Consumption of Mesona chinensis attenuates postprandial glucose and improves antioxidant status induced by a high carbohydrate meal in overweight subjects.

Am. J. Chin. Med. 2014.42:315-336. Downloaded from www.worldscientific.com by KOREA UNIVERSITY SEJONG CAMPUS LIBRARY on 01/01/15. For personal use only.

The American Journal of Chinese Medicine, Vol. 42, No. 2, 315–336 © 2014 World Scientific Publishing Company Institute for Advanced Research in Asian Science and Medicine DOI: 10.1142/S0192415X14500219

Consumption of Mesona chinensis Attenuates Postprandial Glucose and Improves Antioxidant Status Induced by a High Carbohydrate Meal in Overweight Subjects Charoonsri Chusak,*,‡ Thavaree Thilavech†,‡ and Sirichai Adisakwattana*,‡ *Department

of Nutrition and Dietetics, Faculty of Allied Health Sciences

†

Program in Biomedical Sciences, Graduate School

‡

Research Group of Herbal Medicine for Prevention and Therapeutic of Metabolic Diseases Chulalongkorn University, Thailand

Abstract: Edible plants constitute a potential source for controlling postprandial hyperglycemia and oxidative stress. The objective of this study was to investigate in vitro antioxidant and intestinal -glucosidase inhibitory activities of Mesona chinensis (MC). In addition, the acute effect of MC on postprandial glucose and plasma antioxidant status after the consumption of a high carbohydrate (HC) meal by overweight subjects was also determined. The results showed that total phenolic and flavonoid contents in the extract were 212:37 5:64 mg gallic acid equivalents/g dried extract and 23:44 2:50 mg catechin equivalents/g dried extract, respectively. MC extract markedly inhibited the intestinal maltase and sucrose with the IC50 values of 4:66 0:22 mg/mL and 1:30 0:43 mg/mL, respectively. However, MC extract had no inhibitory activity against pancreatic -amylase. In addition, MC extract had antioxidant properties including DPPH radical scavenging activity, superoxide radical scavenging activity (SRSA), hydroxyl radical scavenging activity (HRSA), trolox equivalent antioxidant capacity (TEAC), ferric reducing antioxidant power (FRAP), oxygen radical absorbance capacity (ORAC), and ferrous ion cheating activity (FICP). The significant decrease in postprandial plasma glucose, triglyceride and malondialdehyde levels, and the increase in plasma antioxidant capacity (FRAP and ORAC) were observed in overweight subjects receiving a HC meal together with MC extract (1 g). The finding supports that MC helps normalize and enhance antioxidant defense induced by a HC meal, suggesting that MC may have the potential for the prevention of chronic conditions and diseases associated with overweight and obesity. Correspondence to: Dr. Sirichai Adisakwattana, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, 154 Rama 1 Rd., Wangmai Pathumwan, Bangkok, Thailand 10330. Tel: (þ66) 2-218-1067, E-mail: [email protected]

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C. CHUSAK et al. Keywords: Mesona chinensis; Antioxidant; -Glucosidase; High Carbohydrate Meal; Overweight.


