Spray-dried xylooligosaccharides carried by gum Arabic

Industrial Crops & Products 135 (2019) 330–343

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Spray-dried xylooligosaccharides carried by gum Arabic a

a,b,e,⁎

c

a

a

a,b,e

Liangqing Zhang , Xianhai Zeng , Jiarong Qiu , Juan Du , Xuejuan Cao , Xing Tang ⁎ Yong Suna,b,e, Shuirong Lia,b,e, Tingzhou Leid, Shijie Liuf, Lu Lina,b,e,

,

T

a

College of Energy, Xiamen University, Xiamen 361102, China Xiamen Key Laboratory of High-valued Conversion Technology of Agricultural Biomass, 361102, China Key Laboratory of Food Processing and Quality Control, College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China d Henan Key Laboratory of Biomass Energy, Huayuan Road 29, Zhengzhou 450008, China e Fujian Engineering and Research Center of Clean and High-valued Technologies for Biomass, Xiamen University, Xiamen 361102, China f SUNY-College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210, USA b c

ARTICLE INFO

ABSTRACT

Keywords: Xylooligosaccharides Spray drying Modelling Gum Arabic Antioxidant activity Physicochemical and morphological characterization

Prebiotic xylooligosaccharides (XOS) are derived from xylan-rich agricultural residues and have important applications in the food, pharmaceutical, and cosmetic fields. The high hygroscopicity and low glass transition temperature (Tg) of XOS could result in operating problems and deterioration of product quality during the drying process and storage, so it is important to enhance physicochemical properties of dried product for improve XOS quality. The objectives of this work were spray drying XOS and comprehensive studying their rheological properties, physicochemical, and morphological characterization, when carried by gum Arabic (GA). The antioxidant effects of the products were evaluated by 2,2-Diphenyl-1-picrylhydrazyl (DPPH), 2,2′-Azinobis (3-ethylbenzothiazoline-6-sulfonic acid ammonium salt) (ABTS+), ferric reducing antioxidant power (FRAP), and oxygen radical absorbance capacity (ORAC). The intuitive perturbation plot was applied to analyse the effects of the independent variables on the responses. A polynomial equation and the Gordon-Taylor equation were used to model the experimental data, and the fitted equations revealed the powder quality and storage stability well (R2 > 0. 95). The molecular weight of the carbohydrate affected the rheological properties and Tg. Increasing the solid content of the initial solution tended to increase the apparent viscosity and median diameter. The EC50 values of representative products were 1126.00 and 651.69 μg/mL by DPPH and ABTS+ assays, and antioxidant activity values of representative products were 49.68 and 64.95 μmol TE/g by FRAP and ORAC assays, which shown the remarkable antioxidant effects. The drying yield, hygroscopicity, Tg, microencapsulating efficiency, and colour attributes (L*, a*, and b*) of representative high GA concentration (GAC) products were 76.10%, 13.00 g H2O/100 g dry weight, 71.10°C, 99.69%, 96.93, 1.13, and 3.66, respectively, which shown better quality properties than low GAC products. According to the X-ray diffraction and scanning electron microscopy analysis, the microparticles were amorphous, and well-separated under an appropriate GAC. The Fourier transform infrared spectra results shown that the XOS and GA preserved their structural integrity during the spray drying process.

1. Introduction Currently, xylooligosaccharides (XOS) as emerging prebiotics have attracted tremendous attention (Rajagopalan et al., 2017). Xylooligosaccharides are sugar oligomers made of 2–7 xylose (Xyl) units linked by β-1, 4 linkages (Chen et al., 2016). Xylooligosaccharides are mainly produced from hydrolysis of hemicellulose (Li et al., 2016), which are present in many lignocellulosic materials, including corncobs, straws, hardwoods, and hulls (Vazquez et al., 2000). Xylooligosaccharides exhibit potential for applications in the pharmaceutical industry and ⁎

functional foods due to their properties with health benefits, such as being an antioxidative, non-cariogenicity, anti-cancerous, and positive effects on type II diabetes and immunomodulatory activity (GonzálezGarcía et al., 2018; Rajagopalan et al., 2017; Wan Azelee et al., 2016). As potential applications for human consumption and substitutes for antibiotics in feed, XOS have enormous market potential and economic benefits (Álvarez et al., 2017; Zhang et al., 2016). A powder-based product has many merits, such as convenience for consumption, a longer shelf-life, protection for the main bioactive components and ease of handling. Spray drying is one of the most

Corresponding authors at: College of Energy, Xiamen University, Xiamen 361102, China. E-mail addresses: [email protected] (X. Zeng), [email protected] (L. Lin).

https://doi.org/10.1016/j.indcrop.2019.04.045 Received 28 August 2018; Received in revised form 17 April 2019; Accepted 19 April 2019 Available online 09 May 2019 0926-6690/ © 2019 Elsevier B.V. All rights reserved.

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conventional powder-production technologies applied in the food industry due to its high production capacity, low processing cost, the availability of equipment, and producing high-quality products (Cao et al., 2018; Tupuna et al., 2018). However, there are certain inherent drawbacks associated with spray drying high sugar-rich XOS, as demonstrated in this work, such as stickiness, hygroscopicity, caking, and surface liquefaction, occurring during the spray drying process and storage, leading to an inferior quality, a lower drying yield, and packaging and utilization difficulties. In this case, encapsulation is widely used to avoid these technological problems (Karadeniz et al., 2018). The selection of a suitable microcapsule is of paramount importance to producing a high-quality powder product. Gum Arabic (GA) is primarily used as a stabilizer in the food industry (Suhag et al., 2016; Zokti et al., 2016). Gum Arabic is a hydrocolloid with polysaccharide chains containing a small fraction of protein, which is a suitable emulsifier with a high water solubility and skin-forming property. Gum Arabic can also help increase the glass transition temperature (Tg), reduce the hygroscopicity and caking, and improve the physicochemical properties of the obtained powder (Bhusari et al., 2014; Krishnaiah et al., 2014). Moreover, the use of GA as a carrier for microencapsulation with prebiotic properties, dietary fibre actions, and other health-related benefits (Cherbut et al., 2003) could endow powder with more functional properties. Therefore, this work aims to evaluate the effects of the processing conditions on the physicochemical characteristics and antioxidant activity of spray-dried XOS by using GA as the microcapsule. The rheological properties of the initial solutions, and the modelling equations are also assessed. This study contributes to the technology development for manufacturing XOS and other sugar-rich carbohydrate powders.

Table 1 Experiment design for the spray drying assays. Assays T (°C) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

160.00 160.00 130.00 160.00 160.00 160.00 160.00 160.00 160.00 210.45 130.00 130.00 190.00 190.00 160.00 109.55 190.00 130.00 190.00 160.00

(0) (0) (−1) (0) (0) (0) (0) (0) (0) (1.68) (−1) (−1) (1) (1) (0) (−1.68) (1) (−1) (1) (0)

XC (%)

GAC (%)

Outlet air temperature (°C)

2.45 (−1.68) 26.00 (0) 40.00 (1) 49.55 (1.68) 26.00 (0) 26.00 (0) 26.00 (0) 26.00 (0) 26.00 (0) 26.00 (0) 40.00 (1) 12.00 (−1) 12.00 (−1) 40.00 (1) 26.00 (0) 26.00 (0) 12.00 (−1) 12.00 (−1) 40.00 (1) 26.00 (0)

10.00 (0) 10.00 (0) 15.00 (1) 10.00 (0) 1.59 (−1.68) 10.00 (0) 18.41 (1.68) 10.00 (0) 10.00 (0) 10.00 (0) 5.00 (−1) 5.00 (−1) 5.00 (−1) 15.00 (1) 10.00 (0) 10.00 (0) 15.00 (1) 15.00 (1) 5.00 (−1) 10.00 (0)

61.00 65.40 65.20 73.00 63.00 65.80 69.50 65.40 65.90 86.70 63.00 55.60 75.00 88.30 65.70 56.00 77.40 59.80 84.00 66.00

Note: % means the solids fraction in the feed solution (weight/volume). Values in the parenthesis (−1.68, −1, 0, +1, and +1.68) represent the coded variables. T: inlet air temperature. XC: xylooligosaccharides concentration. GAC: gum Arabic concentration.

and the resulting solution was decolorized with activated carbon (0.5% w/v). Then, ultrafiltration/nanofiltration membranes, electrodialysis, and rotary evaporator were used to purify and concentrate the extract and finally to obtain 50.69% w/v XOS solution.

