Innovative Nanofibrillated Cellulose from Rice Straw as Dietary Fiber

Research Article pubs.acs.org/journal/ascecg

Cite This: ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

Innovative Nanofibrillated Cellulose from Rice Straw as Dietary Fiber for Enhanced Health Benefits Prepared by a Green and Scale Production Method Jiai Yan,†,‡,§ Jianxue Hu,†,‡,§ Ruijin Yang,†,‡,§ Zhong Zhang,∥ and Wei Zhao*,†,‡,§ †

State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, 1800 Lihu Road, Wuxi, Jiangsu 214122, P.R. China ‡ National Engineering Research Center for Functional Food, Jiangnan University, 1800 Lihu Road, Wuxi, Jiangsu 214122, P.R. China § Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province, Jiangnan University, 1800 Lihu Road, Wuxi, Jiangsu 214122, P.R. China ∥ Department of Food Science and Technology, Food Innovation Center, University of Nebraska − Lincoln, 1901 N. 21 Street, Lincoln, Nebraska 68588-6205, United States ABSTRACT: Increased focus has been directed toward the use of agricultural residues. Conversion of lignocellulosic biomass to nanocellulose, such as nanofibrillated cellulose (NFC) has prompted a revolution in biobased materials for diverse applications. Currently used chemical methods for the preparation of NFC are not environmentally friendly and even exhibit toxicity, limiting the application of NFC in food. The present study proposes an innovative NFC as dietary fiber, prepared using a green and scale production method. This technique provides an integrated approach that combines physicochemical pretreatment (high-density steam flashexplosion, HDSF at 2.0 MPa) and successively enzymatic catalysts (45 U/g xylanase for 3 h, 60 U/g laccase for 4 h, and 150 U/g cellulose for 12 h) for the conversion of rice straw into NFC which is characterized by long and distinct fibrillated cellulose with widths of 30−200 nm, exhibiting excellent water retention capacity (20 g water/g) and swelling capacity (105 mL/g). Based on the NFC, hydrophobic groups (octenyl succinic anhydride, OSA) were further grafted onto the surface of NFC to prepare an innovative OSA−NFC as dietary fiber with enhanced health benefits (such as bile acids, cholesterol, nitrite ion, and oil/fat adsorption), especially which could markedly increase the adsorption capacity for oil in vitro (17.8 g oil/g after digestion model) and in vivo (almost 500 mg fat/g feces of rats). OSA−NFC could be used as highquality dietary fiber with a strong ability to absorb oil to help regulate body weight, representing an innovative way of transforming cheaper biomass into value-added products. KEYWORDS: Agricultural residues, Biomass, Nanofibrillated cellulose (NFC), Dietary fiber, Oil/fat adsorption

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dietary fibers (e.g., wheat dietary fiber, WDF) with granular structures, NFC exhibits more branching and a higher aspect ratio (Figure 1). Accordingly, NFC exhibits potential as dietary fiber with extremely superior composite and swelling capacity (SWC). Chemical treatments are currently the most widely used technologies in the conversion of cellulose fibers to nanocellulose. Chemical methods such as acid,9 alkaline, or 2,2,6,6-tetramethylpiperidine-1-oxyl radical (TEMPO)-mediated oxidation10 have been developed to treat various lignocellulosic biomasses, such as cotton, ramie, and kenaf cellulose. In these processes, the cellulose is hydrolyzed by sulfuric acid,11 hydrochloric acid,12 phosphate, or acetic acid. Moreover, a large amount of wastewater is produced, which is

INTRODUCTION Nanofibrillated cellulose (NFC) is a novel nanomaterial from microcrystalline cellulose based on a fibrillation process that produces finer particle diameters with a high aspect ratio (width = 4−20 nm; length = 500−2000 nm).1,2 NFC is equipped with superior characteristics: nanoscale dimension, high surface area, high Young’s modulus, very low coefficient of thermal expansion, low weight and low density, distinct optical properties, and stiffness, together with the biodegradability and renewability of cellulose.3,4 The material has caused a revolution in biobased materials for diverse applications in construction, packaging, automobile, transportation, and biomedical fields.5−8 As a special cellulose fiber, NFC can be used as a new dietary fiber exhibiting health benefits, including its ability to evade hydrolysis and digestion, increase fecal bulk, adsorb harmful substances, and reduce cholesterol. Compared with commercial © XXXX American Chemical Society

Received: October 16, 2017 Revised: January 15, 2018 Published: February 5, 2018 A

DOI: 10.1021/acssuschemeng.7b03765 ACS Sustainable Chem. Eng. XXXX, XXX, XXX−XXX

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ACS Sustainable Chemistry & Engineering

Figure 1. Microscopic images of NFC (a) and WDF (b).

