Effect of Gum Arabic on Glucose Levels and Microbial Short-Chain

Article pubs.acs.org/JAFC

Effect of Gum Arabic on Glucose Levels and Microbial Short-Chain Fatty Acid Production in White Rice Porridge Model and Mixed Grain Porridge Model Jie-Lun Hu,† Shao-Ping Nie,*,† Na Li,† Fang-Fang Min,† Chang Li,† Deming Gong,‡ and Ming-Yong Xie† †

State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang 330047, China School of Biological Sciences, The University of Auckland, Auckland, Private Bag 92019, New Zealand

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‡

ABSTRACT: White rice porridge and mixed grain porridge, which are often consumed in many countries, were used as two models to evaluate the effects of gum arabic on glucose levels and microbial short-chain fatty acids (SCFA). Gum arabic was incorporated into the two porridges individually. Apparent viscosity of the two porridges was significantly increased, and their glucose productions during gastrointestinal digestion were notably lowered (p < 0.05). Diffused glucose amount was significantly decreased after gum arabic addition (p < 0.05). Furthermore, blood glucose rise after oral administration of porridges in mice was considerably lowered after fortified with gum arabic (p < 0.05). Microbial SCFA production during in vitro fermentation of porridges was significantly increased after gum arabic addition, which may also have beneficial effects on reducing postprandial glycemic response. Therefore, gum arabic may be a helpful ingredient, which could be added in porridges to have benefits for the reduction of postprandial glycemic response. KEYWORDS: gum arabic, porridge, glucose production, glucose diffusion, blood glucose, microbial short-chain fatty acid

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seeds.13,15−18 Mixed grain porridge could be made by a mixture of these grains and thought to have a relative lower GI. Therefore, in this study, we use two representative porridge models (white rice porridge as high GI porridge model while mixed grain porridge as relative low GI porridge model) to evaluate the effects of gum arabic on glucose levels and microbial short-chain fatty acid productions. Gum arabic was incorporated into white rice porridge and mixed grain porridge individually. The apparent viscosity levels of porridges were evaluated, and glucose production of porridges was investigated in artificial simulated gastric and intestinal digestion in vitro. In addition, the diffusion of glucose after digestion, the blood glucose levels in mice after oral administration of porridges, and microbial short-chain fatty acid productions after in vitro fermentation of porridges were also studied.

INTRODUCTION

The dietary factors that can mitigate the symptoms of diabetes and other chronic diseases have been reported by many researchers.1 Studies have shown that some dietary fibers could have effects on postponing digestion of carbohydrates in foods, thus resulting in a lower level of postprandial blood glucose.2,3 Some viscous dietary fibers could also bind and absorb the glucose, and thus the glucose in the small intestine could be kept at low concentration by dietary fibers.4 In addition, dietary fiber could be further fermented by colonic bacteria to result in short-chain fatty acid (SCFA) production. Reports have found that SCFA concentration (mainly acetic acid, propionic acid, and butyric acid) in the large bowel might also play an important role in beneficial metabolic effects including the reduction of the postprandial glycemic response.5 Gum arabic is a kind of dietary fiber from the stems and branches of Acacia senegal and A. seyal.6 Gum arabic has wide industrial uses as a stabilizer, thickening agent, and emulsifier, mainly in the food industry.7 Some recent reports have claimed that gum arabic possesses antioxidant, nephroprotectant, and other effects.8−10 However, there is limited information on the effects of gum arabic on the glucose levels and microbial shortchain fatty acids production in food models. White rice porridge or mixed grain porridge is often consumed in many countries, and especially as the breakfast. It was reported that the blood glucose could be mostly influenced at breakfast, before which the stomach was empty.11 However, white rice was reported to be high in glycemic index (GI),12,13 and the high GI has been reported to be correlated with diabetes and metabolic conditions.14 Some other grains were reported to have a lower GI than white rice, such as oat, buckwheat, brown rice, peanut, corn dregs, beans, and coix © 2014 American Chemical Society

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MATERIALS AND METHODS

Materials and Animals. White rice, oat, buckwheat, brown rice, corn dreg, peanut, red bean, kidney bean, and coix seeds were purchased from a local supermarket. Gum arabic from Acacia tree was purchased from Shanghai Chemicals and Reagents Co. (Shanghai, China). All other reagents were purchased from Sigma-Aldrich (Shanghai, China). Kunming mice, weighing 20.0 ± 2.0 g [Grade II, Certificate Number SCXK (gan) 2006-0001], were purchased from Jiangxi College of Traditional Chinese Medicine, Jiangxi Province, China. All animals used in this study were cared for in accordance with the Guidelines for the Care and Use of Laboratory Animals published by the United States National Institute of Health (NIH, Publication no. Received: Revised: Accepted: Published: 6408