2. Materials and methods 2.1. Materials The corncob was obtained from local farmers and was washed before being sun-dried. Next, the corncob was ground to a particle size of 10 mesh to 20 mesh and stored at room temperature until further treatment. Gum Arabic from acacia tree (Robinia pseudoacacia L.), was obtained from Sigma-Aldrich (Sigma-Aldrich, China). The standards of xylobiose (Xyl2), xylotriose (Xyl3), xylotetraose (Xyl4), xylopentaose (Xyl5), and xylohexose (Xyl6) were purchased from Yikuo (Yikuo Corporation, China). Glucose, arabinose, and Xyl were obtained from Sinopharm (Sinopharm Group Corporation, China) and were used as standards. Fluorescein sodium salt, 2,2′-Azobis (2-methylpropionamidine) dihydrochloride (AAPH), 2,2′-Azinobis (3-ethylbenzothiazoline6-sulfonic acid ammonium salt) (ABTS+), 2,2-Diphenyl-1-picrylhydrazyl (DPPH), potassium persulfate, 2,4,6-Tris (2-pyridyl)-s-triazine (TPTZ), and ( ± )-6-Hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid (Trolox) were obtained from Aladdin (Aladdin Industrial Corporation, China). All chemicals were of analytical reagent grade in this study.

2.3. Design of drying experiments Central composite design was applied to investigate the effects of the inlet air temperature (T) (x1), XOS concentration (XC) (x2), and gum Arabic concentration (GAC) (x3) on the drying yield (y1), moisture content (y2), hygroscopicity (y3), Tg (y4), and microencapsulation efficiency (MEE) (y5). Three independent variables with five levels (−1.68, −1, 0, +1, and +1.68), including six repetitions at the central point and two axial points, totaling 20 assays (recorded as assay 1, assay 2, assay 3…assay 20) were used (Table 1). In addition, the variation in outlet air temperatures with various drying conditions were presented in Table 1. 2.4. Preparation of XOS mixture with gum Arabic and spray drying Gum Arabic was dissolved in distilled water before adding the XOS for preparation of XOS mixture with gum Arabic (Table 1). The mixtures were homogenized for 10 min at 5000 rpm using a Colour Squid (IKA Guangzhou, China) until fully dissolved and mixed. A lab-scale spray dryer was utilized for spray drying (RY-1500, Ruiyuan Corporation, China). The atomizer consists of a two-fluid nozzle with a diameter of 2.0 mm. The cylindrical spray chamber is made of transparent glass with 18 cm long and 20 cm in diameter. The parameters of spray drying were: 13 r/min (6.5 mL/min) feed flow rate (controlled by peristaltic pump), 54.96 Hz fan frequency, and 2 bar compressor pressure. Spray drying of the feed liquid was carried out when reaching the desired constant inlet air temperature (Table 1). The powder was collected from the recovery chamber and the cyclone, and was immediately aliquoted and sealed in PA/PE vacuum bags and were stored at 25°C until the next experimental steps.

2.2. Production of XOS extraction Feed solution was extracted from the corncob using the modified methods as reported by Pang et al. (2012) and Bian et al. (2013). Briefly, an appropriate weight of MgO, corncob, and distilled water were added to our own-developed and designed ball-shaped digester for cooking under 2.0 MPa oxygen pressure at 165°C for 3 h. After cooking and separating lignin, the obtained pulp was washed with distilled water for 2–3 times. The Highsun xylanase (Jining Highsun Biotech Co., Ltd., China), pulp, and distilled water were added to the fermenter in an appropriate weight for fermentation at 50°C, pH of 4.5–5.0, and 80 rpm for 7 h, and the weight ratio of pulp to distilled water is 1 to 20. After the enzymatic hydrolysis, the residue in the hydrolysate was filtered, 331

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2.5. Process modelling

intervals during one week. Eq. (9) was used to calculate the hygroscopicity:

The response values were modelled with polynomial equation, as shown in Eq. (1):

y = a+ bx1 + cx2 + dx3 + ex1 x2 + fx1 x3 + gx2 x3 + hx12 + ix2 2 + jx3 2

Hygroscopicity(%) = (Wt

5.12x1

5.71x12

y2 = 3.06 +

0.88x1

0.13x12

5.62x2 + 9.92x3

7.28x2 2

+ 0.50x2 + 0.17x3

y3 = 16.74 + 1.17x1 + 1.16x2 0.18x12

(2)

0.69x2 + 0.12x3 + 0.14x1 x2 + 0.17x1 x3 2

0.36x2 + 0.14x3

(3)

0.28x1 x3 + 0.07x2 x3 (4)

2

y4 = 63.14 + 1.95x1 + 3.17x2 + 2.85x3 + 0.72x1 x2 + 0.69x1 x3 0.03x12 y5 = 97.33

0.35x2 x3 (5)

1.17x2 2 + 0.67x3 2

0.89x1

1.24x12

0.17x2 x3

2

1.01x3 + 0.10x1 x2

2

1.61x2 + 3.34x3

0.14x2

2

1.17x3

2.8.3. Measurement and modelling of glass transition temperature (Tg) A differential scanning calorimeter (DSC 214 Polyma, Netzsch, Germany) was used to determine the Tg (including the dried products and the samples prepared using different saturated salt solutions). Powder that were 5–10 mg were placed in aluminium hermetic pans (50 μL), were cooled to −30°C at 10 °C/min, were equilibrated for 6 min, were heated to 200°C at 10 °C/min, and finally were cooled to 25°C at 10 °C/min. High purity nitrogen was used as the protective gas (50 mL/min), and liquid nitrogen was used to cool the samples. The results were expressed as the onset temperature of the abrupt change in the apparent heat capacity. Samples with different levels of water content that were prepared using various salt solutions were used to model the Gordon-Taylor equation. Approximately 2.00 g of powder (drying conditions with 160.00°C, 26.00% XC, and 10.00% GAC) were placed in sealed vessels, which contained various saturated salt solutions (LiCl, CH3COOK, MgCl2, K2CO3, NaBr, NaCl, KCl, and BaCl2 with aw ranging from 0.11–0.90) to obtain various relative humidity levels within 24 h at 25°C for the prepared different moisture levels of the samples. The Gordon-Taylor equation (Gordon and Taylor, 1952) is provided as Eq. (10):

2.10x1 x2 + 0.07x1 x3 + 0.78x2 x3

5.53x3 2

0.86x1 x2 + 0.57x1 x3 + 0.87x2 x3

2

(6)

Tg = 2.6. Rheological measurement

n

(7)

(Xs + kXw )

(10)

2.8.4. Determination of MEE using high-performance liquid chromatography (HPLC) A Waters e2695 HPLC apparatus (Waters, USA) was utilized to detect the MEE. Separation was performed on a Sugar KS-802 (Showa Denko, Japan) column at 80°C, and used distilled water as the mobile phase at a 0.6 mL/min flow rate. Eqs. (11) and (12) were used to calculate the content of XOS2–4 (XOS with the degree of polymerization from 2 to 4) and XOS (g per100 g sample):

where σ, v, γ, and n represent the shear stress (Pa), consistency coefficient (Pa·sn), shear rate (s− 1), and flow behaviour index, respectively. The model parameters v and n were evaluated using the non-linear regression analysis of OriginPro 2016 (OriginLab Corporation, USA). 2.7. Drying yield A sugar refractometer (CNT 65, Lohang Corporation, China) was used to determine the total mass of the liquid extract. Eq. (8) was used to calculate the drying yield:

Amount of spray dried powder Drying yield(%) = × 100 Amount of extract and GA

(Xs Tgs + kXw Tgw)

where Xs, Xw, and k stand for the solids mass fraction (g/g), water mass fraction (g/g), and Gordon-Taylor parameter, respectively, and Tgw and Tgs are the glass transition temperature of amorphous water (−135°C) and anhydrous solids (°C), respectively. The model parameters k and Tgs were evaluated using the non-linear regression analysis of OriginPro 2016.