Figure 2. Diagram of HDSF process. Whole structure (A) in catapult explosion mode composed of a cylinder and piston. HDSF equipment with a 100L chamber (B). HDSF equipment for industrial application with a 10 m3 chamber (C).

intends to increase the accessibility of cellulose fibers to chemical attack or enzymatic hydrolysis in order to produce a nanosize cellulose intermediate. High-density steam flashexplosion (HDSF)16 is an innovative and ecofriendly method for biomass pretreatment. This technique was successfully used in the preparation of feather keratin rather than chemical hydrolysis and hydrothermal treatment in our previous study.17 Compared with conventional steam explosion technologies, HDSF adopts a structure in the catapult explosion mode that principally consists of a cylinder and a piston, which can complete the explosion within 0.00875 s. Thus, HDSF exhibits sufficiently rapid decompression. Most of the steam in the biomass can quickly expand and detach themselves from the structure. Thus, the internal structure of the biomass is disrupted by mechanical shearing. During this process, the temperature of the biomass under HDSF can instantly decrease to 50 °C or lower and thus shorten the violent treatment of biomass under high temperature and high pressure.17 One of the advantages of HDSF is that it has been performed on a large scale in 10 m3 chamber. A diagram illustrating the process and equipment of HDSF for industrial application is presented in Figure 2. Increased attention has currently been directed toward the utilization of biomass.18−20 Rice straw is widely known to provide an annual renewable low cost and abundant source of

not environmentally friendly and even exhibits toxicity, thus limiting the application of NFC in food. Enzymatic treatment is an environmentally friendly alternative to chemical pretreatment for NFC production.13 However, enzymatic treatment shows a considerably low efficiency. Thus, researchers have focused on developing simple and ecofriendly methods to produce NFC. Nontoxic and safe techniques of preparing NFC as dietary fiber are particularly preferable. In addition, oil holding capacity (OHC) is an important property for dietary fiber to exert its health benefits. Dietary fiber is found to be randomly complex with oil intake and passes through the digestive tract to help regulate body weight. OHC is often employed to evaluate dietary fiber. It relies on the surface properties, overall charge density, thickness, and hydrophobicity of the fiber.14 However, dietary fiber is highly hydrophilic, implying that it can first interact with water, hindering its binding to oil. Different from traditional dietary fiber (Figure 1), NFC contains more active hydroxyl groups on the surface. Hydrophobic groups can be potentially grafted onto the surface of fibrillated cellulose to better compatibilize the OHC of NFC. Generally, biomass pretreatment is necessary to ensure the separation of the cellulose component from the tight bond of polymeric constituents (cellulose, hemicellulose, and lignin) in lignocellulosic biomass.15 This fractionation treatment mainly B


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ACS Sustainable Chemistry & Engineering natural cellulose fibers. Conversion of rice straw to products by using highly accessible and nonpollutant high technology entails difficulty. This study aims to present a method of preparing NFC with rice straw as dietary fiber used in food. Hydrophobic groups were grafted onto active hydroxyl groups on the surface of NFC to prepare an innovative NFC as dietary fiber for enhanced health benefits (such as oil/fat adsorption), representing a new technique for the reuse of rice straw and other biomass.

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MATERIALS AND METHODS

Materials. Dry rice straw was supplied by farmers in Wuxi, China. The rice straw was chopped into 3−5 cm segments. Xylanase (xylanase 80000 U/g, from Trichoderma reesei and with main enzyme activities EC 3.2.1.8 and EC 3.2.1.37 was purchased from Beijing Shibojiaxing Bio-Technology Co., Ltd., P.R. China) and cellulase (cellulase CL8000, 8000 U/g, supplied by Biofnornoon Bio-Engineering Co., Ltd., P.R. China) were used for enzymatic hydrolysis. Laccase (Laccase SUKALacc, 2000 U/g, from Aspergillus and with main enzyme activity EC. 1.10.3.2 was purchased from Sukahan (Weifang) Bio-Technology Co., Ltd., P.R. China) was used for delignification in 0.2 moL/L acetate buffer (pH 4.8). Enzymatic hydrolysis was conducted at 50 °C and with pH 4.8. Wheat dietary fiber (WDF) (about 75% of cellulose and 25% hemicellulose) was extracted from wheat straw from Shanghai Nuoruixian Bio-Technology Co., Ltd., P.R. China. Octenyl succinic anhydride (OSA) and Sudan Black B (of analytical reagent grade) were purchased from Sigma−Aldrich Chemical Co. (St. Louis, MO, USA). Sodium cholate (CA) and sodium deoxycholate (DCA) were supplied by Shanghai Yuanye Bio-Technology Co., Ltd. Other chemicals were purchased from Sinopharm Chemical Reagent Co., Ltd. All chemicals and reagents used in this study were of analytical grade. Methods. Preparation of NFC by HDSF and Enzymatic Hydrolysis. The process and conditions of NFC preparation by HDSF are presented as follows:

Dried rice straw (10 g) powder (80 mesh) was treated by alkaline extraction (15% NaOH) at 80 °C for 1 h, and the residue was washed thoroughly with distilled water until neutral pH was obtained. The solvent of fibers were converted to ethanol by washing the fibers in ethanol four times for 20 min at a ratio of 11:100. The ethanolinfiltrated residue was obtained after centrifugation at 5000 r/min for 20 min. After impregnation with a solution consisting of 0.91 g of monochloroacetic acid in 500 mL of isopropanol for 30 min, fibers were added gradually to a solution of NaOH (1.47 g), methanol (45.5 mL), and isopropanol (181.8 mL) that had been heated to temperatures slightly below its boiling point. The carboxymethylation reaction was allowed to continue at 85 °C for 1 h with constant stirring. After the reaction, the fibers were washed in three steps: first with deionized water (1818 mL), then with acetic acid (0.1 M, 181 mL), and finally with deionized water (1909 mL) again. The fibers were then impregnated with a NaHCO3 solution (4 wt % solution, 118 mL) and washed with deionized water after 1 h. Lastly, the fibers were prepared with deionized water at a concentration of 2%, and the slurry was passed through a laboratory high-pressure homogenizer (APV1000, APV, USA) for seven cycles under the operating pressure of 50 MPa. The suspension of NFC (Chemical) was stored at 4 °C. Chemical Analysis Methods. The cellulose, hemicellulose, and lignin contents were measured in accordance with Van Soest et al.21,22 The total dietary fiber is the sum of soluble dietary fiber and insoluble dietary fiber. The soluble dietary fiber and insoluble dietary fiber contents were determined using the AOAC method.23 Ash content was determined using a muffle furnace (SX2-10-12N, Shanghai Yiheng Sci-Technology Co., Ltd., P.R. China) maintained at 600 °C for 6 h.23 Characterization Methods. Hydrolysis. HDSF pretreatment is aimed to break the lignocellulosic complex, solubilize the noncellulosic contents (lignin and hemicellulose) but preserve the materials for further valorization, reduce cellulose crystallinity, and increase the porosity of the materials for subsequent depolymerization.24 HDSF treatment can also effectively remove and recover most of the hemicellulose portions as soluble sugars in an aqueous solution. To evaluate the efficiency of HDSF, the samples were treated by alkaline extraction (20% NaOH) at 80 °C for 3 h in a 1:20 ratio. The residue was then washed thoroughly with distilled water until neutral pH was obtained. Hydrolysis was performed with 150 U/g cellulase in a 1:20 ratio (sample:deionized water) under constant stirring. The content of reducing sugar was measured using the DNS method.25 Scanning Electron Microscopy (SEM) and Transmission Electron Microscopy (TEM). SEM images of rice straw treated by HDSF or the chemical method and TEM images of NFC were captured using a Quanta 200 microscope (PHILIPS, Netherlands) and a JEM-200CX microscope (JEOL, Japan), respectively. The samples (SEM) treated by HDSF were dehydrated with a graded ethanol series, and the samples were observed under a scanning electron microscope after they were plated by sputter coating. Samples (TEM) were dispersed into ethanol solution and treated with ultrasound for 1 h. The samples were then placed on a 400-mesh copper net and observed under a transmission electron microscope after drying.

The rice straw was chopped into 3−5 cm segmentsand placed in a 5.0 L HDSF reactor (QBS-200B, Gentle Science & Technology Co., Ltd., P.R. China), following the procedure in the study by Zhao et al.18 The rice straw was then treated at 0.9, 1.2, 1.6, and 2.0 MPa for 240 s, respectively. All experiments were conducted with the same amount (1 kg) of air-dried rice straw. After HDSF, the samples were dried and crushed to 80 mesh. The powder was then treated with cellulase, laccase, and xylanase. The enzyme was subsequently inactivated, and the material was homogenized using a T25 digital ULTRA TURRAX (IKA, Germany) homogenizer at 11 × 103 r/min for 2 min. The slurry (2 wt %) was then passed through a laboratory high-pressure homogenizer (APV-1000, APV, USA) for seven cycles under the operating pressure of 50 MPa. The suspension was stored at 4 °C. Preparation of NFC by Chemical Treatment. The process and operating conditions of NFC preparation by chemical treatment followed the method used in the study by Cervin et al.9 and are presented as follows: C


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ACS Sustainable Chemistry & Engineering Table 1. Constituents and Concentrations of Various Simulated Juices Used in the in Vitro Digestion Model Saliva

Gastric juice

Duodenal juice

Bile juice

Inorganic solution

10 mL KCL 89.6 g/L 10 mL KSCN 20 g/L 10 mL NaH2PO4 88.8 g/L 10 mL NaSO4 57 g/L 1.7 mL NaCl 175.3 g/L 20 mL NaHCO3 84.7 g/L

15.7 mL NaCl 175.3 g/L 3.0 mL NaH2PO4 88.8 g/L 9.2 mL KCl 89.6 g/L 18 mL CaCl2·2H2O 22.2 g/L 10 mL NH4Cl 30.6 g/L 6.5 mL HCl 37% g/g

40 mL NaCl 175.3 g/L 40 mL NaHCO3 84.7 g/L 10 mL KH2PO4 8 g/L 6.3 mL KCl 89.6 g/L 10 mL MgCl2 5 g/L 180 μL HCl 37% g/g

30 mL NaCl 175.3 g/L 4.2 mL KCl 89.6 g/L 150 μL HCl 37% g/g

Organic solution

8 mL urea 25 g/L

10 mL glucose 65 g/L 10 mL glucuronic 2 g/L 3.4 mL urea25 g/L 10 mL glucosamine hydrochloride 33 g/L

4 mL urea 25 g/L

10 mL urea 25 g/L

Add to mixture organic + inorganic solution

290 mg α-amylase 15 mg uric acid

1 g BSA 2.5 g Pepsin

9 mL CaCL2·2H2O 22.2 g/L 1 g BSA 1.5 g Lipase

10 mL CaCL2·2H2O 22.2 g/L 1.8 g BSA 1 g sodium cholate 1 g sodium deoxycholate 1 g sodium taurocholate