Introduction Syndrome X is a group of metabolic abnormalities related to abdominal obesity, dyslipidemia, hypertension, and hyperglycemia. Excessive accumulations of abdominal fat, inner abdomen, and visceral fat create the form of overweightness and/or obesity that leads to an increased risk of cardiovascular diseases and type 2 diabetes (Boyko et al., 2000; Grundy et al., 2004). Consumption of carbohydrate-rich diets result in marked increase in postprandial glucose that causes oxidative stress by increasing the production of reactive oxygen species through several biochemical pathways (Hill and Prentice, 1995; Gregersen et al., 2012). Increased oxidative stress has been associated with impaired endothelial function and atherosclerosis, leading to coronary artery disease (Sies and Stahl, 1995; Burton-Freeman, 2010; Hanhineva et al., 2010). In people who are overweight and obese, attenuating postprandial glucose excursion by inhibiting -glucosidase and the reduction of oxidative stress by increasing antioxidant dietary intakes could be a possible strategy to reduce the incidence of diabetes and its complications (Liao et al., 2006; Satoh et al., 2006; O’Keefe et al., 2008; Adisakwattana et al., 2010). A number of studies have shown the beneficial effect of plant-based diets for the inhibition of -glucosidase in vitro and in vivo that delays postprandial hyperglycemia (Mai et al., 2007; Ranilla et al., 2010; Adisakwattana et al., 2011). Furthermore, plantbased diets also contain variable chemical families and amounts of antioxidants. Polyphenols, naturally occurring compounds found in plant-based diets, are considered important to human health. In the last decade, there has been much interest in the potential health benefits of dietary plant polyphenols as antioxidants and -glucosidase inhibitors (Hanhineva et al., 2010). It is believed that dietary plant polyphenols may help to delay postprandial hyperglycemia and increase plasma antioxidant capacity in humans with minimal side effects. Mesona chinensis (MC) Benth (Chinese Mesona) belongs to the same mint family as Lamiaceae. It is an economically valued agricultural plant in Southeast Asia and China (Zhao et al., 2011). MC is most commonly consumed as an herbal drink and a gelatin-type dessert (Grass jelly). This plant-based diet has also been used as an ancient folk medicine to treat hypertension, diabetes and liver diseases (Shen et al., 2000). Previous studies have shown that MC contains 17 amino acids (seven essential amino acids), carbohydrates, fat, fiber, polyphenols, and flavonoids (Liu et al., 2005; Hailan et al., 2011). However, there is currently no evidence of the effects of MC on postprandial glycemia and antioxidant status in humans. The objective of this study, therefore, was to investigate the effects of MC extract on the inhibition of intestinal -glucosidase and antioxidant activity in vitro. In addition, this work was also designed to investigate the acute effect of MC extract on postprandial glucose and plasma antioxidant status in overweight subjects after the consumption of a high carbohydrate (HC) meal.

MESONA CHINENSIS ON BODY WEIGHT

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Materials and Methods


Chemicals and Reagents Fluorescein sodium salt, 2,2 0 -Azobis (2-methylpropionamidine) dihydrochloride, 6-Hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid, bovine xanthine oxidase, 2,2 0 Azino-bis (3-ethylbenzothiazoline-6-sulfonic acid diammonium salt, 2,4,6-Tris(2-pyridyl)s-triazine, rat intestinal acetone powder, porcine pancreatic-amylase, 2,2 0 -diphynyl-1picrylhydrazyl, 2-thiobarbituric acid, tris(hydroxymethyl)aminomethane, 2,2 0 -bipyridyl, hydroxylamine hydrochloride, Folin–Ciocalteu’s phenol reagent, and (þ)-catechin hydrate were purchased from Sigma–Aldrich (St. Louis, MO, USA). Trichloroacetic acid (TCA) was purchased from Merck (Darmstadt, Germany). Gallic acid was purchased from Fluka (St. Gallen, Switzerland). 2-Deoxy-D-ribose was purchased from Affymetrix Inc. (Santa Clara, CA, USA). Glucose and triglyceride liquicolor were purchased from HUMAN GmbH (Wiesbaden, Germany). All other chemicals used were of analytical grade. Plant Preparation and Extraction The dried whole plants were purchased from a specific herbal drugstore in Bangkok, Thailand. The dried plants (300 g) were boiled in distilled water (4 L) at 90 C for 4 h. After boiling, the residue of the plant was filtered with a colander. The aqueous solution was dried using a spray dryer SD-100 (Eyela World, Tokyo Rikakikai Co., LTD, Japan). The condition of the spray dryer was inlet temperature 178–180 C, outlet temperature 85– 95 C, blower 0.80–0.90 m3/min, and atomizing at 90 kPa. The powder extract was kept in a dry place. Measurement of Total Phenolic and Flavonoid Content The content of total phenolics and total flavonoids in the extract was determined using the Folin–Ciocalteu’s phenol reagent and aluminum chloride colorimetric method with a previously published report, respectively (Adisakwattana et al., 2010). The content of total phenolics was expressed as mg gallic acid equivalents/g dried extract. The content of total flavonoids was expressed as mg catechin equivalents/g dried extract. The extract was freshly dissolved in distilled water before use. Intestinal -Glucosidase and Pancreatic -Amylase Inhibitory Activity The intestinal -glucosidase inhibitory activity was done according to a previous study (Adisakwattana et al., 2011). 100 mg of rat intestinal acetone powder was briefly homogenized in 3 mL of 0.9% NaCl solution. After centrifugation (12,000 g 30 min), the crude enzyme solution (10 L) was incubated with 80 L maltose (25.9 mM) or sucrose (60 mM) in 0.1 M phosphate buffer pH 6.9, and 10 L of the sample at various concentrations in distilled water at 37 C for 30 min (maltase assay) and 60 min (sucrase assay).