The flow characteristic of the fluid was evaluated using an ARES rheometer (TA Instruments, USA), which was operated using a specific set of disks with a 25 mm diameter and a 1 mm gap at 25°C (10 mL sample volume). The data were modelled with Ostwald power law, as shown in Eq. (7):

=v

(9)

where W0 is the initial sample mass, and Wtis the sample mass as measured at daily intervals.

(1)

where y represents the experimental response; a, b, c, d, e, f, g, h, i, and j represent regression coefficients; x1, x2, and x3 are the coded independent variables. According to the regression coefficients of Table S1 (cf. Subsection 3.2 in Supplementary material for a more detailed analysis), the secondorder polynomial equations that describe the drying yield, moisture content, hygroscopicity, Tg, and MEE in terms of coded values are shown in Eqs. (2)–(6):

y1 = 69.51

W0 ) × 100

XOS2-4 =

(8)

XOS =

[a2 × F1 + (a3 + a4 ) × F2] × C × V × 100 a1 × m × 1000

(11)

[a2 × F1 + (a3 + a4 + a5 + a6 + a7 ) × F2] × C × V × 100 a1 × m × 1000 (12)

2.8. Microparticles characterization

where C, m, V, and a1 stand for the concentration of a standard solution of Xyl, the sample mass, the sample volume, and peak area of Xyl standard solution, respectively; a2, a3, a4, a5, and a6 represent the sample peak areas of Xyl2, Xyl3, Xyl4, Xyl5, and Xyl6, respectively; a7 represents the total peak area of XOS with a degree of polymerization above 6, and F1 and F2 (conversion coefficient) are 0.93 and 0.94. Chemical compounds of the liquid extract were identified as 92.42 g XOS2–4 (XOS with the degree of polymerization from 2 to 4) per 100 g sample and 5.73 g XOSn > 4 (XOS with the degree of polymerization greater than 4) per 100 g sample. Eq. (13) was used to calculate the XOS2–4 (%):

2.8.1. Moisture content The moisture content was determined gravimetrically (3–5 g powder) by a vacuum drying at 65°C to a constant mass. 2.8.2. Hygroscopicity A modified method of that described by Cai and Corke (2000) was used to determine the hygroscopicity. The sample (1.00 g) was weighed, placed on a dish and placed into a vessel with a saturated sodium chloride solution at 25°C to determine the hygroscopicity (relative humidity of 75.3%). The gain in weight was recorded at daily 332

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XOS2-4 (%) =

XOS2-4 content of final product × 100 XOS content of initial solution

2.8.6.3. Iron (III) reduction to iron (II). Ferric reducing antioxidant power (FRAP) was detected using the modified method as reported by Boneza and Niemeyer (2018). The FRAP reagent was freshly prepared [10 mM of TPTZ dissolved in 40 mM hydrochloric acid, 300 mM of acetate buffer (pH 3.6), and 20 mM aqueous iron (III) chloride hexahydrate in a ratio of 1:10:1]. Briefly, 100 μL of FRAP solution was mixed with 100 μL of the test sample (3000 μg/mL) in a white 96well microplate, shaken for 1 min and incubated at 37°C for 30 min before the absorbance was measured at 593 nm using a multimode microplate reader (TECAN Infinite M200 PRO, Switzerland). Similarly, the standard solution of Trolox (1.6–100 μg/mL, dissolved in ethanol) was prepared for a calibration curve (y = 0.0445x+0.0165, r2 = 0.9996) and the results were reported as μmol Trolox equivalent (TE) per g sample (μmol TE/g sample).

(13)

Microencapsulation efficiency (%) was calculated using Eq. (14):

Microencapsulation efficiency(%) =

XOS content of final product × 100 XOS content of initial solution (14)

2.8.5. Colour measurements Powder colour was determined using an ADCI-2000 (Chentaike Corporation, China) to obtain the CIELab attributes (L*, lightness, 0—black, 100—white; a*, 0–60, red intensity; b*, 0–60, yellow intensity). 2.8.6. Antioxidant assay 2.8.6.1. Evaluation of antioxidant activity capacity by DPPH. Antioxidant capacity of initial solutions, GA, Xyl, and dried products were evaluated by testing the free radical DPPH with the modified method of dos Santos et al. (2018). Water was used as the solvent for the test samples, and prepared solutions with the concentrations of 125, 250, 500, 1000, 2000, 3000, and 4000 μg/mL for each sample. A 2 mL ethanol solution with a DPPH concentration of 0.1 mmol/L was prepared and the aforementioned dissolved samples (2 mL) were added into the prepared solution. A 200 μL of the mixed solution was loaded into the white 96-well microplate after 120 min incubation at room temperature. The absorbance was detected at 517 nm using a multimode microplate reader (TECAN Infinite M200 PRO, Switzerland). The DPPH radical scavenging was calculated using Eq. (15):

DPPH radical scavenging(%) = (

Ac

As Ac

) × 100

2.8.6.4. Oxygen radical absorbance capacity (ORAC). The ORAC was detected according to the modified method of Kang et al. (2017) by using fluorescein as a fluorescent probe. Trolox (1.6–100 μg/mL), 0.956 μmol/L of fluorescein sodium salt, AAPH, and the sample (3000 μg/mL) were made daily in a 75 mM of phosphate buffer (pH 7.4). A standard curve of Trolox was used to determine the antioxidant activity of the samples (y = 1.647x+1.5913, r2 = 0.9996). Briefly, 50 μL of the fluorescein working solution and 50 μL of AAPH were mixed with 100 μL of the test sample in a black 96-well microplate, shaken for 1 min and incubated at 37°C for 20 min. The fluorescein intensity was measured at intervals of 2 min for 120 min at 485 nm excitation and 535 nm emission, in a multimode microplate reader (TECAN Infinite M200 PRO, Switzerland). The ORAC radical scavenging capacity was based on the calculation of the area under the curve (AUC), using Eq. (17):

(15)

AUC = 1 +

where Ac is the absorbance of the control without the sample, As is the absorbance with the presence of the dissolved samples. The antioxidant activity of the samples was expressed as EC50, as the antioxidant concentration providing 50% reduction of DPPH radicals. The EC50 was established with the nonlinear regression using the GraphPad Prism Software (GraphPad Software, San Diego, USA). Trolox (1.6–100 μg/mL, dissolved in ethanol), a reference antioxidant, was used to compare with the antioxidative capacities of the samples.

Ac

As Ac

) × 100

+

f2 f0

+…

fi f0

+…

f59 f0

+

f60 f0

(17)

where f0: initial fluorescence reading at cycle 0, fi: fluorescence reading at cycle i. The net AUC was obtained by subtracting the AUC of the negative control from that of the test sample. The results were expressed as μmol TE/g sample. 2.8.7. Particle size and distribution A LISST-100X Type-B (Sequoia Scientific, USA) was carried out to determine the particle size. The measurements were conducted in a liquid dispersion using ethanol. The particle size distribution is expressed as a volumetric concentration (μL/L) of the sample within each size interval.