April 2, 2014 June 17, 2014 June 17, 2014 June 18, 2014 dx.doi.org/10.1021/jf501557b | J. Agric. Food Chem. 2014, 62, 6408−6416

Journal of Agricultural and Food Chemistry

Article

85-23, 1996), and all procedures were approved by the Animal Care Review Committee (Animal application approval number 0064257), Nanchang University, China. Porridge Preparation. Porridges were prepared according to the recipes in Table 1 in a stainless steel pot. For white rice porridge, 1 L

prepared (SIENZY). The SIENZY solution contained 100 g of SIES, 100 g of pancreatin solution (7%, w/w, Sigma), 13 mg of trypsin (Sigma), and 200 g bile salt solution (4%, w/w). For the pancreatin solution, 14 g of pancreatin was dissolved in 200 g of water, and the solution was mixed for 10 min with a magnetic stirrer and centrifuged for 10 min at 2800g. The supernatant (100 g) was used for the preparation of the SIENZY solution. The dilution was performed using SIES as dilution medium, and the pH was adjusted to 7.5 by NaOH (0.1 M). Simulated Digestion. Digestion studies were performed using an RC806 flow-through dissolution system (Tianfa Corp., Tianjing, China), equipped with a temperature circulator-controller, which allowed one to maintain the temperature at 37 °C throughout all of the experiments. Stirring paddles (Tianfa Corp., Tianjing, China), which were at the top of sample cells, were also equipped with a flowthrough dissolution system for simulating the gastric peristalsis. In addition, several pumps (HL-2D, Qingpu Corp., Shanghai, China) were connected to the dissolution system to pump in the gastric and intestinal medium for digestion. Further, a pH meter (XB89-PH-2612, XG Corp., Beijing, China) was also connected to the dissolution system for controlling the pH in digestion system. The pH was monitored and continuously controlled by adding either water or 1 M HCl into the stomach, and either electrolytes or 1 M NaHCO3 into the small intestine. Before each experiment, the system was washed with detergent and rinsed with water. For the gastric digestion tests of porridges, cells were loaded with 100 mL of porridge, and 150 mL of gastric medium was pumped through the cells at a constant flux of 0.4 mL min−1. For the intestinal digestion of porridges, porridges that were predigested by gastric medium were placed inside another sample cells. Around 200 mL of small intestinal medium was pumped at a constant flux of 0.56 mL min−1. For all of the experiments, a fraction collector (BSZ-100, Jingke Corp., Shanghai, China) was used to withdraw 3 mL samples at specified time intervals. The collected samples were used for the determination of glucose concentration and the calculation of glucose amount. The gastric digestion of the porridges was followed for 6 h. Samples were analyzed before and after digestion. Glucose concentration was determined at 0, 0.5, 1, 2, 3, 4, 5, and 6 h according to the hexokinase method of Yokoyama et al.2 Three independently replicated extractions were performed for each sample. The intestinal digestion of the porridge was also followed for 6 h. Samples were analyzed after digestion, and the glucose concentration was determined after 0.5, 1, 2, 3, 4, 5, and 6 h according to the hexokinase method.2 Three independently replicated extractions were performed for each sample. The maximum producing velocity of glucose (Vmax1) for porridges during intestinal digestion was calculated as follows. The experimental data were fitted with an equation of parabola:

Table 1. Preparations of Different Porridges porridges porridge porridge porridge porridge

1a 2 3 4

recipes white rice (75 g) boiled in 1 L of water mixed grains (75 g) boiled in 1 L of waterb white rice (75 g) and gum arabic (10 g) boiled in 1 L of water mixed grains (75 g) and gum arabic (10 g) boiled in 1 L of water

