvalho et al., 2009).

3.4.3. Nitrite ion adsorption capacity Nitrite is a reactive ion, which can react with secondary amines and amides under acid conditions to form N-nitroso compounds, many of which have been shown to be carcinogenic in animals. Many food constituents such as vitamin C and polyphenolic compounds could inhibit the formation of N-nitroso compounds, and react as a nitrite scavenger. Fig. 3E depicts the changes of both MBDFs for NO2− adsorption capacity at different time and pH values (pH 2.0 and pH 7.0, simulated gastric and intestinal environment). At the same pH value, both MBDFs exhibited similar trends for NO2− adsorption. NIAC reached the maximum at 6 h, which were 2.32 mg/g (UF-MBDF) and 4.60 mg/g (F-MBDF) at pH 2.0, 0.35 mg/g (UF-MBDF) and 0.85 mg/g (F-MBDF) at pH 7.0. pH had an obvious effect on the NIAC of MBDFs and the NIAC of both MBDFs at pH 2.0 were higher than that at pH 7.0, indicating the NIAC of MBDFs in stomach was higher than that in intestine. Our results were in agreement with the results of Møller, Dahl, and Bøckman (1988), who found that wheat bran could act as nitrite scavenger under stomach mimic environment (low pH value). They also found that the nitrite scavenging effect of wheat bran was due to the presence of phenolic acids such as coumaric or ferulic acid. These 83

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

Fig. 3. Physiochemical properties of water holding capacity (A), water swelling capacity (B), oil holding capacity (C), and functional properties of cholesterol binding capacity (D) and nitrite ion adsorption capacity (E) of UF-MBDF and F-MBDF. UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from B. natto fermented millet bran. a–cDifferent small letters on the bar mean significant difference within the same color columns (P < 0.05). *Superscript asterisk on the bar mean significant difference between UF-MBDF and F-MBDF at the same treatment time (P < 0.05).

phenolic acids were reported to ester-linked to lignin and/or carbohydrates in the cell walls and reacted very rapidly and efficiently with nitrite at low pH value (≤2.5). The nitrite scavenging capacity might be the possible role of bran in protecting against gastric cancer development. Here the NIAC of F-MBDF was higher than that of UF-MBDF, perhaps due to the increased TPC content in F-MBDF (See Section 3.4.5). This property of high nitrite adsorption capacity provides FMBDF a potential to be used as functional food in protecting against gastric cancer development.

Table 2 The SCAC and GAC of UF-MBDF and F-MBDF. Samples UF-MBDF F-MBDF

SCAC(μmol/g) a

75.1 ± 1.0 105.6 ± 0.6b

GAC(μmol/g) 2424.4 ± 0.8a 3376.7 ± 1.2b

UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from Bacillus natto fermented millet bran; SCAC, sodium cholate adsorption capacity; GAC, glucose adsorption capacity. a,bDifferent small letters within a column mean significant difference (P < 0.05).

3.4.4. Cation exchange capacity It was reported that the main functional groups in fiber related to 84

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

Table 3 The cation exchange capacity (mmol/100 mg) of UF-MBDF and F-MBDF. Samples

UF-MBDF F-MBDF

Binding time (h) 2

4

6

8

10

24

1.23 ± 0.05 1.40 ± 0.01

1.23 ± 0.11 1.39 ± 0.10

1.24 ± 0.01 1.39 ± 0.06

1.24 ± 0.03 1.40 ± 0.04

1.21 ± 0.24 1.38 ± 0.17

1.24 ± 0.02 1.40 ± 0.01

UF-MBDF, dietary fiber from unfermented millet bran; F-MBDF, dietary fiber from Bacillus natto fermented millet bran.

References

CEC were carboxylic and hydroxyl phenolic groups, which could produce a function similar to weak acidic cation exchange resin and reversibly interact with cations (Zheng & Li, 2018). The results shown in Table 3 indicated that the CEC of F-MBDF was a little higher than that of UF-MBDF, but the difference was not significant (P > 0.05). Adsorption time had no significant effect on the CEC of both MBDFs. Here the ECE values of F-MBDF and UF-MBDF were higher than that of dietary fibers from wheat bran (0.48 mmol/g) and soybean hull (0.52 mmol/g) (Zhang et al., 2011). DFs with high CEC values would entrap, destabilize, and disintegrate the micelles of lipid, thus retarding the diffusion, absorption and utilization of lipids and cholesterol, further resulting in the reduction of blood cholesterol (Lan, Chen, Chen, and Tian, 2012). The high cholesterol adsorption capacity of F-MBDF might be related to its high CEC.