2.8.6.2. Evaluation of cationic radical scavenging activity by ABTS+. The ABTS+ radical scavenging capacity assay was carried out by using the modified method as reported by da Silva Andrade et al. (2018). The ABTS+ radical solution was obtained by mixing 7 mM of ABTS+ and 2.45 mM potassium persulfate in a ratio of 1:1 and incubated at room temperature in dark at least 14 h, for radical stabilization. Before the test, the ABTS+ radical solution was diluted in methanol with a ratio of 1:30. The solutions with the concentrations of 125, 250, 500, 1000, 2000, 3000, and 4000 μg/mL for each sample (initial solutions, GA, Xyl, and dried products) were prepared, and water was used as the solvent. Trolox (1.6–200 μg/mL) was dissolved in ethanol and used as a standard. A 100 μL of the test sample and 100 μL of ABTS+ radical solution was loaded into the white 96-well microplate. The mixture was shaking for 1 min and incubated at 25°C for 20 min before the absorbance was detected at 734 nm using a multimode microplate reader (TECAN Infinite M200 PRO, Switzerland). Eq. (16) was used to calculate the ABTS+ radical scavenging:

ABTS+radical scavenging(%) = (

f1 f0

2.8.8. Scanning electron microscopy, X-ray diffraction, and Fourier transform infrared spectroscopy The sample morphology was evaluated using scanning electron microscopy (SEM) (S-4800, Hitachi Ltd., Japan). Particles were attached to a specimen stub with double-sided sticky tapes, were coated with approximately 200 Å of gold and were observed with 15 kV at × 2000 magnifications. The X-ray diffraction (XRD) characteristic of the powder was detected using a Rigaku diffractometer (Rigaku Co., Ltd, Japan). The diffraction pattern was recorded at 2θ = 5–90° with a scanning speed of 10°/min at room temperature. The spectra of the physical mixture (mechanical mixing of the two solid constituents of GA and XOS at an equivalent formulation) and the products were scanned using Fourier transform infrared spectroscopy (FT-IR) (Nicolet IR200, Co., Ltd, China) at wavelengths in the range of 4000 cm−1 to 400 cm−1. 2.9. Statistical analysis

(16)

The ABTS+ antioxidant activity was expressed as the EC50, as described previously for the DPPH assay.

The measurements were done in triplicate. The results were expressed as means ± standard deviation using the Duncan multiple test 333

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termed shear thinning) (Yanjun et al., 2014). According to RodeaGonzález et al. (2012), the polymeric fluids system with form of a reversible “structure” or network in the equilibrium state that could result in shear thinning behaviour when the system shears and the structure breaks down. Compared with that of the non-Newtonian fluids, the apparent viscosity values of the Newtonian fluids were much smaller (0.0001–0.1 Pa.s), and nearly remained constant with the increase of the shear rate (Fig. 1b). The consistency coefficient (v) is related to the flow properties and apparent viscosity of a fluid (Botrel et al., 2014). Campelo et al. (2017) also mentioned that the size behaviour of a particle is commonly predicted by the consistency coefficient due to its association with the droplet size that will be atomized and dried. The two key factors that influence apparent viscosity of a polymeric fluid: the solid content and the molecular weight. As shown in Table S2, the higher consistency coefficient value was observed with increasing the solid content in the fluid, indicating a positive correlation between the apparent viscosity and the solid content. Similar results were reported by Klongdee et al. (2012) and Maskan and Göǧüş (2000) in the study of the effect of the chitosan concentration on the rheological properties of lecithin-stabilized emulsions and the effect of sugar on the rheology of sunflower oil–water emulsions, respectively. Additionally, an increase in the XC or GAC resulted in the increase of the consistency coefficient value (Table S2), indicating a higher apparent viscosity of these fluids. However, the apparent viscosity is more affected by the GAC (Table S2). According to Hay et al. (2017), the molecular weight of the polymers in a fluid influences the rheological behaviours, and a low molecular weight will result in a lower apparent viscosity. Apparently, the XOS are oligosaccharides that are composed of Xyl units linked by β-1, 4 xyloside bonds with X2, X3, and X4 as the main components and that have low molecular weight (containing 92.42 g XOS2–4 per 100 g sample); the GA is a thickening agent in food formulations with a ramified structure and long chains, which caused the higher viscosity (Gómez-Díaz et al., 2008). As mentioned by Bakry et al. (2016), high molecular weight molecules in the aqueous phase tend to increase the flow resistance, resulting in an increase in the apparent viscosity of the fluid. The apparent viscosity of the fluid might be associated with the drying yield since increasing the apparent viscosity to an optimal value can minimize the tiny droplets oscillation and prevent the colliding of wet droplets onto the spray chamber and the sufficient drying of the particles, thus reducing wall deposition. In contrast, an excessive increase of the apparent viscosity often interferes with the atomization process, since spraying jet cannot be atomized into tiny droplets normally at high apparent viscosity, occurring wall deposition when large droplets are insufficiently dry, which adversely affects the drying yield (Vishnu et al., 2017). As shown in Tables 1 and 2, there was no direct negative correlation between the apparent viscosity and the drying yield (detailed discussion is presented Subsection 3.2.1), indicating that the viscosities of the assays are within the reasonable range and the GA as a relatively low viscosity carrier is promising for the spray drying of XOS.

Fig. 1. (a) Flow behaviours of the initial solutions; (b) apparent viscosity of the initial solutions as a function of the shear rate (XC: xylooligosaccharides concentration; GAC: gum Arabic concentration).

at the p < 0.05 significant level (SPSS 20.0, SPSS Inc., USA). Design Expert 10.0.6 Software (Stat-Ease, Inc., USA) was used for generating 3D response surface graphs, perturbation plots and the analysis of variance (ANOVA). The ANOVA was used to determine the interaction regression coefficient, quadratic, and regression models. 3. Results and discussion 3.1. Rheological properties The study of the rheological properties of food provides knowledge about the fluid structure and drying behaviour for convenience when producing the specific product (Yanjun et al., 2014). Nine different fluids were prepared according to the experimental design (Table 1). As mentioned by Alves et al. (2016), the flow behaviour index (n) reveals how close the fluid conforms to Newtonian behaviour (n approaching 1 referred to as Newtonian behaviour). For the samples of 2.45% XC, 10.00% GAC and 12.00% XC, 5.00% GAC, the polymeric fluids showed Newtonian behaviour, since the flow behaviour indexes approached 1 (Table S2), and there is a linear relationship between the shear rate and the shear stress (Botrel et al., 2014) (Fig. 1a). While the other polymeric fluids exhibited non-Newtonian characteristics, as indicated by the flow behaviour indexes being significantly lower than 1 (Table S2), with a non-linear correlation between the shear rate and the shear stress (Monsoor, 2005) (Fig. 1a). As shown in Fig. 1b, an increase in the shear rate was accompanied by a decrease in the apparent viscosity, which indicates that the non-Newtonian fluids are a pseudoplastic type (also

3.2. Model fitting and analysis The results of the drying yield, moisture content, hygroscopicity, Tg, and MEE for each assay, are shown in Table 2. The intuitive perturbation plot would help to analyse the effects of independent variables at a reference point in the design space. The influence of the XC, T, and GAC on the drying yield, moisture content, hygroscopicity, Tg, and MEE can be visualized in Fig. S1. 3.2.1. Drying yield Masters (1996) mentioned that wall deposition was the main reason for the decrease in drying yield. A drying yield over 50% is taken as the criterion for a successful spray drying (Bhandari et al., 1997). The extreme value of the response result can be easily identified from the 334

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Table 2 Experimental results of the drying yield, moisture content, hygroscopicity, glass transition temperature (Tg), microencapsulating efficiency (MEE), and median diameter (representative samples). Assays

Drying yield (%)

Moisture content (%)

Hygroscopicity (g H2O/100 g dry weight)