a

Porridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. bMixed grains: oat (15 g), buckwheat (15 g), brown rice (15 g), corn dregs (6 g), peanut (6 g), red bean (6 g), kidney bean (6 g), and coix seed (6 g). of distilled water was boiled to 98 ± 2 °C in the pot, and then 75 g of white rice was dropped into the pot. For mixed grain porridge, 75 g of mixed grains was soaked in 500 mL of distilled water for 6 h first. Another 500 mL of distilled water was boiled to 98 ± 2 °C in the pot. After that, the mixed grains together with the water used for soaking were poured into the pot. For white rice porridge added with gum arabic, 10 g of gum arabic was dissolved in 1 L of distilled water in the pot first, then boiled to 98 ± 2 °C. After that, 75 g of white rice was dropped into the pot. For mixed grain porridge added with gum arabic, mixed grains were soaked in 500 mL of distilled water for 6 h first. Ten grams of gum arabic was dissolved in another 500 mL of distilled water in the pot, then boiled to 98 ± 2 °C. After that, the mixed grains together with the water used for soaking were poured into the pot. For all of the porridges, the pot was boiled with frequent stirring for 60 min after water boiling again to cause full gelatinization of starches. The cooked porridge was then transferred to a glass container and left to cool at room temperature. Determination of Apparent Viscosity of Porridges. Apparent viscosity of each porridge was measured at 25 °C with a Brookfield DV-Ultra Programmable rheometer (Brookfield, Stoughton, MA), equipped with a CP52 spindle (spindle multiplier constant = 9.83, shear rate constant = 2).19 Simulated Gastric and Intestinal Digestion of Porridges in Vitro. Digestion Media Used Throughout the Digestion Experiments. All chemicals and enzymes were obtained from Sigma Chemical Co. (St. Louis, MO) and Amano Enzyme Inc. (Nagoya, Japan). The simulated gastric and intestinal fluids were prepared according to the protocol used by a model gastrointestinal system (TNO Intestinal Model 1, TIM1 from TNO Zeist, The Netherlands), which simulates the physiological conditions of the human stomach and small intestine.20,21 Gastric Medium Preparation. The gastric medium was prepared according to the method by Tedeschi et al. with some modifications.22 The gastric electrolyte solution (GES) consisted of 3.1 g L−1 NaCl, 1.1 g L−1 KCl, 0.15 g L−1 CaCl2·2H2O, and 0.6 g L−1 NaHCO3. The final pH was adjusted to 3 by addition of HCl (0.1 N). Next, 37.5 mg of gastric lipase (Lipase DF Amano 15, Amano Enzyme Inc., Japan) and 35.4 mg of pepsin from porcine gastric mucosa (Sigma) were added to a solution of 150 g of GES and 1.5 mL of CH3COONa (1 M, pH 5). The solution was gently mixed for 10 min on a magnetic stirrer at room temperature, and simultaneously the pH was adjusted to 3 by additions of HCl (0.1 N). The solution was stored on ice before use. Small Intestinal Alkaline Medium. The small intestinal medium was prepared according to the method by Tedeschi et al.22 The simulated small intestinal electrolyte solution (SIES) consisted of 5.4 g L−1 NaCl, 0.65 g L−1 KCl, and 0.33 g L−1 CaCl2·2H2O. The pH was adjusted to 7 using NaOH (0.1 M). To simulate a duodenum residue solution, bile salt was added to a SIES containing the enzymes pancreatine and trypsin. A SIES with enzymes and bile salts was first

Y = ax 2 + bx + c where Y is the glucose concentration (mM); x is time (min); and a, b, and c are coefficients. The equation to calculate the producing rate (Y′) at any time is Y′= 2ax + b. When x is close to 0, Y′ = Vmax1 = b. Determination of Glucose Diffusion. The residue digestion mixtures of porridges after digestion were used to determine diffusion of glucose according to the method by Ou et al. with some modifications.23 Briefly, a total of 12 samples (3 replicates of 4 different porridges), 25 mL each, were dialyzed in dialysis bags with a molecular weight cutoff of 8000−14 000 against 200 mL of deionized water at 37 °C. The glucose concentration in 2.0 mL of the dialysate was determined after 10, 20, 30, 60, 90, 120, 150, 180, 240, 300, and 360 min (the results at 12 h proved 360 min was enough for equilibrium) according to the hexokinase method.2 The maximum diffusion velocity of glucose (Vmax2) was calculated as follows. The experimental data were fitted with an equation of parabola: Y = ax 2 + bx + c where Y is the glucose diffusion concentration (mM); x is time (min); and a, b, and c are coefficients. The equation to calculate the diffusion 6409

dx.doi.org/10.1021/jf501557b | J. Agric. Food Chem. 2014, 62, 6408−6416


Article

sample for GC analysis was 0.2 μL, and the running time for each analysis was 20.5 min. The independently replicated determinations were performed three times for each sample. Data handling was carried out with HP Chem Station Plus software (A.09.xx, Agilent). Statistical Analysis. All of the experiments were done in triplicate. Statistical analysis was carried out using SPSS (version 16.0, Chicago, IL). The results were expressed as mean ± standard deviations and compared using the Tukey test at 5% confidence level.