pH

6.8 ± 0.2

2.0 ± 0. 2

8.1 ± 0.2

8.2 ± 0.2

H2SO4. The test tubes were placed into the 70 °C water bath for 10 min and then cooled to room temperature in an ice bath before the absorbance was evaluated at 510 nm. Cholesterol Binding Capacity. The measurement of the binding capacity of the cholesterol samples was investigated using the egg yolk cholesterol model system proposed by Zhang et al.33 and NsorAtindana et al.34 with slight modifications. Fresh egg was whipped with nine volumes of deionized water and 10 mL of it mixed with 1.500− 2.000 g of each fiber sample (weight content was known.) at pH levels 2.0 and 7.0 to create similar conditions as those in the stomach and small intestine, respectively. After they were sufficiently mixed, the mixtures and the diluted yolk without the sample (blank) were shaken at 200 r/min for 2 h in an incubator maintained at 37 °C. After the 2 h incubation, the mixtures were filtered through a 200-mesh nylon cloth, and the supernatants were centrifuged at 8000 r/min for 5 min. The cholesterol content was measured at 550 nm by using the ophthaldialdehyde method.35 Nitrite Ion Adsorption Capacity. A dried sample (0.500−1.000 g) was mixed with a 10 mL 10 mg/mL NaNO2 solution in a 50 mL centrifuge tube. The pH level was adjusted to 2.0 or 7.0. The mixture was shaken at 8000 r/min for 2 h in an incubator maintained at 37 °C. The residual concentration of nitrite ion was determined colorimetrically by using N-(1-naphthyl)-ethylenediamine and sulphanilamide in accordance with the AOAC method.23 Oil and Adsorption on OSA−NFC in vitro. The in vitro digestion model used was a modified version of that described by Versantvoort et al.36 and Hur et al.37 The compositions of simulated saliva, gastric fluid, duodenal fluid, and bile are listed in Table 1. (1) Pre-ingestion: The initial lipids consists of 10 mL of distilled water, 5.0 g of sample, and oil. The fiber dry weight is about 1% of the quality of oil. (2) Mouth: The initial lipid is mixed with 10 mL of simulated saliva (pH 6.8) and then incubated at 150 r/min for 6 min at 37 °C. (3) Stomach: About 25 mL of simulated gastric fluid (pH 2) is added, and the mixture is incubated at 150 r/min for 2 h at 37 °C. (4) Small Intestine: About 25 mL of duodenal juice and 10 mL of bile are added, and the mixture is incubated at 150 r/min for 2 h at 37 °C. (5) The adsorption for oil content in the supernatant (3000 r/min, 10 min) is evaluated in accordance with the methods used by Zou et al.38 Adsorption for Oil of OSA−NFC in Rats. Female Sprague-Dawley rats were maintained on standard rodent chow until 45 d old at which

X-ray. Wide-angle diffraction data were collected using a Bruker AXS X-ray diffractometer equipped with Cu Kα radiation at 40 kV and 40 mA to investigate the XRD spectra of the cellulosic sample. Scattered radiation was detected in the range of 2θ = 5°−50° at a speed of 2°/min. Crystallinity index (CI) was calculated according to Segal et al.26 Fourier Transform Infrared (FTIR). FTIR spectroscopy (Nicolet iS10) was employed to record the cellulosic samples in the range of 400−4000 m−1 with a resolution of 4 cm−1. The samples were ground and mixed with KBr, and the resultant powder was pressed into pellets. Graft Modification of NFC by OSA (OSA−NFC). NFC fibers (3 g, dry weight) were suspended in distilled water with agitation. A weighed quantity of OSA was added (diluted five times with absolute alcohol, v/v) slowly over 2 h, and the reaction was continued for the required time and with the required pH. The pH was then adjusted to 6.5, and the samples were centrifuged for 15 min at 8500 r/min (Aclegar TM 25R centrifuge, Beckman Coulter) and washed three times with 70% alcohol. The resultant sample was stored in zip-lock bags. The degree of substitution (DS) is the average number of hydroxyl groups substituted per glucose unit. The DS of OSA−NFC was determined by titration.27 The modification conditions for OSA were optimized with the substitution degree (DS) and the reaction efficiency (RE) as the standards. Functional Properties of NFC and OSA−NFC. Water Retention Capacity, Oil Holding Capacity, and Swelling Capacity. The water retention capacity (WRC) and the OHC of the NFC or OSA−NFC were determined following the method used by Prakong et al.,29 and the SWC was determined using the method developed by Femenia et al.28 Apparent Viscosity. The apparent viscosity (AV) of NFC or OSA− NFC was determined using a rotary viscometer (NDJ-1). The samples were prepared by adding an appropriate amount of fiber to distilled water and then mixing at a high speed in a warring blender for 1 min. The measurement was taken at 3# rotor, shear rate 60 s−1. Bile Acid Binding Capacity. Bile acid binding in vitro was improved by using the methods described by Huang et al.29 and Hu et al.30 Each bile salt (as substrate) was dissolved in physiological saline (pH 6.8 ± 0.2) to prepare 2 mg/mL solution. About 0.5 g (dry weight) of each sample was mixed with 10 mL bile salt solution. The tubes were then incubated for 2 h at 37 °C on a shaking table. Mixtures were filtered using 450-mesh nylon cloth, and the supernatant was stored at −20 °C for bile acid analysis. The bile acid binding capacity was determined by colorimetry.31,32 About 1 mL supernatant was collected for analysis, and the appropriate amount was mixed with 1 mL 1% furfural solution and 10 mL 75% D


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ACS Sustainable Chemistry & Engineering Table 2. Composition of Diets (g/100 g dry diet)a

a

Ingredients

Fiber-free diet

NFC−OPFF

OSA−NFC−OPPE

WDF−OPPE

Protein dl-Methionine Corn oil NFC OSA−NFC WDF Mineral mixture (AIN, 76) Vitamin mixture (AIN, 76) Choline bitartrate Corn starch