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The mixtures were suspended in boiling water for 10 min to stop the reaction. The concentrations of glucose released from the reaction mixtures were determined by the glucose oxidase method. The pancreatic -amylase inhibition assay was performed according to a previous report (Adisakwattana et al., 2011). Porcine pancreatic -amylase was dissolved in 0.1 M phosphate buffer saline, pH 6.9. The various concentrations of the sample were added to a solution containing the starch (1 g/L) in 0.1 M phosphate buffer with a pH of 6.9. The reaction was initiated by adding pancreatic -amylase (3 units/mL) to the incubation medium (final volume: 500 L). After 10 min the reaction was stopped by adding 500 L dinitrosalicylic (DNS) reagent (1% 3,5-dinitrosalicylic acid, 0.2% phenol, 0.05% Na2SO3, and 1% NaOH in aqueous solution) to the reaction mixture. The mixtures were heated at 100 C for 10 min to develop the yellow–brown color. Thereafter, 500 L of 40% potassium sodium tartarate solution was added to the mixtures to stabilize the color. After cooling to room temperature in a cold water bath, absorbance was recorded at 540 nm using a spectrophotometer. DPPH Radical Scavenging Activity 2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity was measured according to a previous literature (Mäkynen et al., 2013). Briefly, the sample (100 L) was added to 100 L DPPH solution (0.2 mM in ethanol) and incubated for 30 min at room temperature. The decrease in the solution absorbance was measured at 515 nm. The DPPH radical scavenging activity was calculated from a standard curve using ascorbic acid. The DPPH radical scavenging activity was expressed as an equivalent of ascorbic acid (mg ascorbic acid/g dried extract). Ascorbic acid was used as a positive control for this study. Trolox Equivalent Antioxidant Capacity (TEAC) Assay The Trolox equivalent antioxidant capacity (TEAC) assay was measured according to a previously published report (Mäkynen et al., 2013). Briefly, a 2,2 0 -azinobis(3-ethylbenzothiazoline-6-sulfonate) free radical (ABTS þ ) solution was prepared by mixing 7 mM ABTS þ in 0.1 M phosphate buffer saline (pH 7.4) with 2.45 mM K2S2O4 in distilled water. The solution was kept for 16 h at room temperature in the dark. The ABTS þ was diluted with 0.1 M phosphate buffer saline (pH 7.4) to absorbance between 0.900 and 1.000 at 734 nm. 10 L of the extract (1 mg/mL) was mixed with 90 L the diluted ABTS þ solution. After 6 min, the absorbance was measured at 734 nm. The TEAC value was calculated from the calibration curve of Trolox. The TEAC value was expressed as mg Trolox equivalents/mg dried extract. Ferric Reducing Antioxidant Power (FRAP) Assay The FRAP assay was measured according to a previously published report (Mäkynen et al., 2013). The FRAP reagent contained 0.30 M sodium acetate buffer solution (pH 3.6),


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10 mM 2,4,6-tripyridyl-S-triazine (TPTZ) in 40 mM HCl and 20 mM FeCl3 in the ratio 10:1:1 and freshly prepared. 90 L of the FRAP reagent was mixed with 10 L of the extract (1 mg/mL). The mixture reaction was incubated at room temperature and kept in the dark. After 4 min, the absorbance was measured at 595 nm. The FRAP value was calculated from the calibration curve of FeSO4. The FRAP value was expressed as mM FeSO4 equivalents/mg dried extract.