Tg (°C)

MEE (%)

Median diameter (μm)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

60.04 ± 2.18 67.43 ± 1.80 60.84 ± 2.42 41.20 ± 2.98 35.02 ± 3.53 70.64 ± 1.66 76.10 ± 1.25 71.36 ± 1.47 70.26 ± 1.62 45.69 ± 2.73 41.26 ± 2.94 51.46 ± 2.40 44.36 ± 2.88 45.62 ± 2.67 69.21 ± 2.02 64.42 ± 1.80 61.09 ± 2.29 64.80 ± 1.56 28.87 ± 3.92 67.56 ± 1.95

5.90 ± 0.09 3.14 ± 0.04 3.84 ± 0.01 3.22 ± 0.08 3.79 ± 0.02 2.93 ± 004 3.45 ± 0.01 3.15 ± 002 3.05 ± 002 1.99 ± 0.08 3.99 ± 0.08 5.12 ± 0,08 2.81 ± 0.01 2.77 ± 0.02 2.87 ± 0.02 5.03 ± 0.09 4.01 ± 0.06 5.72 ± 0.02 2.17 ± 0.03 3.18 ± 0.07

13.00 16.72 15.35 18.14 18.84 16.65 15.10 16.82 16.64 17.76 16.59 15.07 18.05 17.62 16.81 14.40 15.44 13.66 19.87 16.84

53.90 ± 0.32 63.02 ± 0.27 63.80 ± 0.40 66.23 ± 0.29 59.47 ± 0.33 63.14 ± 0.29 71.10 ± 0.36 62.72 ± 0.24 63.11 ± 0.33 66.47 ± 0.41 61.26 ± 0.30 56.12 ± 0.33 57.55 ± 0.36 70.85 ± 0.21 63.48 ± 0.39 60.14 ± 0.36 64.22 ± 0.24 60.53 ± 0.46 65.09 ± 0.27 63.26 ± 0.24

99.69 ± 0.11 97.22 ± 0.14 98.61 ± 0.17 94.03 ± 0.12 88.35 ± 0.23 97.31 ± 0.14 99.53 ± 0.11 97.29 ± 0.13 97.53 ± 0.15 92.82 ± 0.19 91.87 ± 0.25 94.46 ± 0.15 93.35 ± 0.22 96.33 ± .0.08 97.26 ± 0.12 94.70 ± 0.15 98.92 ± 0.14 98.82 ± 0.15 86.22 ± 0.17 97.40 ± 0.14

4.30 ± 0.12 – – 8.54 ± 0.21 4.66 ± 0.14 5.10 ± 0.14 6.30 ± 0.15 – – 5.73 ± 0.12 – – – – – 4.92 ± 0.11 – – – –

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.15 0.16 0.21 0.27 0.24 0.21 0.14 0.19 0.19 0.22 0.13 0.17 0.24 0.16 0.19 0.15 0.17 0.13 022 0.15

three-dimensional response surface plot. Drying yield of the samples ranged from 28.87 to 76.10% (Table 2). As shown in Fig. S2, the highest drying yield was obtained for the conditions of T = 170.00°C, XC = 30.70%, and GAC = 18.41%. The trend of particular response changes as one factor moves from the design range with the other factors hold constant at the reference value is shown by the perturbation plot (Fig. S1). In this study, the reference point of the perturbation plot is set at the middle of the design space (XC = 26.00%, T = 160.00°C, and GAC = 10.00%). The results of the perturbation plot show that the drying yield initially increased and then decreased with the increase of T and XC (curves A and B in Fig. S1a), and the GAC had a positive effect on the drying yield (curve C in Fig. S1a). Increasing the inlet air temperature caused a slight increase of the drying yield, which can be attributed to higher heat and mass transfer rates and better water removal at higher temperatures, thereby avoiding inadequately dried particles. As the temperature further increased (inlet air temperature/measured outlet air temperature above 190.00°C/75.00°C), which probably caused the particle surfaces to heat beyond the sticky-point temperature (sticky-point temperature, i.e. outlet air temperature generally over 5–20°C above Tg), the drying yield reduced (Bhandari et al., 1997). The drying yield increased with the increase of the GAC, which is attributed to two reasons. First, an increase of the GAC increased Tg of the surface layer and overcame the surface stickiness of particles, thus reducing the powder deposition onto the inner chamber wall (Goula and Adamopoulos, 2005, 2010). Second, as mentioned in subsection 3.1, increasing the apparent viscosity to an optimal value reduces the wall deposition, and hence, the drying yield increases. Regarding the influence of XC on the drying yield, an increase in the XC led to a slightly increased the drying yield, which can be attributed to a higher Tg and apparent viscosity in the systems, while a further increase of the XC, will generate the high hygroscopic powder (prone to stickiness and flow problems), decreasing the drying yield.

the moisture content (curves A and B in Fig. S1b), while the fairly flat line of curve C shows that the moisture content is insensitive to the GAC. Increasing the inlet air temperature led to a greater loss of water due to higher heat transfer to the tiny droplets, resulting in a greater driving force for water evaporation, and a lower moisture content was thus obtained. Increasing the XC slightly reduced the moisture content, which can probably be attributed to an increase in the solids of the feed and a decreased amount of free water for evaporation. This result was consistent with those of other researchers (Fazaeli et al., 2012; Pang et al., 2014; Quek et al., 2007). The moisture content slightly increased with an increase in the GAC, which may be attributed to skin-forming property of GA (Tupuna et al., 2018). The thickness of skin gradually increases as the GAC increases, which progressively reduced the mass transfer and moisture evaporation and thus powders with slightly higher moisture content was observed (Aghbashlo et al., 2012; Hassan and Mumford, 1993a, b; Zhang et al., 2019). Zhang and co-workers studied the drying behaviours of noni juice with GA as a wall material by single droplet drying (Zhang et al., 2019). The result demonstrated that the formation of a surface crust by the GA acted as a barrier that increased activation energy and hindered moisture evaporation in the core, which could possibly impair the further water removal from the droplet. 3.2.3. Hygroscopicity Hygroscopicity is an important parameter for its influence on the food stickiness and caking during processing and storage. The hygroscopicity of the products varied from 13.00 to 19.87 g H2O/100 g dry weight (Table 2). As shown in Fig. S4, the lowest hygroscopicity value was obtained for the conditions of T = 109.55°C, XC = 2.45%, and GAC = 18.41%. The storage behaviour of the representative samples is shown in Fig. 2a. This study proved that GA is a good stabilizer to reduce the hygroscopicity of XOS (Fig. 2a) and that the moisture absorption has approximately no negative influence on the products (e.g., caking and liquefaction; Fig. S7). As shown in Fig. 2a, a higher hygroscopicity occurred on the first day. When the ratio of GA is higher, the hygroscopicity of the product is lower (twice the moisture absorption of 190.00°C, 40.00% XC, and 5.00% GAC), confirming the more hygroscopic nature of the XOS powder. The moisture absorption became slower during the next few

3.2.2. Moisture content Generally, a moisture content below 5% is considered to be good for dried food (Daza et al., 2016). The moisture content of the dried products varied from 1.99 to 5.90% (Table 2). As shown in Fig. S3, the lowest moisture content was obtained for the conditions of T = 209.55°C, XC = 49.55%, and GAC = 1.59%. As shown in Fig. S1b, the T and XC had negative correlations with 335

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Fig. 2. (a) Storage behaviour of the representative samples; (b) particle size distributions of the representative sample; (c) X-ray diffraction patterns of the gum Arabic (GA) and representative samples (XC: xylooligosaccharides concentration; GAC: gum Arabic concentration).