20 0.3 5.0 − − − 3.5 1.0 0.2 70

20 0.3 5.0 5.0 − − 3.5 1.0 0.2 65

20 0.3 5.0 − 5.0 − 3.5 1.0 0.2 65

20 0.3 5.0 − − 5.0 3.5 1.0 0.2 65

AIN, American Institute of Nutrition (1977); OPFFF, oil palm fat−free flour.

time they were housed individually in hanging wire cages and administered a modified AIN-semipurified diet (Table 2) in doublewalled glass feeder jars. At 50 d old, the animals were divided randomly into four groups of six rats each: (1) fiber free diet (C), (2) NFC−OPFF, (3) OSA−NFC−OPFF, and (4) WDF−OPFF. The animals were located in individual cages with a normal cycle of 12 h light ± darkness with constant air circulation. The temperature of the room was kept at 24 °C ± 2 °C with free access to food and water. Each group was administered one of the experimental diets described in Table 2 for 6 weeks with food and water. All experimental protocols were approved by the Animal Care and Use Committee of Zhejiang Academy of Medical Sciences, China, and were in accordance with the Guide for the Care and Use of Laboratory Animals approved by the National Research Council.. The food intake of the rats was measured daily, and the fecal weights and lipid contents were measured following the method used by Jackson et al.39 Statistical Analyses. Each experiment was conducted at least three times. All statistical analyses were conducted using SAS software (version 8.0), and P < 0.05 was used to determine statistical significance in all tests.

in pressure during HDSF pretreatment, the mechanical force could promote removal of hemicellulose and lignin. The structure of the materials became less compact. The hemicellulose and the lignin were easily washed away by steam and water after HDSF by thermal and mechanical force.40,41 However, only a small amount of cellulose was degraded (the maximum loss of cellulose during HDSF was less than 5.5% involving solid fraction yield after pretreatment) because it contains numerous crystalline regions, resulting in increased cellulose content in the straw residue. To evaluate the efficiency of HDSF, the rice straw was hydrolyzed using cellulase. The hydrolysis rate of rice straw treated by HDSF using different pressures is shown in Figure 3a. The hydrolysis properties of rice straw showed significant improvement from 0.9 to 2.0 MPa of HDSF treatment, indicating HDSF detached cellulose from hemicellulose and lignin to increase the enzymatic accessibility of cellulose. FTIR spectra (Figure 3b) show that all the characteristic peaks of cellulose (i.e., O−H, C−H, and C−O stretching vibration) were observed, which indicates that the functional components of fiber were not destroyed after HDSF. The intensity of the bands at 1628 and 1515 cm−1 attributed to the aromatic CC in the plane symmetrical stretching vibration of the aromatic ring in lignin42 was weakened via delignification by HDSF. As the treatment severity increased from 0 to 2.0 MPa, the intensity of the band at 1628 cm−1 decreased in the treated rice straw samples. Using the ratio between band intensities at near 1600 and 1500 cm−1, it is possible to evaluate the proportion of lignin with condensed and cross-linked structures which is a characteristic feature of the concentration in guaiacyl, known as the cross-linked lignin ratio.43 The decrease in the cross-linked lignin ratio indicates the delignification of HDSF, which is in accordance with the recent study43 in which miscanthus and wheat straw were treated by steam explosion. SEM micrographs of rice straw treated by HDSF are presented in Figure 3c, clearly illustrating the morphological changes induced by HDSF. When the rice straw was treated by HDSF at low pressure (0.9 and 1.2 MPa), samples exhibited compact morphology, limiting the cellulose accessibility. By contrast, HDSF with 1.6 MPa-treated samples presented a more disorganized morphology characterized by the separation and greater exposure of fibers as well as loosening of the fibrous network. When pressure was increased to 2.0 MPa, the treated samples appear as large aggregates of fibrous tissue. HDSF involves exposing lignocellulosic biomasses to high-pressure saturated steam and then reducing pressure swiftly (within 0.00875 s), making the materials undergo an explosive decompression.43,44 This results in the

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RESULTS AND DISCUSSION Action of HDSF on Rice Straw. The recalcitrance of lignocellulosic biomass is attributed to the compact structure of the cellulose, which is embedded in a matrix of polymer−lignin and hemicellulose. Lignocellulosic biomass pretreatment is generally aimed at overcoming the recalcitrance, which is targeted to alter the size and structure of biomass via the separation of cellulose from the matrix polymers and to create access for hydrolysis to turn cellulose into nanocellulose with controllable reaction. After HDSF treatment, the cellulose content was increased, whereas the hemicellulose and lignin contents were markedly decreased with an increase in pressure during HDSF (Table 3). HDSF at 2.0 MPa led to decreases in hemicellulose and lignin contents by 67.0% and 56.7%, respectively. The result indicates that HDSF treatment could effectively break the lignocellulosic complex. With the increase Table 3. Chemical Compositions of Raw Rice Straw and HDSF-Treated Samplesa Pressure (MPa) 0 0.9 1.2 1.6 2.0 a

Cellulose (%) 34.76 35.28 36.94 38.31 40.65

± ± ± ± ±

0.49 1.20 4.07 0.48 2.58

Hemicellulose (%) 27.69 27.31 24.83 18.6 9.14

± ± ± ± ±

2.34 3.07 2.38 4.59 0.77

Acid insoluble Lignin (%) 21.78 14.85 12.51 10.60 9.24

± ± ± ± ±

1.26 1.67 2.14 2.50 1.04

Content of each component is based on the dry basis of the fiber. E


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Figure 3. Action of HDSF pretreatment on rice straw. (a)Enzymatic hydrolysis properties of rice straw after HDSF. (b) FTIR spectra for HDSFtreated samples. (c) SEM images of rice straw treated by HDSF at 0.9 MPa (A), 1.2 MPa (B), 1.6 MPa (C), and 2.0 MPa (D).