Hydroxyl Radical Scavenging Activity The HRSA measurement was done according to a previously described method (Halliwell et al., 1987). The reaction mixture was generated by adding 30 L of 2-deoxy-2-ribose (17 mM), 30 L of the extract, 30 L of 1.2 mM EDTA, 60 L of 0.3 mM FeCl3, 30 L of 34 mM hydrogen peroxide (H2O2), and 60 L of 0.6 mM ascorbic acid. The reaction was performed at 37 C for 1 h. Thereafter, 150 L of 1% (w/v) thiobarbituric acid (TBA) and 300 L of 2.8% (w/v) TCA were added to the mixture, which was then incubated at 100 C for 15 min. After cooling, the absorbance was measured at 532 nm against a blank containing deoxyribose and buffer. Trolox was used as a positive control for this study. Superoxide Radical Scavenging Activity The measurement of superoxide radical scavenging activity (SRSA) was done according to a previous method (Kweon et al., 2001) with slight modification. In brief, 7.5 L of the sample, 150 L of 0.30 mM xanthine, 50 L of 0.15 mM NBT, 50 L of 0.60 mM EDTA, and 7.5 L of xanthine oxidase (0.05 unit/mL) were mixed in a microplate. After incubation for 40 min at 37 C, the absorbance was measured at 560 nm against an appropriate blank to determine the quantity of formazan generated. A Trolox was used as a positive control for this study. Ferrous Ion Chelating Activity The ferrous ion chelating activity (FICP) was measured according to a previous report with a minor modification (Yamaguchi et al., 2000). In brief, 25 L of 1 mM FeSO4 solution and an equal volume of extract was mixed with 100 L of Tris-HCl buffer (pH 7.4), 100 L of 2,2 0 -bipyridyl solution (0.1% in 0.2 M HCl), 40 L of 10% (w/v) hydroxylamine-HCl, and 150 L of ethanol, respectively. After the total volume of the reaction mixture was adjusted to 1 mL by distilled water, the absorbance was recorded at 522 nm. The FICP was calculated from the calibration curve of EDTA. The activity was expressed as mg of EDTA equivalents/mg dried extract. Oxygen Radical Absorbance Capacity (ORAC) Assay The ORAC assay was done according to a previous method with slight modification (Wang et al., 2011). The sample (25 L) was mixed with 48 nM sodium fluorescein (150 L) in

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75 mM phosphate buffer saline. After incubation for 10 min at 37 C, AAPH (25 L) solution was then added to the mixture. The fluorescence intensity (excitation ¼ 485 nm; emission ¼ 535 nm) was measured every minute until 1 h. The quantitation of the antioxidant capacity was calculated using the area under the curve (AUC). The ORAC value was calculated from AUC of Trolox. The ORAC value was expressed as mol Trolox equivalents/mg dried extract.