AACCI (1999). Method 32-07.01. Soluble, insoluble, and total dietary fiber in foods and food productsApproved Methods of Analysis of AACC International (11th ed.). St. Paul, MN, USA: AACC International. Bhise, S., & Kaur, A. (2017). Synergistic effect of polyols and fibres on baking, sensory and textural quality of bread with improved shelf life. International Journal of Current Microbiology and Applied Sciences, 6(11), 1–12. Bijalwan, V., Ali, U., Kesarwani, A. K., Yadav, K., & Mazumder, K. (2018). Hydroxycinnamic acid bound arabinoxylans from millet brans-structural features and antioxidant activity. International Journal of Biological Macromolecules, 88, 296–305. Carvalho, A. F. U., Portela, M. C. C., Sousa, M. B., Martins, F. S., Rocha, F. C., Farias, D. F., & Feitosa, J. P. A. (2009). Physiological and physico-chemical characterization of dietary fibre from the green seaweed Ulva fasciata Delile. Brazilian Journal of Biology, 69(3), 969–977. Chen, J. L., Gao, D. X., Yang, L. T., & Gao, Y. X. (2013). Effect of microfluidization process on the functional properties of insoluble dietary fiber. Food Research International, 54, 1821–1827. Chen, Y., Ye, R., Yin, L., & Zhang, N. (2014). Novel blasting extrusion processing improved the physicochemical properties of soluble dietary fiber from soybean residue and in vivo evaluation. Journal of Food Engineering, 120(1), 1–8. Cheng, L., Zhang, X. M., Hong, Y., Li, Z. F., Li, C. M., & Gu, Z. B. (2017). Characterization of physicochemical and functional properties of soluble dietary fibre from potato pulp obtained by enzyme-assisted extraction. International Journal of Biological Macromolecules, 101, 1004–1011. Cui, J., Gu, X., Zhang, Q. H., Ou, Y. J., & Wang, J. Z. (2015). Production and anti-diabetic activity of soluble dietary fiber from apricot pulp by Trichoderma viride fermentation. Food & Function, 6(5), 1635–1642. Dai, F. J., & Chau, C. F. (2017). Classification and regulatory perspectives of dietary fiber. Journal of Food and Drug Analysis, 25, 37–42. Devi, P. B., Vijayabharathi, R., Sathyabama, S., Malleshi, N. G., & Priyadarisini, V. B. (2014). Health benefits of finger millet (L.) polyphenols and dietary fibre: A review. Journal of Food Science and Technology, 51(6), 1021–1040. Elleuch, M., Bedigian, D., Roiseux, O., Besbes, S., Blecker, C., & Attia, H. (2011). Dietary fibre and fibre-rich by-products of food processing: Characterisation, technological functionality and commercial applications: A review. Food Chemistry, 124, 411–421. Fuller, S., Tapsell, L. C., & Beck, E. J. (2018). Creation of a fibre categories database to quantify different dietary fibres. Journal of Food Composition and Analysis, 71, 36–43. Kabir, A. U., Samad, M. B., D’Costa, N. M., Akhter, F., Ahmed, A., & Hannan, J. M. A. (2014). Anti-hyperglycemic activity of Centella asiatica is partly mediated by carbohydrase inhibition and glucose-fiber binding. BMC Complementary and Alternative Medicine, 14, 31–44. Kang, L. J., Kou, F., Shen, M., Wang, W. H., & Cao, L. K. (2017). Optimization of modification process for millet bran dietary fiber and structural elucidation. Food Science (China), 38(2), 240–247. Lamuela-Raventós, R. M., Singleton, V. L., & Orthofer, R. (1998). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Exercises in general chemistry and qualitative analyses (pp. 152–178). J. Wiley & sons. Lan, G. S., Chen, H. X., Chen, S. H., & Tian, J. G. (2012). Chemical composition and physicochemical properties of dietary fiber from Polygonatum odoratum as affected by different processing methods. Food Research International, 49, 406–410. Ma, G. L., Lu, J. B., & Cao, Q. (2015). Research on separation of lignin, hemicellulose, cellulose from corn straw. Journal of Agricultural Science and Technology, 17(6), 70–79. Ma, M. M., & Mu, T. H. (2016). Modification of deoiled cumin dietary fiber with laccase and cellulose under high hydrostatic pressure. Carbohydrate Polymers, 136, 87–94. Marconi, E., Ruggeri, S., Cappelloni, M., Leonardi, D., & Carnovale, E. (2000). Physicochemcial, nutritional and microstructure characteristics of chickpeas (Cicer arietinum L.) and common beans (Phaseolus valgaris L.) following microwave cooking. Journal of Agricultural and Food Chemistry, 48(12), 5986–5994. Min, Z. M., Gao, L., Gao, Y. Z., Xu, C. H., Deng, X. X., & Xiao, Z. G. (2018). Optimization of the preparation process for soluble dietary fiber from rice bran by Aspergillus niger fermentation and its physicochemical properties. Food Science(China), 39(2), 112–118. Møller, M. E., Dahl, R., & Bøckman, O. C. (1988). A possible role of the dietary fibre product, wheat bran, as a nitrite scavenger. Food & Chemical Toxicology, 26(10), 841–845. NHFPC (2016). GB/T5009. National food safety standards of China. Approved Methods of National Health and Family Planning Commission of People's Republic of China. Niu, Y. G., Li, N., Xia, Q., Hou, Y. W., & Xu, G. N. (2018). Comparisons of three modifications on structural, rheological and functional properties of soluble dietary fibers from tomato peels. LWT, 88, 56–63.