Table 4. Composition of Rice Straw, NFC (HDSF), and NFC (Chemical)a

a

Component (%)

Ash content

Total dietary fiber

Insoluble dietary fiber

Rice Straw NFC (HDSF) NFC (Chemical)

13.45 ± 0.19 5.11 ± 0.73 10.39 ± 2.89

− 85.86 ± 3.99 75.89 ± 3.21

− 84.25 ± 2.89 72.63 ± 4.78

Content of each component is based on the dry basis of the fiber.

breakdown of the lignocellulosic matrix and significant enhancement of the cellulose accessibility. Characterization of NFC Prepared by HDSF and Enzymatic Treatment. The rice straw treated with HDSF at 2.0 MPa was successively treated using xylanase (45 U/g for 3 h), laccase (60 U/g for 4 h), and cellulose (150 U/g for 12 h) to prepare NFC. NFC was also prepared using chemical methods to present a comparison with that prepared by HDSF. The components of the NFC and rice straw were measured (Table 4). The ash content of NFC (by HDSF or chemical treatment) decreased. The total dietary content of NFC prepared by HDSF was considerably higher than that prepared using the chemical method, indicating the deconstruction and

removal of noncellulosic contents in lignocellulosic biomass during HDSF and enzymatic treatments. The morphology of NFC prepared using the two methods is illustrated in Figure 4. Apparent morphological changes were induced by HDSF (Figure 4a), characterized by long and distinct nanofibrillated cellulose. As shown in Figure 4a, the width of NFC prepared by HDSF is 30−200 nm. Regardless, the NFC prepared using the chemical method was a mixture of long fibrous fibers and flaky fibers with diameters ranging from 500 to 1000 nm, which was clearly bulkier than the fibers prepared by HDSF. Crystallinity significantly influences the strength and stiffness of cellulose. Xray wide-angle diffraction (Figure 4b) revealed that NFC prepared by HDSF and the chemical method maintained the F


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Figure 4. Characterization of NFC (HDSF) and NFC (Chemical): TEM images (a), X-ray diffraction (b), and FTIR spectra (c), of NFC (HDSF) and NFC (Chemical).

Surface Modification and Activation of NFC. Dietary fiber is thought to be randomly complex with oil intake and to pass through the digestive tract to help regulate body weight. However, dietary fiber is highly hydrophilic; that is, it could first interact and be filled with water, impeding its ability to bind to oil. Oil absorbency may be enhanced by increasing the hydrophobic groups on the surface of the dietary fiber. Owing to the interaction of cellulose molecules via intramolecular and intermolecular hydrogen bonds, a tight crystalline region is formed, which limits the chemical grafting modification of cellulose owing to lack of adequate active hydroxyl groups on the surface of the cellulose. OSA has an oily nature and long hydrophobic alkyl chains. The OSA-modified starch (OSA−starch) was produced by Cadwell and Wurzburg (1953)47 and was permitted by the U.S. Food and Drug Administration (FDA) to be added in foods in 1972. Compared with cellulose, starch possesses substantial active hydroxyl groups on the molecular surface and could be subjected to OSA modification for use as an emulsion stabilizer.48 Different from traditional dietary fiber (Figure 1), NFC contains more active hydroxyl groups on the surface. Hydrophobic groups may be grafted onto the surface of fibrillated cellulose to better compatibilize the OHC of NFC. OSA modification of NFC can potentially contribute to improve hydrophobility in NFC. During OSA−NFC preparation, the concentration of OSA, reaction time and temperature, pH, and concentration of NFC, among other factors, were investigated and optimized. The DS and RE were identified for all the treatments, and the results of

crystalline pattern of the cellulose. The CIs of NFC prepared by HDSF and the chemical method were 55.67% and 50.52%, respectively. Two concurrent processes occur in NFC prepared by HDSF and NFC prepared using the chemical method: decrystallization and a simultaneous increase in CI via the removal of noncellulosic polysaccharides. The result was in agreement with the study by Kargazadeh et al.45 The CI is closely related to the ratio of the amorphous region to the crystalline region; thus, the removal of the amorphous regions can increase the CI of the cellulose. NFC prepared by HDSF exhibits higher total dietary fiber content (85.86%) (Table 4) but lower CI (50.52%) than the NFC prepared using the chemical method. This result indicates that HDSF can more effectively break lignocellulosic biomass. As shown in Figure 4c, all the characteristic peaks of cellulose (i.e., O−H, C−H, and C−O stretching vibration) were observed, and the findings indicate that the functional components of fiber were not destroyed after HDSF or chemical treatment. The increase in intensity of the band around 1604 cm−1 attributed to carboxyl groups46 indicates the carboxymethylation into −COOH in NFC treated using the chemical method. Compared with the chemical method, NFC prepared by HDSF exhibits weaker intensity of the bands between 1300 and 1600 cm−1 attributed to a large contribution of aromatic skeletal vibrations of lignin,43 illustrating the stronger action of delignification of HDSF than the chemical method. This is in accordance with the results in Table 4. G