rate (Y′) at any time is Y′ = 2ax + b. When x is close to 0, Y′ = Vmax2 = b. Animal Study. Male 6-week-old Kunming mice (20.0 ± 2.0 g) were individually housed in stainless steel cages in a room with controlled temperature (25.0 ± 0.5 °C), relative humidity (50 ± 5%), and 12 h/ 12 h light/dark cycle. All mice were fed with the same amount of basal diet, which was prepared according to the published formula,24 and water was provided ad libitum. Food was stopped to the mice 12 h before the experiment. All mice were randomly divided into four groups: (1) porridge 1 group, mice were given oral administration of white rice porridge at 25 mL/kg body weight (solid content = 1.875 g solid/kg body weight); (2) porridge 2 group, mice were given mixed grain porridge at 25 mL/kg body weight (solid content = 1.875 g solid/kg body weight); (3) porridge 3 group, mice were given white rice porridge fortified with gum arabic at 25 mL/kg body weight (solid content = 2.125 g solid/kg body weight; gum arabic content = 0.25 g/ kg body weight); (4) porridge 4 group, mice were given mixed grain porridge fortified with gum arabic at 25 mL/kg body weight (solid content = 2.125 g solid/kg body weight; gum arabic content = 0.25 g/ kg body weight). Each group had 12 mice, and 6 mice were put in one cage. The blood glucose of each mouse was determined before oral administration (0 h) and also 0.5, 1, 2, and 3 h after being given oral administration of porridge. Blood glucose levels were obtained by using an Accu-Chek Performa blood glucose meter (Roche, Mannheim, Germany). In Vitro Fermentation of Porridges. Fecal Slurry Preparation. The fresh fecal samples were collected from four healthy donors who never had large bowel disease before. The donors also had followed normal diets and had not been treated with antibiotics for at least 3 months. Collected fecal samples were mixed with an equal amount of feces from each donor. The mixed fecal samples were immediately stored in an anaerobic jar before use.25 Preculture. Mixed fecal samples (120 g) was precultured in 1 L of preculture medium (10 g of tryptone, 5 g of yeast, 10 g of NaCl, 5 g of glucose, and 6 g of maltose) anaerobically. After overnight growth, 120 mL of the preculture was filtered through sterile gauze sponges to remove large particles and stored in an anaerobic jar before use.26 Fermentation. The composition of 1 L growth medium was: 4.5 g of NaCl, 4.5 g of KCl, 1.5 g of NaHCO3, 0.69 g of MgSO4·H2O, 0.8 g of L-cysteine HCl·H2O, 0.5 g of KH2PO4, 0.5 g of K2HPO4, 0.4 g of bile salt, 0.08 g of CaCl2, 0.005 g of FeSO4·7H2O, 1 mL of Tween 80, and 4 mL of resazurin solution (0.025%, w/v) as anaerobic indicator.25 Growth medium was sterilized at 121 °C for 15 min before use and divided into sterile anaerobic vessels. The porridge samples (after gastrointestinal digestion) were subjected to the in vitro fermentation with the precultured human fecal microbiota. The total volume of the fermentation slurry was 50 mL. For the tested samples, the final fermentation volume was 40% growth medium, 40% human fecal preculture, and the last 20% was porridge or distilled water (control). All samples and the fecal preculture were introduced in different anaerobic sealed tubes containing growth medium, under the condition of 10% H2, 10% CO2, and 80% N2 in Forma Anaerobic System (Thermo Electron Corp., Marietta, OH).27 Separated tubes were prepared for each replicate at each time point (0, 6, 12, and 24 h during fermentation). The anaerobic sealed tubes were then incubated at 37 °C for 24 h in a TC-2112B Thermostat shaker (160 rpm, Shanghai Nuoji Corp., Shanghai, China). SCFA Measurement. The fermentation cultures were centrifuged at 4800g for 15 min. The supernatants were used for determination of SCFA. Chromatographic analysis was carried out using the Agilent 6890 N GC system according to our published method.28 A GC column (HP-INNOWAX, 190901N-213, J & W Scientific, Agilent Technologies Inc., U.S.) of 30 m × 0.32 mm i.d. coated with 0.50 μm film thickness was used. Nitrogen was supplied as the carrier gas at a flow rate of 19.0 mL/min with a split ratio of 1:10. An initial column temperature was held at 100 °C for 0.5 min, then programmed at a rate of 4 °C/min to 180 °C. The temperature of the FID and injection port was 240 °C. The flow rates of hydrogen and air were 30 and 300 mL/min, respectively. The volume of injected standard SCFA and

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RESULTS AND DISCUSSION Apparent Viscosity of Porridges. There was some difference in the apparent viscosity among porridges (Table 2). The apparent viscosity level (shear rate = 30 or 50 s−1) of Table 2. Apparent Viscosities of Different Porridges at Different Shear Rates (s−1)a apparent viscosity (mPa s−1) 30 s−1

sample porridge porridge porridge porridge

b

1 2 3 4

633 602 720 683

± ± ± ±

3 2 4 2

50 s−1 c

a b c d

342 303 435 410

± ± ± ±

4 2 2 3

a b c d

Data are presented as means ± standard deviations of triplicate measurements. bPorridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. c Mean values in the same column with different letters are significantly different (Tukey test, p < 0.05). a