Human Study Men (n ¼ 11) aged 20–40 years that were free of any serious illness, did not use tobacco products and were not taking any medications or nutritional supplements were recruited for the study. Other inclusion characteristics were BMI of 23–30 kg/m2, resting blood pressure < 160=100 mm Hg, fasting blood glucose < 100 mg/dL, fasting total cholesterol < 200 mg/ dL, fasting triglyceride < 150 mg/dL. The study was approved by the office of Ethics Review Committee for Research Involving Human Research Subjects, Human Science Group, Chulalongkorn University (COA No. 178/2555). A randomized, controlled, 3period crossover study with two weeks’ separation between testing sessions was conducted. The three test conditions were a HC meal, a HC meal plus 0.5 g of MC extract and a HC meal plus 1 g of MC extract. A HC meal consisted six tablespoons of Ensure® (230 mL) and three slices of white bread with one tablespoon of condensed milk. The consumption of the meal was approximately 69% of calories as carbohydrate, 15% as protein, and 16% as fat. Participants were instructed to avoid high antioxidant foods for 48 h prior to testing. After 8 h of fasting, the participants were allowed 15 min to consume the meal. The first postprandial blood sample was collected at the end of the 30 min eating period. Subsequently, blood was collected every 30 min for 4 h. For each sample, blood was centrifuged and portions of plasma were kept and stored at 20 C. Assay Methods Plasma glucose was determined by using a glucose oxidase method (HUMAN GmbH, Germany). Serum triglyceride was determined by using a triglyceride enzymatic colorimetric method (HUMAN GmbH, Germany).

Plasma FRAP Assay Plasma FRAP was determined according to a previously published report (Benzie and Strain, 1996). The plasma was diluted to 1:5 with 0.1 M phosphate buffer saline (pH 7.4). The FRAP reagent contained 0.3 M of sodium acetate buffer saline (pH 3.6), 10 mM TPTZ in 40 mM HCl, and 20 mM FeCl3. 90 L of FRAP reagent was mixed with 10 L of the diluted plasma. The reaction mixture was incubated in the dark at room temperature for 30 min and the absorbance was read at 595 nm. The FRAP value was calculated from the calibration curve of FeSO4 and expressed as mM FeSO4 equivalents.


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Plasma ORAC Assay Plasma ORAC assay was determined according to a previously published report with slight modifications (Wang et al., 2011). The plasma was diluted to 1:10 with 0.1 M phosphate buffer saline (pH 7.4). The diluted plasma (25 L) was mixed with 4.8 nM sodium fluorescein in 75 mM phosphate buffer saline (150 L). After incubation at 37 C for 10 min, 25 L of 64 mM AAPH was added to the mixture. The fluorescence intensity (excitation ¼ 485 nm; emission ¼ 535 nm) was measured every 2 min for 1 h. The quantitation of the antioxidant capacity was calculated by using the AUC following equation: AUCantioxidant ¼ AUCS AUCb where AUCS was the AUC of the diluted plasma and AUCb was the area under the curve of the blank (0.1 M PBS). The ORAC value was calculated from the calibration curve of Trolox and expressed as mol Trolox equivalents. Plasma MDA Assay Plasma malondialdehyde (MDA) was determined according to a previously published report (Wolff and Dean, 1987). The plasma (160 L) was mixed with 160 L of 10% thichloroacetic acid (TCA) and 30 L of 50 M 2,6-di-tert-butyl-4-methylphenol (BHT). The mixture was centrifuged at 13,000 rpm for 10 min at 4 C to precipitate proteins. After 0.67% thiobarbituric acid (150 L) was added to the supernatant (150 L), the mixture solution was incubated at 95 C for 10 min. Then, the solution was cooled at room temperature and was read at 532 nm. MDA was used for a calibration curve. Plasma MDA concentration was calculated from the calibration curve of MDA. Statistical Analysis The IC50 values were calculated from plots of the log concentration of inhibitor concentration vs. percentage inhibition curves. Data were expressed as mean standard error of the mean (SEM), n ¼ 3. In the human study, postprandial incremental areas were calculated by the trapezoidal method as the AUC above the baseline value. One-way repeated measure ANOVA was used for comparison of the time point within groups, followed by Post hoc test by Least Square Significance (LSD) for multiple comparisons. p value < 0:05 was considered to be a statistically significant difference.