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in-plane bending, respectively.49 The adsorption bands at 897 (−COC− deformation) and 657 cm−1 (−OH out-of-plane bending) can be observed in the FTIR spectrum of the original NFC, which indicates that the samples derived from rice straw possess the characteristic functional groups of cellulose. The new characteristic band near 1744 cm−1 was found in the spectra of OSA−NFC (DS = 0.034), which was attributed to the stretching vibration of the ester carbonyl groups.50 The results indicated that esterification modification occurred, and the octenyl succinate groups were introduced to the NFC. Meanwhile, the intensity of bands at 1058 and 1108 cm−1 due to the stretching vibration of hydroxyl of cellulose51 decreased with an increase in DS, which also indicates the esterification of hydroxyl of NFC by octenyl succinate groups. Enhanced Functional Properties of NFC as Dietary Fiber. Dietary fiber can effectively adsorb intestinal waste, which is regarded as an “intestinal scavenger”.52 The high adsorption capacity is attributed to its vesicular structure and active groups on the molecular surface. The particle size, surface area, and microstructure of fiber are important factors influencing its hydration properties, including the WRC, SWC, AV, and OHC. In this study, functional properties including the WRC, OHC, SWC, and AV of NFC, OSA−NFC (DS = 0.0344 ± 0.0062), and WDF as the control were determined (Figure 7). NFC and OSA−NFC exhibited excellent WRC, SWC, AV, and OHC. The WRC and SWC of NFC and OSA−NFC could reach 20 g water/g and 105 mL/g, 17 g water/g and 45 mL/g, respectively, which were considerably higher than WDF (5 g water/g and 10 mL/g) and other dietary fibers extracted from agricultural byproducts in other studies.53,54 Similarly, the AV and OHC of NFC and OSA−NFC were much higher than those of WDF specifically; the AV and OHC of OSA−NFC can reach 364 mPa·s and almost 20 g oil/g, respectively. Figure 7 shows that WRC and SWC decrease after OSA grafting modification of NFC, but AV and OHC increase. Succinylation helped introduce a substituting group with a long hydrophobic chain into a cellulose molecule and produced an amphiphilic derivative.55 OSA esterification reduced the hydration ability of NFC and enhanced the surface hydrophobicity of NFC. As shown in Figure 1, the nanofibers showed a net structure with many branches in the main cellulose chains, promoting adsorption capacity. Compared with WDF, the size of NFC decreased, the surface area increased, polar groups and other positions became exposed, and the long fibrous structure of

pH and temperature are shown in Figure 5. With 3% OSA concentration, the highest values for DS and RE were obtained

Figure 5. Effect of pH (a) and temperature (b) on the DS and RE of OSA−NFC.

under the following reaction conditions: reaction period = 4 h, reaction temperature = 40 °C, pH of reaction system = 8.5, concentration of NFC = 3%. Under optimal conditions, RE can exceed 95%. However, the commercially available dietary fiber WDF (Figure 1b) is difficult to graft owing to the shortage of active hydroxyl groups. The FTIR spectra of NFC and OSA− NFC present similar profiles (Figure 6). As shown in Figure 6, the adsorption band at 3419 cm−1 is attributed to the stretching vibration of hydroxyl (−OH), and bands at approximately 1372 and 1430 cm−1 are assigned to C−H deformation and −OCH−

Figure 6. FTIR spectra of NFC and OSA−NFC. H


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Figure 7. Water retention capacity (WRC) (a), swelling capacity (SWC) (b), apparent viscosity (AV) (c), and oil holding capacity (OHC) (d) of NFC, OSA−NFC, and WDF.

Figure 8. Adsorption of bile acids (CA, cholic acid; DCA, dexycholic acid) (a), cholesterol (b), and nitrite ion (c) of NFC, OSA−NFC, and WDF.

enterohepatic cycle.32 In a study in vitro, bile acid binding was used to evaluate the hypocholesterolemic potential of dietary fiber.31,32 The results (Figure 8a) showed that both NFC and OSA−NFC exhibited the high adsorption capacity of common bile acids, cholic acid (CA), and dexycholic acid (DCA), owing to the relation of the bile acid binding capacity to the matrix, porosity, surface heterogeneity, and adsorption field strength, among others, of the fiber.29 Upon surface modification by OSA, the CA and DCA binding capacity of OSA−NFC

NFC became porous, facilitating NFC binding to water and oil. Figure 8 shows the adsorption capacities of NFC and OSA− NFC for bile acids, cholesterol, and nitrite ions. Hypercholesterolemia refers to the excessive level of cholesterol in the blood, increasing the risk of heart disease. Dietary fibers were reported to be responsible for binding bile acids and excretion. As bile acids are products of cholesterol decomposition in the liver, the effect of dietary fiber and bile acid binding on lowering cholesterol is based on the negative feedback of bile acids in the I