white rice porridge was higher than that of mixed grain porridge. The difference in the apparent viscosity between white rice porridge and mixed grain porridge may be due to the difference of the materials in the porridges. This was consistent with previous result reported by Wood et al.29 However, apparent viscosity of the two porridges was significantly increased after addition of gum arabic (p < 0.05). The apparent viscosity of white rice porridge was improved from 633 ± 3 to 720 ± 4 mPa s−1 at shear rate = 30 s−1 and increased from 342 ± 4 to 435 ± 2 mPa s−1 at shear rate = 50 s−1. Meanwhile, the apparent viscosity of mixed grain porridge increased from 602 ± 2 to 683 ± 2 mPa s−1 at shear rate = 30 s−1 and increased from 303 ± 2 to 410 ± 3 mPa s−1 at shear rate = 50 s−1. This may result from the addition of gum arabic to porridges. Viscous water-soluble dietary fibers could affect the apparent viscosity of solution.30 A higher viscosity of solution could be provided by gum arabic.31 In addition, gum arabic was reported to belong to the family of dietary fiber, and our results agreed well with those of other dietary fibers, which could improve the values of apparent viscosity.30,32 The increase in the apparent viscosity may have an effect on the glucose production and diffusion, which affect the blood sugar response.29 Glucose Production of Porridges during Gastric Digestion. As shown in Table 3, the total amount of glucose in white rice porridge was 40 mmol at the beginning and then increased to 460 mmol at 6 h. These amounts of the glucose may result from hydrolysis of the starch in the white rice porridge, which may be due to the acid environment of the gastric medium (pH = 3) because there was no enzyme in gastric medium that could hydrolyze the whole starch in white rice porridge to glucose. In addition, the glucose amount of white rice porridge fortified with gum arabic was significantly lower than that of the white rice porridge at the same time point throughout the whole gastric digestion (p < 0.05). This 6410



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Table 3. Glucose Amount of Different Porridges during Gastric and Intestinal Digestiona glucose amount samples

0h

Gastric Digestion (mmol) porridge 1b 40 ± 6 ac porridge 2 5±1b porridge 3 38 ± 5 a porridge 4 5±1b Intestinal Digestion (mol) porridge 1 porridge 2 porridge 3 porridge 4

0.5 h

1h

2h

3h

4h

5h

6h

298 45 222 22

± ± ± ±

18 a 5b 25 c 2d

377 74 274 37

± ± ± ±

22 a 10 b 12 c 4d

395 89 348 44

± ± ± ±

24 a 6b 14 c 6d

417 113 384 52

± ± ± ±

20 a 5b 10 c 4d

438 128 388 59

± ± ± ±

18 a 16 b 16 c 5d

440 142 399 67

± ± ± ±

16 a 18 b 15 c 9d

460 160 410 80

± ± ± ±

22 a 15 b 15 c 8d

3.0 2.0 2.5 1.4

± ± ± ±

0.2 0.3 0.2 0.1

6.7 5.0 5.2 4.2

± ± ± ±

0.6 0.5 0.4 0.5

11.5 6.9 8.6 5.2

± ± ± ±

0.7 0.6 0.5 0.5

13.2 8.5 9.9 6.4

± ± ± ±

0.7 0.5 0.2 0.2

16.7 10.6 13.1 8.3

± ± ± ±

1.0 1.0 1.0 0.9

18.9 13.6 14.8 10.8

± ± ± ±

1.0 0.5 0.5 0.8

22.6 14.8 16.8 11.7

± ± ± ±

1.2 1.1 1.2 1.0

a b b c

a b b c

a b c d

a b c d

a b c d

a b c d

a b c d

Data are presented as means ± standard deviations of triplicate measurements. bPorridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. cMean values in the same column (from the same digestion) with different letters are significantly different (Tukey test, p < 0.05). a

may be because the gum arabic coated on the surface of grains, which could affect the starch in the white rice porridge to get in touch with the gastric medium and delay the glucose production. Furuta et al. also found the coating of another dietary fiber, water-soluble soybean polysaccharides, on the surface of cooked rice grains.33 The glucose amount in mixed grain porridge at 0 h was only 5 mmol, and the amount increased to 160 mmol at 6 h (Table 3). The lower initial glucose amount of mixed grain porridge would be due to less rice in the formula. The increase of glucose amount would also result from weak hydrolysis of the carbohydrates in mixed grain porridge, which was due to the acid environment of the gastric medium (pH = 3). The glucose amount of mixed grain porridge fortified with gum arabic was significantly lower than those of mixed grain porridge at the same time points during gastric digestion (p < 0.05), and very little glucose was produced in mixed grain porridge fortified with gum arabic during gastric digestion (22−80 mmol). This may be also because the gum arabic could inhibit the carbohydrates in mixed grain porridge to get in touch with the gastric medium and thus reduce the glucose production. Glucose Production of Porridges during Intestinal Digestion. The glucose amounts of porridges during intestinal digestion were also shown in Table 3. The glucose amount of white rice porridge was high (approximately 3.0 mol) in the initial time point (0.5 h), and the glucose amount differed significantly from 0.5 to 6 h. The glucose amount of white rice porridge increased along with the digestion time, with the maximum level of 22.6 mol at 6 h, for there was an enzyme, amylase, which could hydrolyze the starch in white rice to glucose. However, after addition of gum arabic, the level of glucose amount in the white rice porridge was significantly decreased at all time points (p < 0.05), with a maximum level of around 16.8 mol at 6 h. The maximum glucose producing velocity (Vmax1) of white rice porridge fortified with gum arabic (0.2233 ± 0.0010 mM min−1) was significantly lower than that of white rice porridge (0.2880 ± 0.0015 mM min−1) (Table 4, p < 0.05). As presented in Table 3, the glucose amount of mixed grain porridge was approximately 2.0 mol at the initial time point (0.5 h), and it differed significantly from 0.5 to 6 h. The glucose amount of mixed grain porridge increased along with the digestion time, with the maximum level of around 14.8 mol at 6 h. However, after addition of gum arabic, the level of glucose amount in the mixed grain porridge was significantly decreased