Results Phytochemical Analysis Phenolic compounds and flavonoids are considered as major contributors to antioxidant activity as well as the intestinal -glucosidase and pancreatic -amylase inhibitory activity. Therefore, the dried extract was examined for total phenolic content and flavonoids. The

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Table 1. The IC50 Values for Intestinal ®-Glucosidase (Maltase and Sucrase), and Pancreatic ®-Amylase by MC MC

IC50 Values

Intestinal maltase Intestinal sucrase Pancreatic -amylase

4.66 0.22 1.30 0.43 NI

Note: Results are expressed as means SEM, n ¼ 3. Intestinal maltase and sucrase inhibitory activities are expressed as the IC50 value (mg/mL). NI ¼ no inhibition.

results showed that the total phenolic and flavonoid content of MC extract was 212:37 5:64 mg gallic acid equivalents/g dried extract, and 23:44 2:50 mg catechin equivalents/g dried extract, respectively. The Intestinal -Glucosidase and Porcine -Amylase Inhibitory Activity MC extract was investigated for inhibitory activity against the intestinal -glucosidase (maltase and sucrase). The results exhibited that MC extract markedly inhibited the intestinal maltase and sucrase in a concentration-dependent manner (data not shown). As shown in Table 1, the IC50 values of MC extract on intestinal sucrase and maltase were 1:30 0:43 mg/mL and 4:66 0:26 mg/mL, respectively. Nevertheless, MC extract did not show any effect on pancreatic -amylase inhibition. Antioxidant Capacities The effects of MC extract on different antioxidant capacities are shown in Table 2. On the DPPH assay, MC extract had significant radical scavenging activity, with increasing concentration in the range of 0.05–1.00 mg/mL. The IC50 values of MC extract and ascorbic acid were found to be 0:14 0:02 mg/mL and 0:02 0:01 mg/mL, respectively, indicating that MC extract had seven times less potency than ascorbic acid. According to

Table 2. The DPPH, TEAC, FRAP, ORAC, HRSA, SRSA, and FICP of MC Antioxidant Activity

MC

DPPH

TEAC

FRAP

ORAC

HRSA

SRSA

FICP

0.14 0.02

0.41 0.02

1.42 0.06

25.98 1.30

0.09 0.01

0.38 0.03

0.33 0.01

Note: Data are expressed as mean SEM, n ¼ 3. DPPH radical scavenging activity, SRSA (superoxide radical scavenging activity), and HRSA (hydroxyl radical scavenging activity) were expressed as the IC50 value (mg/mL). TEAC was expressed as mg trolox equivalents/mg dried extract. FRAP was expressed as mM FeSO4 equivalents/mg dried extract. ORAC was expressed as mol trolox equivalents/mg dried extract. FICP was expressed as mg EDTA equivalents/mg dried extract.



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the results from the TEAC assay, MC extract had the ability of 0:41 0:02 mg Trolox equivalents/mg dried extract. A FRAP assay determined the reducing ability of an antioxidant reacting with a ferric tripyridyltriazine (Fe 3þ –TPTZ) complex and producing a colored ferrous tripyridyltriazine (Fe 2þ –TPTZ). MC extract had a FRAP value of 1:42 0:06 mM FeSO4 equivalents/mg dried extract. Moreover, the ORAC value of the extract was 25:98 1:30 as mol Trolox equivalents/mg dried extract. The hydroxyl radical is one of the representative reactive oxygen species generated in the body. The results showed that the IC50 values of MC and Trolox were 0:09 0:01 mg/mL and 0:03 0:01 mg/mL, respectively. This suggests that MC extract had three times less potency than Trolox. In addition, MC extract had the superoxide radicals scavenging activity in a concentration-dependent manner with the IC50 value of 0:38 0:03 mg/mL, while the IC50 value of Trolox was found to be 1:40 0:21 mg/mL. The results showed that MC extract had 3.65 times more potency than Trolox. Furthermore, MC extract had the FICP with 0:33 0:01 mg EDTA equivalents/mg dried extract. Human Study The screening and visit baseline characteristics of the participants are presented in Table 3. The effects of MC extract, together with a HC meal, on the incremental postprandial glucose are presented in Fig. 1A. The basic carbohydrate meal caused a rapid rise of glucose, with the peak concentration at 30 min, followed by a rapid fall below the baseline level within 210 min. Ingestion of MC extract together a HC meal results in a lower glucose concentration and a slow decline during the 210 min. Comparing at individual time points with a HC meal, the incremental plasma glucose concentration was significantly decreased at 120 min ( p ¼ 0:041), 150 min ( p ¼ 0:020), 180 min ( p ¼ 0:021), and 240 min ( p ¼ 0:008) after consuming the HC meal plus 0.5 g of the extract. Meanwhile, the incremental plasma glucose concentration was significantly decreased at