3.4.5. Antioxidant activity In this work, the TPC and DPPH free radical scavenging activity of F-MBDF were 7.02 ± 0.01 mg/g and 81.11 ± 0.59%, respectively, which both were significantly higher than those of UF-MBDF, 3.05 ± 0.01 mg/g and 41.92 ± 0.27% (P < 0.05). It was observed that there was a positive correlation between the TPC and DPPH free radical scavenging activity. Fermentation probably helped to dissolve the total phenols as well as improve the extraction efficiency. The increased TPC contributed to the DPPH free radical scavenging capacity, which was consistent with previous report (Zhu et al., 2015). 4. Conclusion Results showed that fermentation of millet bran with B. natto led to the structural change of MBDF, and yielded a kind of health beneficial dietary fiber with high SDF content. Dietary fiber from B. natto fermented millet bran had many remarkable physicochemical characteristic such as good water holding capacity, water swelling capacity, oil binding capacity and functional characteristic such as nitrite ion absorption capacity, cholesterol adsorption capacity, bile acid adsorption capacity and glucose adsorption capacity. Total phenolic content and DPPH free radical scavenging capacity increased after B. natto fermentation treatment. Strong correlation was observed among total phenolic content and DPPH free radical scavenging capacity. In general, B. natto fermentation treatment can not only benefit the yield of SDF, but also improve some physicochemical and functional properties of millet bran dietary fiber, which make the millet bran dietary fiber find many applications as inexpensive non-caloric bulking agents, quality enhancers of water and oil retention in baked goods, dairy, meat and fruits products. Further research about the functional properties of dietary fiber from fermented millet bran in vivo will be done. Declaration of Competing Interest The authors declare no competing financial interest. Acknowledgments This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. 85