Table 4. Maximum Producing Velocity of Glucose (Vmax1) and Maximum Diffusion Velocity of Glucose (Vmax2) for Different Porridgesa Vmax (mM min−1) Vmax1

samples porridge porridge porridge porridge

1b 2 3 4

0.2880 0.1779 0.2233 0.1350

± ± ± ±

0.0015 0.0008 0.0010 0.0005

Vmax2 ac b c d

0.0348 0.0250 0.0297 0.0196

± ± ± ±

0.0007 0.0010 0.0005 0.0008

a b c d

Data are presented as means ± standard deviations of triplicate measurements. bPorridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. c Mean values in the same column with different letters are significantly different (Tukey test, p < 0.05). a

at all time points (p < 0.05), with a maximum level of around 11.7 mol at 6 h. The maximum glucose producing velocity (Vmax1) of mixed grain porridge fortified with gum arabic (0.1350 ± 0.0005 mM min−1) was significantly lower than that of mixed grain porridge (0.1779 ± 0.0008 mM min−1) (Table 4, p < 0.05). Annison and Topping reported that dietary fibers can be adsorbed to starch and thus decreased hydrolysis of starch by αamylase in the intestinal digestion.34 The activity of α-amylase was also influenced to some extent by the kind of dietary fiber. However, further studies are needed to investigate whether the gum arabic is a competent inhibitor of α-amylase or simply acts as a barrier between the enzyme and starch.23 Diffusion of the Glucose. Diffusion of glucose was different for different porridges (Table 5). Diffused glucose for white rice porridge was significantly higher than that for white rice porridge fortified with gum arabic at all of the time points (p < 0.05). The maximum diffusion velocity (Vmax2) of white rice porridge fortified with gum arabic was (0.0297 ± 0.0005) mM min−1, which was significantly lower than that of white rice porridge (0.0348 ± 0.0007 mM min−1) (Table 4, p < 0.05). Diffused glucose for mixed grain porridge was also significantly higher than that for mixed grain porridge fortified with gum arabic at all of the time points (Table 5, p < 0.05). The maximum diffusion velocity (Vmax2) of mixed grain porridge fortified with gum arabic was 0.0196 ± 0.0008 mM min−1 and was notably lower than that of mixed grain porridge (0.0250 ± 0.0010 mM min−1) (Table 4, p < 0.05). 6411


a b c d 0.02 0.03 0.04 0.02

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The viscosity of porridge may influence the diffusion of glucose. For example, Wood et al. reported that the rates of glucose diffusion from the high viscous solution were considerably less than diffusion in low viscous solution.29 Thus, the increase of the apparent viscosity of porridges due to addition of gum arabic (Table 2) may have some effects on the glucose diffusion. Water-soluble dietary fibers were also reported to have the effects of hampering the diffusion of glucose and postponing the absorption.2 Thus, the addition of gum arabic in porridges may also have the ability of slowing the diffusion of glucose, which was similar to other dietary fibers, such as guar gum, xanthan gum, and oat gum.23,29 Mouse Blood Glucose Rise after Oral Administration of Porridges. As shown in Figure 1, the initial glucose level of

a Data are presented as means ± standard deviations of triplicate measurements. bPorridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. cMean values in the same column with different letters are significantly different (Tukey test, p < 0.05).

0.01 0.04 0.04 0.03 ± ± ± ± 7.50 5.33 5.85 4.44 0.02 0.03 0.05 0.02 ± ± ± ± 6.82 4.61 5.53 4.12 0.02 0.05 0.03 0.04 ± ± ± ± 6.17 4.24 5.02 3.43 0.01 0.05 0.05 0.04 ± ± ± ± 5.13 3.95 4.34 3.23 ± ± ± ±