days. A tendency of the hygroscopicity equilibrium was observed during the fifth day of storage (Fig. 2a). From the perturbation plot analysis (Fig. S1c), the T and XC had positive correlations with the hygroscopicity (curves A and B in Fig. S1c), and the GAC had a negative correlation with the hygroscopicity (curve C in Fig. S1c). The hygroscopicity was increased with the increase of the inlet air temperature, due to the increase of the inlet air temperature resulting in a faster drying rate, thus producing products with a lower moisture content. Apparently, the moisture content is relevant to the hygroscopicity (Fig. S1c and Table 2). This result indicates that in addition to the product composition, the moisture content is another factor effect on the hygroscopicity of the sample. Daza et al. (2016) reported that low moisture spray-dried cagaita fruit powder had a greater water concentration gradient and consequently a higher capacity to adsorb moisture from the surrounding air. A higher XC led to the increase of the hygroscopicity due to the powder containing a high ratio of XOS. The high hygroscopicity of the XOS probably correlated with their low molecular weight carbohydrate contents (LMWC). Chu and co-workers studied the hygroscopicity of thirteen dried crude herbal extracts with various relative humidity, and modelled the data with Brunauer-Emmett-Teller and GuggenheimAnderson-de Boer (GAB) model to obtain theoretical amount of monolayer moisture content (Mm) (Chu and Chow, 2000). The result found that the extracts with LMWC had high Mm, indicating high moisture sorption of the LMWC samples. On the contrary, samples with high molecular weight carbohydrates tended towards low Mm, indicating poor hygroscopicity of the samples. The hygroscopic behaviours of different molecular weight carbohydrates samples indicated that the hygroscopicity of dried crude herbal extract was mainly

attribute to the LMWC, not polysaccharide (Chu and Chow, 2000). In addition, Du and Liu mentioned that the critical relative humidity (CRH) of the water-soluble LMWC is equal to multiply the CRH of each component (Du and Liu, 2008). On the basis of summarizing literatures, Du and Liu concluded that the presence of various water-soluble LMWC in the dried extract reduced CRH of the mixture, which was the main reason for the strong hygroscopicity of the extract (Du and Liu, 2008). Apparently, the XOS are water-soluble oligosaccharides with Xyl2, Xyl3, and Xyl4 as the main components, and the CRH decreases with the increase of the XC, hence increase the hygroscopicity of the products. Likewise, Fu and co-workers applied the GAB model to fit the hygroscopic data of galacto-oligosaccharide mixture and found that the galacto-oligosaccharide altered water sorption isotherm which significantly increased the product hygroscopicity (Fu et al., 2019). The GAC had a negative correlation with the hygroscopicity, which might be attributed to the fact that incorporating GA can modify the balance of the hydrophilic/hydrophobic sites of the particles and finally decrease the amount of absorbed moisture. Similar results were reported by Moreira et al. (2009) and Suhag et al. (2016) about spray drying of acerola pomace powder and honey powder, respectively. 3.2.4. Glass transition temperature (Tg) Glass transition temperature is one of the most important parameters in food science. The food stability is related to Tg. A higher Tg value leads to a more stable performance. The Tg values of the samples ranged from 53.90 to 71.10°C (Table 2). As shown in Fig. S5, the highest Tg value was obtained for the conditions of T = 210.45°C, XC = 49.55%, and GAC = 18.41%. The differential scanning calorimeter thermograms for the representative samples are shown in Fig. 3a. The initial point (onset 336

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affecting Tg (Fernandes et al., 2014), since water has a strong plasticizing effect (Wang and Zhou, 2013). Therefore, an initially glassy (amorphous) food component will become rubbery (sticky) following a moisture-induced decrease of Tg. 3.2.5. Microencapsulating efficiency (MEE) The MEE of the microparticles varied from 86.22 to 99.69% (Table 2). As shown in Fig. S6, the highest XOS retention was obtained for the conditions of T = 170.00°C, XC = 2.45%, and GAC = 18.41%. The results of the perturbation plot showed that the MEE first increased and then decreased with the increase of T (curve A in Fig. S1e), XC had a negative correlation with MEE (curve B in Fig. S1e), and GAC had a positive correlation with MEE (curve C in Fig. S1e). Since GA is a skin-forming material with a relative high Tg value and the surfaces are easily dried below the point of non-adhesion, and the thermoplastic particles sticking on the dryer wall is minimized (Werner et al., 2007). Moreover, GA as a wall material for encapsulation of a core material is a good protection for XOS (cf. Table 2 and SEM analysis). Therefore, increasing the GAC led to improvement of the MEE. With respect to the temperature effect, an inappropriate temperature resulted in an increase in the wall deposition and degradation and hence a reduced MEE. As mentioned by Courtin et al. (2009), the chemical compounds (e.g., anomeric configuration, ring form or linkage type) and exposure conditions (e.g., temperature or pH) are both important factors that affect oligosaccharides degradation. Xylooligosaccharides are linked with β-1, 4 linkages and are formed through Xyl pyranose ring residues. Generally, XOS have more thermal stability than those molecules with α-linkages or furanoses compounds (Courtin et al., 2009). This work also found that XOS retention during the drying process relates to the microcapsule protection (affected the susceptibility to degradation), the drying temperature and wall deposition. In conclusion, spray drying with a low GAC under an inappropriate temperature had a tendency to promote XOS degradation (Tables 2 and S3). 3.3. Verification of the predictive models

Fig. 3. (a) Typical differential scanning calorimeter thermograms of the representative samples; (b) relations between the moisture content and glass transition temperature (Tg) (drying conditions with 160.00°C, 26.00% xylooligosaccharides concentration (XC), and 10.00% gum Arabic concentration (GAC); Tgm: the glass transition midpoint; Tge: the glass transition end point).

Verification experiments were conducted to confirm the adequacy of the polynomial models obtained for drying yield (< 5.60% error), moisture content (< 8.80% error), hygroscopicity (< 4.50% error), Tg (< 1.90% error), MEE (< 0.80% error) (Table S4). Gordon-Taylor equation obtained for Tg (< 2.50% error) to evaluate powder stability (Table S5). The experimental values were shown to be close to the predicted values, which indicated that precision of models is good (Tables S4 and S5).

temperature, Tg) was obtained from the intersection of two tangents at the start of the corresponding endotherm. The heat flow signal exhibited distinct endothermic peaks with a notable trend of the changes. The endothermic peak of the heat flow signal was delayed with the increase of the molecular weight, which was consistent with the response surface analysis. The Gordon-Taylor equation is typically applied to predict the impact of the moisture content on Tg. The values of Tgs and k were 71.79°C and 1.17, respectively. The correlation coefficient of 0.986 indicated that the experimental data fitted the Gordon-Taylor equation well (Fig. 3b). The results of the perturbation plot show that the curve shape of GAC (curve C in Fig. S1d) was steeper than that of the T and XC (curves A and B in Fig. S1d), which indicates that Tg is more sensitive to the GAC. Glass transition temperature is correlated with the molecular weight (Alves et al., 2016), and GA has a higher Tg due to its larger molecule size. Similarly, an increase of the XC increased Tg, which can be attributed to the samples having components with higher molecular weights. A decrease in Tg was observed at a lower temperature, confirming the similar behaviour described in a previous study (Hashib et al., 2015). As previously mentioned, lower heat and mass transfer rates occur at lower inlet air temperatures, resulting in higher residual water contents of the sample. The moisture content is a crucial parameter for