Table 3. Baseline Characteristics of Eleven Participants in the Study Variable Age (years) Weight (kg) Height (cm) BMI (kg/m 2 ) Plasma glucose (mg/dL) Total cholesterol (mg/dL) Serum triglyceride (mg/dL) Creatinine (mg/dL) SGOT (U/L) SGPT (U/L)

25.0 73.15 172.64 24.71 94.0 194.0 89.7 0.97 20.08 12.08

0.68 2.98 1.86 0.34 2.51 5.86 7.43 0.02 1.04 1.90

Note: Data are expressed as mean SEM, n ¼ 11.


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(A)

(B) Figure 1. The effects of MC on the incremental plasma glucose concentration (A) and the incremental AUCs of plasma glucose concentration (B) induced by a HC meal in overweight subjects (n ¼ 11). Values are means with standard error of the means (SEMs). Mean value was significantly different from that of a HC meal: *p < 0:05.

90 min ( p ¼ 0:000), 120 min ( p ¼ 0:017), 180 min ( p ¼ 0:023), and 240 min ( p ¼ 0:003) after consuming a HC meal plus 1 g of the extract. As shown in Fig. 1B, the incremental AUCs of plasma glucose concentration was significantly reduced after consumption of a HC meal plus 1 g of the extract ( 38:98 16:97 min mg=dL) compared to a HC meal (47:20 21:06 min mg=dL) ( p ¼ 0:009). However, there was no significant difference between a HC meal plus 0.5 g of the extract and a HC meal alone (13:01 14:39 min mg=dL).



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(A)

(B) Figure 2. The effects of MC on the incremental plasma FRAP level (A) and the incremental AUCs of FRAP level (B) induced by a HC meal in overweight subjects (n ¼ 11). Values are means with SEMs. Mean value was significantly different from that of a HC meal: *p < 0:05.

As shown in Fig. 2A, consumption of a HC meal with MC extract results in higher plasma FRAP concentrations at 90 min. Comparing with a HC meal at the individual time points, only at 90 min after administration of a HC meal plus 0.5 g of the extract, the incremental plasma FRAP level ( p ¼ 0:006) significantly increased. In the meantime, the incremental plasma FRAP level in a HC meal plus 1 g of the extract was significantly increased at 30 min ( p ¼ 0:013), 90 min ( p ¼ 0:002), 150 min ( p ¼ 0:042) and 210 min

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( p ¼ 0:008), respectively. In Fig. 2B, the incremental AUCs for plasma FRAP level were significantly higher in a HC meal plus 0.5 g of the extract ( p ¼ 0:002; 128:29 72:60 min mol=L), as well as a HC meal plus 1 g the extract ( p ¼ 0:016; 162:22 116:34 min mol=L), when compared to HC meal (220 59:47 min mol=l). The individual time points of the incremental postprandial plasma ORAC level were significantly increased at 30 min ( p ¼ 0:05), 60 min ( p ¼ 0:016), 90 min ( p ¼ 0:028), and 240 min ( p ¼ 0:034) after consumption of a HC meal plus 0.5 g of the extract (Fig. 3A).