0.01 0.03 0.04 0.01

150 min

± ± ± ±

4.45 3.28 3.85 2.37

120 min

3.73 2.53 2.94 2.32 a b c d 0.01 0.01 0.03 0.02 ± ± ± ±

90 min

2.99 2.29 2.05 1.92 0.02 0.04 0.02 0.03 ± ± ± ±

60 min

2.12 1.68 1.55 1.42 a b b c 0.03 0.01 0.01 0.03 ± ± ± ±

30 min

1.20 0.95 0.97 0.86 a b c d 0.01 0.01 0.01 0.01 ± ± ± ±

20 min

0.91 0.74 0.71 0.62 ac b b c 0.01 0.01 0.01 0.01 ± ± ± ±

10 min

0.54 0.47 0.47 0.44 1b 2 3 4

samples

porridge porridge porridge porridge

Table 5. Glucose Diffusion of Different Porridges after Digestiona

a b c d

glucose concentration of dialysate (mM)

a b c d

180 min

a b c d

240 min

a b c d

300 min

a b c d

360 min

a b c d


Figure 1. Changes of blood glucose level in mice orally given different porridges.

all groups of mice was near 4.5 mmol/L. The blood glucose levels of all of the mice then increased from 0 to 0.5 h after oral administration of porridges and reached the maximum levels at 0.5 h. However, the blood glucose level of mice in white rice porridge fortified with gum arabic group (10.7 ± 0.4 mmol/L) was notably less than that in the white rice porridge group at 0.5 h (13.0 ± 0.8 mmol/L, p < 0.05). The blood glucose level of mice in mixed grain porridge fortified with gum arabic group (7.5 ± 0.3 mmol/L) was also obviously lower than that of the mixed grain porridge group at 0.5 h (9.9 ± 0.4 mmol/L, p < 0.05). The blood glucose levels of mice in these porridge groups decreased from 0.5 to 1 h, and porridges fortified with gum arabic group mice had significantly lower blood glucose level than that of the unfortified porridges group of mice at 1 h (p < 0.05). The blood glucose levels of these porridge groups returned to the normal level at 2 and 3 h, and there was no significant difference among them (p > 0.05). It can be recognized that the response of blood glucose rise after oral administration of porridges could be significantly lowered due to the addition of gum arabic (p < 0.05). This was consistent with our results for the glucose production (Table 3) and glucose diffusion (Table 5) in this study. It may be also because the gum arabic carried out some effects on the blood glucose rise after oral administration of the porridge. This was similar to the results reported by Schweizer et al.,35 and they compared the serum glucose response of a study group with low dietary fiber intake and a group with high dietary fiber intake. They found that the glucose index of the former was 100% higher than that of the latter. Furthermore, dietary fibers 6412



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Figure 2. Changes in acetic acid (a), propionic acid (b), butyric acid (c), and total SCFA (d) concentrations after 6, 12, and 24 h of fermentation (37 °C, anaerobic) of different porridge samples (after gastrointestinal digestion) and the control (distilled water). Porridge 1, white rice porridge; porridge 2, mixed grain porridge; porridge 3, white rice porridge fortified with gum arabic; porridge 4, mixed grain porridge fortified with gum arabic. Data are expressed as means ± standard deviations. Values from the same time point differ significantly (p < 0.05) when not sharing a common letter. Values for the start of the fermentation experiment (time 0 h) are 9.5 ± 0.3, 4.1 ± 0.2, 3.7 ± 0.3, and 17.3 ± 1.0 mM for (a), (b), (c), and (d), respectively. 6413



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have been reported to help lower the blood glucose rise and glycemic level in serum by increasing the function of the upper gastrointestinal tract as well as the plasma levels of the intestinotrophic factor,36 lowering the insulin response,37 and slowing glucose absorption through an effect on gastric emptying and/or entrapment of materials in the viscous digesta.38 Microbial SCFA Production of Porridge Fermentation. In this study, mixed fresh fecal samples from four donors were used to minimize the difference of the feces from different people.25 In addition, according to the references, the intestinal anaerobic species, Bacteroides, Eubacterium, Clostridium, Lactobacillus, and Bifidobacterium, were found in high numbers and were considered to be the main anaerobic microbes in the stools of normal adults and children. These anaerobic species were also found as the main species in the precultured human fecal slurry that may degrade and ferment carbohydrates.26,39 During the fermentation of porridges, acetic, propionic, and butyric acids were found as the dominant components in total SCFA (Figure 2). As shown in Figure 2a, acetic acid concentrations were strongly increased for all porridge samples upon incubation with human fecal microbiota, the increase being the strongest in the first 6 h of incubation. After 24 h, acetic acid concentrations of the porridge fermented cultures were always significantly higher than that at the time of 0 h (9.5 ± 0.3 mM). At all time points, fermentation of porridges fortified with gum arabic resulted in significantly (p < 0.01) higher concentrations of acetic acid than fermentation of the unfortified porridges. This may result from the addition of the gum arabic, which is a kind of soluble dietary fiber. It was reported that acetic acid is a SCFA that is produced as a result of colonic bacterial fermentation of dietary fiber, and acetic acid exerts beneficial effects on glucose homeostasis in diabetes.40 Several reports have reported that increased acetic acid production in the bowel might, in part, account for the reduction of the postprandial glycemic response, which is one of the beneficial metabolic effects of dietary fiber. Acetic acid was also considered to be beneficial in enhancing glycogen repletion after fasting.41 It has been demonstrated that propionic acid could lower fatty acids content in liver and plasma, and improve tissue insulin sensitivity. Thus, increased production of propionic acid by the microbiota might be considered beneficial in the context of reducing postprandial glycemic response. The concentration of propionic acid was presented in Figure 2b, and it was increased for all porridges with incubation time. Values after 6, 12, and 24 h incubation differed significantly (p < 0.05) from that at the start (4.1 ± 0.2 mM), and the highest level (at 24 h) was 3.5−6.0 times higher than that at time 0 h. At all time points, fermentation of porridges fortified with gum arabic resulted in significantly (p < 0.05) higher concentrations of propionic acid than fermentation of the responding unfortified porridges. Research indicated that dietary fiber had a profound effect on general health, which included the increase of postmeal satiety and the decrease of body weight, fat mass, and the severity of diabetes.41,42 These effects may be contributed via the fermentation of dietary fiber by the colonic microbiota and in turn the production of propionic acid production.43,44 Good evidence exists that systemically relevant concentrations of propionic acid might exert a beneficial effect on insulin sensitivity, and thus propionic acid may well form the link for prebiotics supplementation and their beneficial effects on diabetes and related diseases.5