3.4. Antioxidant activity Antioxidants are widely used in medicine, cosmetics, and food. The main feature of antioxidative activity is to delay or prevent lipid oxidation as well as the prevention and delay of cancer, cardiovascular diseases, and also anti-aging properties (Kang et al., 2017). The EC50 values of representative dried products (at higher XC) ranged from 1126.00 to 1235.50 μg/mL and 651.69–698.47 μg/mL in DPPH and ABTS+ assays, and antioxidant activity values of representative dried products (at higher XC) ranged from 44.54 to 49.68 μmol TE/g and 61.76–64.95 μmol TE/g sample in FRAP and ORAC assays, respectively. Antioxidant activity is higher or close to the values reported in other literatures (Bian et al., 2013; Coz-Bolaños et al., 2018; Snelders et al., 2013; Valls et al., 2018). The high content of bioactive substances of the XOS products suggest that the powder have high potential as antioxidants for the food, pharmaceutical, and cosmetics industry. 3.4.1. Antioxidant activity by DPPH and ABTS+ assays The radical-scavenging activity of the sample was assessed by measuring their decolorizing effect on stable DPPH/ABTS+ reactive 337

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oxygen radicals in the presence of hydrogen donating antioxidants. The reaction mechanism of DPPH/ABTS+ involves transfer of electrons by the reducing agent to the DPPH/ABTS+ radical. According to Podsędek (2007), phenolic compounds can scavenge reactive oxygen species due to their property of electron donation, as well as the number and location of the hydroxyl group. Total phenolic compounds and hydrogen atom effective release and conveyance contribute to the antioxidant activity of the samples. The electronic radicals (DPPH and ABTS+) are extinguished when reacted with antioxidants, resulting in a distinctive purple and cyan discoloration, respectively (Kang et al., 2017). The radical scavenging of the DPPH and ABTS+ was calculated as a percent reduction in absorbance. The antioxidant potentials of the dried products were quantified as the concentration necessary for a 50% reduction (EC50) of DPPH or ABTS+ radicals in the respective assays. As reported, EC50 is currently the most important parameter, which allows to obtain a doseresponse curve with different concentrations of a tested sample and compare different samples with standards compounds (dos Santos et al., 2018). For trolox, a reference antioxidant, the EC50 values in DPPH and ABTS+ assays were 10.85 μg/mL and 8.42 μg/mL, shown good radical scavenging activity at very low concentration (Table 3). As shown in Fig. 4 and Table 3, the radical scavenging effects of the samples were concentration dependent. Samples with higher concentrations of XOS have higher radical scavenging activity and lower EC50 values. The initial solution of assay 19 had the highest radical scavenging and EC50 values, up to 86.45% (4000 μg/mL of the sample) radical scavenging and 682.80 μg/mL EC50 value in DPPH assay, and 88.53% (4000 μg/mL of the sample) radical scavenging and 461.70 μg/ mL EC50 value in ABTS+ assay. However, the radical scavenging of assay 19 decreased by 13.12% and 8.69%, and EC50 value increased by 64.91% and 41.15% in DPPH and ABTS+ assays, respectively (Fig. 4 and Table 3). The MEE of assay 2 and 17 was high, that is, XOS were only slightly degraded to monosaccharides, and the antioxidant activity was no decreased significantly (compared with assay 19, Tables 2 and 3). These phenomena were also observed in the FRAP and ORAC assays (Table 3). The results showed that the antioxidative activity of the samples was positively associated with MEE, which indicated that the antioxidant activity of the samples was strongly associated with chemical structure of XOS (Fig. 4, Tables 2 and 3). The nearly identical absorbance of the solvent blank, Xyl (mainly degradation from XOS, results not shown) and GA implied that the DPPH radical scavenging activity of Xyl and GA was neglected (results not shown). As shown in Fig. 4 and Table 3, the radical scavenging activity in ABTS+ assay was always higher than that values in DPPH assay at the same concentration. The EC50 values in ABTS+ assay was always lower than that values in DPPH assay at the same concentration. The results might be attributed to two reasons. First, DPPH assay was less sensitive for the XOS antioxidant activity than ABTS+ assay, which was also observed by Valls et al. (Valls et al., 2018). Second, the radical scavenging of pure GA (3000 μg/mL solution) was up to 32.51% in

Fig. 4. Scavenging effect of different test sample concentrations on: (a) 2,2diphenyl-1-picrylhydrazyl (DPPH) radical, (b) 2,2′-Azinobis (3-ethylbenzothiazoline-6-sulfonic acid ammonium salt) (ABTS+) radical.

ABTS+ assay, which helped to increase the antioxidant activity of the product. 3.4.2. Ferric reducing antioxidant power (FRAP) and oxygen radical absorbance capacity (ORAC) assays Ferric reducing antioxidant power assay is a very useful routine analysis. Under the conditions of low pH and the existence of antioxidant, ferric are reduced to ferrous ion to form a coloured ferrous tripyridyl triazine complex. Then the antioxidant activity was estimated by measuring the increase in absorbance. Almost no coloured was detected in the reaction solution of GA and Xyl in FRAP assay, indicating

Table 3 Antioxidant capacity of representative sample in the 2,2-Diphenyl-1-picrylhydrazyl (DPPH), 2,2′-Azinobis (3-ethylbenzothiazoline-6-sulfonic acid ammonium salt) (ABTS+), ferric reducing antioxidant power (FRAP), and oxygen radical absorbance capacity (ORAC) assays. Test samples

DPPHx

ABTS+x

FRAPy

Assay 2 Initial solution of assay 2 Assay 17 Initial solution of assay 17 Assay 19 Initial solution of assay 19 Trolox

1235.50 ± 12.02 c 1200.50 ± 10.61 c 3044.50 ± 18.23 a 2927.50 ± 16.71 b 1126.00 ± 5.41 d 682.80 ± 6.95 e 10.85 ± 0.61 f

698.47 ± 3.84 c 680.95 ± 2.03 cd 1583.50 ± 5.23 a 1510.50 ± 5.57 b 651.69 ± 2.18 d 461.70 ± 1.56 e 8.42 ± 0.34 f

44.54 46.63 19.53 21.42 49.68 64.36 –

ORACy ± ± ± ± ± ±

1.22 0.93 0.42 0.48 0.84 1.14

c c d d b a

64.95 66.90 52.81 54.76 61.76 71.86 –

Note: Different lowercase letters within the same column indicate significant differences (p < 0.05). x The DPPH and ABTS+ were expressed as the antioxidant concentration providing 50% reduction of DPPH and ABTS+ radicals (EC50, μg/mL). y The FRAP and ORAC were reported as μmol Trolox equivalent (TE) per g sample (μmol TE/g sample). 338

± ± ± ± ± ±

0.97 1.20 0.95 0.28 0.40 1.10

b b d d c a

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Fig. 5. Colour attributes of the representative samples. (a) Drying conditions with 26.00% xylooligosaccharides concentration (XC) and 10.00% gum Arabic concentration (GAC), at different inlet air temperature (109.55°C, 160.00°C, and 210.45°C, respectively); (b) drying conditions with 160.00°C and 10.00% GAC, at different XC (2.45%, 26.00%, and 49.55% XC, respectively); (c) drying conditions with 160.00°C and 26.00% XC, at different GAC (1.59%, 10.00%, and 18.41% GAC, respectively).

that the substance with antioxidant activity in the solution was XOS. As discussed in Subsection 3.4.1, MEE affected the antioxidant activity of the dried products. Therefore, it is necessary to maintain a proper temperature and a certain concentration of carrier material during the drying process to keep the structural unity of XOS. The reaction mechanism of the ORAC assay is similar with DPPH and ABTS+ assays, which is based on the transfer of hydrogen electrons. Antioxidants can inhibit fluorescence changes caused by free radicals. The ORAC method has been widely recognized in the industry as a standard analytical method to measure the antioxidant capacity of products. It is worth mentioning that the radical scavenging of pure GA was as high as 37.02 μmol TE/g sample in ORAC assay, was 0.48 times that of pure XOS. The impressive value indicated that GA as a low-cost carrier not only promoted the physicochemical properties of XOS, but also enhanced the antioxidant activity of dried products.