Food Chemistry 294 (2019) 79–86

J. Chu, et al.

and ligin in rice hull. Cereal & Feed Industry, 8, 40–41. Yalegama, L., Karunaratne, D. N., Sivakanesan, R., & Jayasekara, C. (2013). Chemical and functional properties of fibre concentrates obtained from by-products of coconut kernel. Food Chemistry, 141(1), 124–130. Yu, G. Y., Bei, J., Zhao, J., Li, Q. H., & Cheng, C. (2018). Modification of carrot (Daucus carota Linn. var. Sativa Hoffm.) pomace insoluble dietary fiber with complex enzyme method, ultrafine comminution, and high hydrostatic pressure. Food Chemistry, 257, 333–340. Zhang, H. J., Wang, H. N., Cao, X. R., & Wang, J. (2018). Preparation and modification of high dietary fiber flour: A review. Food Research International, 113, 24–35. Zhang, M., Bai, X., & Zhang, Z. (2011). Extrusion process improves the functionality of soluble dietary fiber in oat bran. Journal of Cereal Science, 54, 98–103. Zhang, N., Huang, C., & Ou, S. (2011). In vitro binding capacities of three dietary fibres and their mixture for four toxic elements, cholesterol, and bile acid. Journal of Hazardous Materials, 186(1), 236–239. Zheng, Y. J., & Li, Y. (2018). Physicochemical and functional properties of coconut (Cocos nucifera L) cake dietary fibres: Effects of cellulase hydrolysis, acid treatment and particle size distribution. Food Chemistry, 257, 135–142. Zheng, Y. J., Li, Y., Xu, J. G., Gao, G., & Niu, F. G. (2018). Adsorption activity of coconut (Cocos nucifera L.) cake dietary fibers: Effect of acidic treatment, cellulase hydrolysis, particle size and pH. RSC Advances, 8, 2844–2850. Zhu, F. M., Du, B., & Xu, B. (2015). Superfine grinding improves functional properties and antioxidant capacities of bran dietary fibre from Qingke (hull-less barley) grown in Qinghai-Tibet Plateau, China. Journal of Cereal Science, 65, 43–47. Zhu, Y., Chu, J. X., Lu, Z. X., Lv, F. X., Bie, X. M., Zhang, C., & Zhao, H. Z. (2018). Physicochemical and functional properties of dietary fiber from foxtail millet (Setaria italic) bran. Journal of Cereal Science, 79, 456–461.

Palaniappan, A., Yuvaraj, S. S., Sonaimuthu, S., & Antony, U. (2017). Characterization of xylan from rice bran and finger millet seed coat for functional food applications. Journal of Cereal science, 75, 296–305. Qi, J., Li, Y., Masamba, K. G., Shoemaker, C. F., Zhong, F., Majeed, H., & Ma, J. G. (2016). The effect of chemical treatment on the in vitro hypoglycemic properties of rice bran insoluble dietary fiber. Food Hydrocolloids, 52, 699–706. Qiu, J. Y., Chen, L. L., Wang, W. M., Liu, X. Y., Sun, X., Chen, J. A., & Du, F. L. (2010). Advancement of high-quality dietary fiber preparation by fermentation. Food and Nutrition in China, 6, 24–27. Saiga, A. I., Tanabe, S., & Nishimura, T. (2003). Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. Journal of Agricultural and Food Chemistry, 51(12), 3661–3667. Sangnark, A., & Noomhorm, A. (2003). Effect of particle sizes on functional properties of dietary fiber prepared from sugarcane bagasse. Food Chemistry, 80, 221–229. Sivam, A. S., Sun-Waterhouse, D., & Perera, C. O. (2013). Application of FT-IR and Raman spectroscopy for the study of biopolymers in breads fortified with fibre and polyphenols. Food Research International, 50(2), 574–585. Threapleton, D. E., Greenwood, D. C., Evans, C. E., Cleghorn, C. L., Nykjaer, C., Woodhead, C., ... Burley, V. J. (2013). Dietary fibre intake and risk of cardiovascular disease: Systematic review and meta-analysis. BMJ, 347, f6879. Tosh, S. M., & Yada, S. (2010). Dietary fibres in pulse seeds and fractions: Characterization, functional attributes and applications. Food Research International, 43, 450–460. Wen, Y., Niu, M., Zhang, B. J., Zhao, S. M., & Xiong, S. B. (2017). Structural characteristics and functional properties of rice bran dietary fiber modified by enzymatic and enzyme-micronization treatments. LWT – Food Science and Technology, 75, 344–351. Xiong, S. M., Zuo, X. F., & Zhu, Y. Y. (2005). Determination of cellulose, hemi-cellulose

86