Butyric acid was also considered to have some beneficial effects on diabetes. In this study, butyric acid concentration differed significantly (p < 0.05) from that at the start of the experiment (3.7 ± 0.3 mM) for all porridges after 6 h incubation (Figure 2c). It continued to increase upon further incubation, and values after 12 and 24 h of incubation were 3− 4 times and 4−5 times higher than that at time 0 h, respectively. Fermentation of porridges fortified with gum arabic resulted in significantly higher concentrations of butyric acid than fermentation of the responding unfortified porridges at the time point of 12 h (p < 0.05). This may be also due to the addition of the gum arabic to the porridges. As a product of the dietary fiber fermentation, the butyric acid was found to have some effects on preventing and treating diet-induced diabetes and insulin resistance in mouse models. The mechanism of the butyric acid action is related to the promotion of energy expenditure and induction of mitochondria function.5 In addition, concentrations of total SCFA at 6, 12, and 24 h during fermentation are presented in Figure 2d. The fermentation cultures for porridges fortified with gum arabic contained significantly higher concentrations of total SCFA than the responding unfortified porridges at all time points (p < 0.05). There have been extensive studies on the health benefit of gum arabic on glucose level and SCFA production. Because of the physical properties of gum arabic, such as viscosity, it was found to be a good in vitro glucosidase inhibitor and have effects on the retardation and delay of carbohydrate and glucose absorption.45−47 Gum arabic was also reported to reach the large intestine without digestion in the small intestine, and it can be mostly fermented by intestinal bacteria to SCFA, particularly propionic acid, in large intestine and feces.46−48 Previous studies mainly focused on the gum arabic itself on glucose level and SCFA production. Limited information is available for the effects of gum arabic on glucose levels and microbial SCFA production in food models. Therefore, our results showed in vitro and in vivo information about the effects of gum arabic on glucose levels and microbial SCFA productions in food model (white rice porridge model and mixed grain porridge model) for the first time. Apparent viscosity of the two porridges was significantly increased after addition of gum arabic, and the glucose productions of porridges were both notably lowered at the same time points during gastrointestinal digestion. Diffused glucose amount was also significantly decreased after gum arabic addition. Furthermore, blood glucose rise after oral administration of porridges fortified with gum arabic in mice was considerably lower than the responding unfortified porridges. Microbial short-chain fatty acid production of porridges during in vitro fermentation was also significantly increased after addition of gum arabic. Therefore, gum arabic may be a helpful ingredient, which could be added in porridges to have benefits for the reduction of postprandial glycemic response.

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AUTHOR INFORMATION

Corresponding Author

*Tel./fax: +86-791-88304452. E-mail: [email protected]. Funding

This study is financially supported by the National Key Technology R&D Program of China (2012BAD33B06), the Key Program of National Natural Science Foundation of China (no. 31130041), the Program for New Century Excellent 6414



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Talents in University (NCET-12-0749), the Project of Science and Technology of Jiangxi Provincial Education Department (KJLD13004), the Research Project of State Key Laboratory of Food Science and Technology (SKLF-ZZA-201301, SKLF-KF201202), and the Jiangxi Provincial Postgraduate Innovation Fund (YC2011-B004), which we gratefully acknowledge. Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED GI, glycemic index; SCFA, short-chain fatty acid; GC, gas chromatography; FID, flame ionization detector

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Effect of Gum Arabic on Glucose Levels and Microbial Short-Chain

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