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ACS Sustainable Chemistry & Engineering increased 2 times based on NFC owing to the incorporation of hydrophobic alkenyl groups and thus increased the hydrophobic property of NFC, which is considerably higher than that of the other agricultural byproducts.31 Compared with commercially available dietary fiber (e.g., WDF), both NFC and OSA−NFC exhibited a stronger adsorption capacity for cholesterol. Figure 8b reveals that more cholesterol was bound by WDF, NFC, and OSA−NFC at pH 7. These findings were similar to the results on other dietary fibers from different sources,34 indicating that the adsorption capacity for cholesterol in the intestine is much stronger than that in the stomach. Nitrite is a compound with relatively high toxicity. Consumption of meat products and vegetables with natural nitrate could increase the nitrites in the digestive tract, which react with amino acids to form carcinogenic compounds.56 Therefore, the adsorption capacity of nitrite is an important property for dietary fibers. The results (Figure 8c) showed the positive effects of the stomach condition (pH 2.0) on the nitrite adsorption capacities of three fiber samples and the higher sodium nitrite adsorption capacity of OSA−NFC compared with those of NFC and WDF. Figure 8c reveals that pH played an important role in the adsorption capacity toward NO2−and that the samples exhibited an excellent nitrite adsorbing capacity at pH 2.0. These results indicate that the samples have outstanding potential to adsorb nitrite in the stomach. With an increase in pH, the carboxyl group dissociated and the number of negative charges on the surface of the dietary fiber was increased. Thus, NO2− was rejected.57 Enhanced Adsorption Capacity for Oil in Vitro and in Rats. The ability of the fiber samples to bind oil/fat is one of the most important attributes for dietary fiber to exert its health benefits. Dietary fiber is known to randomly bind with oil intake in the digestive tract.58 The highly hydrophilic dietary fiber tends to first interact and be filled with water, hindering its bind to oil. In the current study, digestion processes from the mouth to the small intestine in vitro were employed to evaluate the oil/fat binding capacity of NFC and OSA−NFC as dietary fiber supplements. The results indicate no significant difference in the adsorption capacity for oil between NFC (1.5 g oil/g) and WDF (1.0 g oil/g) after the digestion model in vitro. However, the OHC of NFC and WDF were 13.5 and 5.0 g oil/ g, respectively, on the basis of conventional methods (Figure 7d). The oil adsorption capacity of NFC and WDF markedly decreased to a similar level, verifying the deduction that dietary fiber could first interact and become filled with water, impeding the binding of fiber to oil. Consistent with the expected results, the adsorption capacity of OSA−NFC for oil reached 17.8 g oil/g after the digestion model in vitro, exhibiting only a slight reduction from 20.0 g oil/g of OHC on the basis of conventional methods (Figure 7d). After esterification of NFC, long carbon chains were grafted onto NFC on hydroxyl, which enhanced the hydrophobicity and the adsorption capacity for oil. Mixtures of digested juices after simulated digestion are shown in Figure 9. NFC (Figure 9A) exhibited higher SWC than WDF (Figure 9A) to form a uniform system. The hydrophilic NFC and WDF interacted and was filled with water, releasing the oil into the digestion system and allowing lipase hydrolysis of oil, thus decreasing the adsorption capacity for oil. Notably, a layer separation occurred when mixing stopped, and the oil-containing OSA−NFC floated to the surface of the aqueous layer (Figure 9C), which was attributed to the extremely lightweight and hydrophobicity of OSA−NFC. Sudan Black B, a fat-soluble dye used in lipid staining,59 was

Figure 9. Mixture of digested juices after simulated digestion, which are (from A to D) NFC, WDF, OSA−NFC, and lipid stained by Sudan black B (0.3 g) based on sample C.

used to stain the lipid in digestive juices after simulated digestion. Figure 9D shows that most of the oil with black color was firmly absorbed by OSA−NFC and separated from the digestive juices containing lipases, thus retaining the excellent oil adsorption capacity in the digestive system. The enhanced oil adsorption capacity of OSA−NFC was further evaluated in rats. As shown in Figure 10, food

Figure 10. Food consumption, average fecal weight, and fat extracted from feces in rats.

consumption was not influenced by the three fiber categories (p > 0.05). The weights of dry feces excreted in a 24 h period by rats fed with NFC and OSA−NFC were similar (about 14 g) and higher than those of rats fed with WDF (12 g) and of the control (10 g). These results reveal that the dietary fiber intake could effectively increase fecal bulk. NFC and OSA−NFC possess much more branched and higher aspect ratio structure, hence the extremely strong complex and high SWC, contributing to the increased ability to increase fecal bulk in rats. Figure 10 shows the significant differences in the amount of fat extracted from feces among different fibers. Similar to the results in vitro, the amount of fat extracted from the feces of rats fed with OSA−NFC could almost reach 500 mg/g, which was considerably higher than that of the NFC−fed (280 mg/g), WDF−fed (80 mg/g), and control (40 mg/g) rats. The results indicate that the innovative nanofibrillated cellulose (NFC and OSA−NFC) with enhanced health benefits can be potentially J


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ACS Sustainable Chemistry & Engineering used as value-added dietary fiber products and functional food ingredients.

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CONCLUSIONS The present study proposed an innovative NFC as dietary fiber prepared by a green and scale production method for enhanced health benefits. This method provides an integrated approach combining physicochemical and enzymatic catalysts for the conversion of natural lignocellulosic biomass into NFC. HDSF is a physicochemical process. Notably, the duration within which materials are under a severe condition (high temperatures) is considerably short, and the temperature could decrease to 50 °C or lower immediately after HDSF. This process can overcome key barriers regarding the natural resistance of biomass while avoiding over degradation of cellulose to small molecular chemicals and maintaining cellulose products for further hydrolysis into nanocellulose materials. Moreover, the explosion speed and treatment efficiency in scale-up applications of catapult explosion can remain consistent with the small equipment.

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AUTHOR INFORMATION

Corresponding Author

*Fax/Phone: 86 510 85919150. E-mail: [email protected]. cn. ORCID

Wei Zhao: 0000-0001-9495-8508 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors gratefully acknowledge the financial support provided by Project 31522044 of the National Natural Science Foundation of P.R. China and National Key Research & Development Program of China (2016YFD0400300).

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REFERENCES

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Innovative Nanofibrillated Cellulose from Rice Straw as Dietary Fiber

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