2.45% XC > 49.55% XC (drying conditions with 160.00°C and 10.00% GAC), and 18.41% GAC > 10.00% GAC > 1.59% GAC (drying conditions with 160.00°C and 26.00% XC), which indicates that wall deposition adversely affected the colour attributes (Fig. 5a–c). Apparently, a higher wall deposition and gradually caramelization with the process of drying would occur under an inappropriate temperature and XC. Once the caramelization powder is shed off, the entire product would be contaminated by the caramelization powder; hence, more colour loss was detected. 3.6. Particle size and distribution The median diameters of the representative samples are presented in Table 2. An increase of the total solid content of the initial solution tended towards a larger particle size (Tables 1 and 2). Similar results were also reported by Jinapong et al. (2008) in the production of spraydried soymilk powder, and by Wu et al. (2014) in dairy powder production using spray freeze-drying and spray-drying. Masters (1985) stated that the difference of the median diameters is related to the fluid viscosity at a fixed atomizer rate. For a higher the fluid viscosity, larger droplets are formed during atomization, and hence larger spray-dried particles are generated (Fig. 1b, Tables 1 and 2). At a given concentration, the median diameter increased with the increase of the inlet air temperature (Tables 1 and 2), which is associated with the higher swelling of GA caused by higher temperature. As reported by Nijdam and Langrish (2006) and Aghbashlo et al. (2013), a higher drying temperature will result in the accelerated drying rate. Thus, the migration of crust-forming soluble materials to the surface of the atomized droplets is greatly expedited. The rapid formation of a dried crust layer on the surface of the droplets hinders particle shrinking during the processing, and therefore smoother and larger particles are produced. In contrast, the skin remains moist and supple for a longer period of time at lower drying temperature so that the hollow particles can deflate and shrivel during cooling, thus forming the shrivelled and smaller particles (Nijdam and Langrish, 2006;

3.5. Colour attributes Colour parameters were applied to evaluate the sensory attributes and quality of the product. The samples with different drying conditions exhibited high L* values, indicating the white colour of the powder (Fig. 5). The colour attributes of a* and b* were located in the first quadrant (+a*, +b*), and presented low values (Fig. 5), indicating a slight tendency of the sample to a redness and yellowness (Daza et al., 2016). The produced powder can be used as an ingredient in formulated foods because the white colour is a perfect attribute for the XOS product. The decrease in the L* value and increase in the a* value are indicative of browning (Denoya et al., 2016). For the effect of T and XC on colour attributes, the L* value first increased and then decreased with the increase of the T and XC, while the opposite trend occurred for the values of a* and b* (Fig. 5a and b). However, the trend for GAC on colour attributes was positive (Fig. 5c). As shown in Tables 1 and 2, the orders of the drying yield were as follows: 160.00°C > 109.55°C > 210.45°C (drying conditions with 26.00% XC and 10.00% GAC), 26.00% XC > 339

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Fig. 6. Micrographs of the representative samples (2000×). (I) (a), (b), and (c) are the samples produced with 2.45%, 26.00%, and 49.55% xylooligosaccharides concentration (XC) (drying conditions with 160.00°C and 10.00% gum Arabic concentration (GAC)), respectively; (II) (d) and (e) are the samples produced with 1.59% and 18.41% GAC (drying conditions with 160.00°C and 26.00% XC), respectively; (III): (f) and (g) are the samples produced with 109.55°C and 210.45°C (drying conditions with 26.00% XC and 10.00% GAC), respectively.

340

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Santhalakshmy et al., 2015). In general, particles with an appropriate medium sizes are preferred in food formulations for their better homogeneity and quality without affecting the microencapsulating efficiency (Arslan et al., 2015; Ferrari et al., 2013). The observed surface topography of the particles shown in the SEM of Fig. 6 can intuitively illustrate that particles dried at relatively gentle temperatures exhibited a more shrivelled appearance (Fig. 6b and f), while particles dried at an extremely high temperature displayed a much smoother surface (Fig. 6g). The representative distributions of the particle sizes are shown in Fig. 2b. The presence of larger particles in each sample might be attributed to the formation of irreversible link bridges during the incipient agglomeration process. 3.7. Characterization of final products 3.7.1. SEM The surface topography images of the representative samples are presented in Fig. 6. The formation of hollow particles is a common characteristic of skin-forming materials (Nijdam and Langrish, 2006), and is particularly obvious in the sample with a high ratio of GA (Fig. 6a). As mentioned by Tonon et al. (2011), a vacuole within the droplet forms instantly after a skin develops on the surface and inflates while the particle temperature is greater than the local ambient boiling point. According to Tonon et al. (2010) and Tupuna et al. (2018), the morphology of GA displayed hollow shape that is useful for microencapsulation of bioactive compounds (Fig. 6a). In the system with a low percentage of GA, it was observed that the microparticles were tightly piled up (Fig. 6c and d). When the GAC increased, the microparticles appeared more separated (Fig. 6a, b, e, f, and g). These results indicate that GA is a good carrier for the microencapsulation of XOS. As mentioned in subsection 3.6, low drying temperatures tend to cause surface roughness of the particles (Fig. 6b and f) when compared with extremely high temperature (Fig. 6g). According to Wang and Langrish (2010), an increase of the surface roughness might decrease the adhesive force between two contacting surfaces; hence, wall deposition was decreased. Moreover, particles with an appropriate surface roughness are desirable in food formulations for their thicker walls with higher retention of the core material without affecting the flow ability and reconstitution properties (Chang et al., 2016).

Fig. 7. Fourier transform infrared spectroscopy (FT-IR) spectra of the PM (physical mixture), gum Arabic (GA), and representative samples.

linkages (Gowdhaman and Ponnusami, 2015). The peak appearing at 897 cm−1 from XOS is assigning to the C1 ring frequency or group frequencies, which is characteristic of beta xylosidic linkages between sugar monomers (Bian et al., 2013). Identical characteristic bands were observed, confirming no chemical reaction occurred between the GA and XOS during the spray drying process (Fig. 7), which indicates that GA is an inert carrier that is suitable for producing prebiotic XOS powder.

3.7.2. XRD As shown in Fig. 2c, the XRD profiles of all the representative samples appeared diffuse with broad peaks, which indicates an amorphous structure of the powder (Cano-Chauca et al., 2005). The spectra of the samples were similar to the previous studies of producing spraydried sucrose powder (Adhikari et al., 2009; Jayasundera et al., 2011). The rapid evaporation of the low molecular weight sugars existing in XOS (Xyl2, Xyl3, and Xyl4, etc.) that occurred under spray drying tends to produce an amorphous powder due to the insufficient crystallization time (Jayasundera et al., 2011). Compared with the crystalline component, the amorphous solid has a good solubility due to the low energy level between its bonds and molecules.

4. Conclusions Natural hygroscopic and thermoplastic properties are the underlying problems of XOS powder during the drying process and storage. The fitted equations and the perturbation plots were successfully used to evaluate the effect of the inlet air temperature, XC, and GAC on the physicochemical properties of the products. The addition of GA is conducive to reducing the stickiness, caking, and liquefaction of the powder and to improving the quality of the XOS powder. This study provides a theoretical basis for the scale-up and industrialization of XOS and other sugar-rich carbohydrate powder.

3.7.3. FT-IR The FT-IR spectra of the physical mixture (PM), GA, and representative GA microcapsules after the spray drying process are illustrated in Fig. 7. The wide band at 3425 cm−1 is attributed to the stretching vibration of the OH–1 bond (Cabral et al., 2009). The peak at approximately 2925 cm−1 from GA is characteristic of carboxylic groups (Rocha-Selmi et al., 2013). The band at approximately 2355 cm−1 is another characteristic of GA (Hu et al., 2016). The peak at 1250 cm−1 corresponds to OH, CeH stretching or CeO bending vibration (Bian et al., 2013). The specific band at approximately 1040 cm−1 from XOS corresponds to CeOeC stretching of glycosidic

Conflict of interests The authors declare that there are no conflicts of interest.

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Acknowledgements

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