(A)

(B) Figure 3. The effects of MC on the incremental plasma ORAC level (A) and the incremental AUCs of ORAC level (B) induced by a HC meal in overweight subjects (n ¼ 11). Values are means with SEMs. Mean value was significantly different from that of a HC meal: *p < 0:05.


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In addition, the group administered a HC meal together with 1 g of the extract also significantly increased the incremental postprandial plasma ORAC level at 90 ( p ¼ 0:018), 210 ( p ¼ 0:016), and 240 min ( p ¼ 0:030), respectively. As shown in Fig. 3B, the incremental AUCs of plasma ORAC level in the groups receiving a HC meal plus 0.5 g of the extract ( p ¼ 0:036; 78:40 20:49 min mol=L) and a HC meal plus 1 g of the extract

(A)

(B) Figure 4. The effects of MC on the incremental plasma MDA level (A) and the incremental AUCs of MDA level (B) induced by a HC meal in overweight subjects (n ¼ 11). Values are means with SEMs. Mean value was significantly different from that of a HC meal: *p < 0:05.

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( p ¼ 0:033; 61:07 18:75 min mol=L) were significantly higher than of a HC meal (154:91 86:45 min mol=L). Comparing at individual time points with a HC meal, a significant decrease in the incremental postprandial plasma MDA level at 30 min ( p ¼ 0:007), 180 min ( p ¼ 0:046) and 210 min ( p ¼ 0:010) was observed after ingestion of a HC meal plus 1 g of the extract (Fig. 4A). No significant changes in the plasma MDA level were seen after a HC meal plus

(A)

(B) Figure 5. The effects of MC on the incremental serum triglyceride concentration (A) and the incremental AUCs of serum triglyceride concentration (B) induced by a HC meal in overweight subjects (n ¼ 11). Values are means with SEMs. Mean value was significantly different from that of a HC meal: *p < 0:05.



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0.5 g of the extract. As shown in Fig. 4B, only the administration of MC extract (1 g) showed a significant decrease in the incremental AUCs of plasma MDA (0:124 0:11 min mol=L), as compared to a HC meal (0:312 0:10 min mol=L) ( p ¼ 0:043). In addition, there was no significant change in the incremental AUCs of a HC meal plus 0.5 g of the extract (0:074 0:15 min mol=L). Figure 5A shows the effects of MC on the incremental postprandial serum triglyceride concentration. After the consumption of a HC meal, the postprandial triglyceride concentration peaks at 180 min, while MC extract (0.5 g and 1.0 g) suppressed the postprandial triglyceride concentrations at 210 min ( p ¼ 0:003 and p ¼ 0:006) and 240 min ( p ¼ 0:008 and p ¼ 0:012), respectively. As shown in Fig. 5B, an intake of a HC meal plus 0.5 g ( p ¼ 0:031) and 1 g ( p ¼ 0:033) of the extract significantly reduced the incremental AUCs of serum triglyceride concentration (32:39 17:43 min mg=dL and 39:92 20:03 min mg=dL, respectively) as compared to a HC meal (123:98 37:06 min mg=dL). Discussion The intestinal -glucosidases are the key enzymes of dietary carbohydrate digestion. Starch is primarily digested in the small intestine through the action of pancreatic -amylase, yielding both linear maltose and branched isomaltose oligosaccharides, which are further hydrolyzed by intestinal -glucosidase (sucrase and maltase) to release absorbable monosaccharides (Inzucchi, 2002). The inhibition of these enzymes significantly suppresses postprandial hyperglycemia and may have beneficial effects on insulin resistance and glycemic index control in diabetic patients (Inzucchi, 2002). The administration of acarbose results in a 20% reduction in the postprandial peak of glycemia and a 25% reduction in the incidence of diabetes (Chiasson, 2006). Additionally, the long-term administration of -glucosidase inhibitor may decrease the level of HbA1c , resulting in a significant reduction in the incidence of diabetic complications such as micro- and macrovascular diseases (Scorpiglione et al., 1999). The most common side effects of acarbose are mild-to-moderate gastrointestinal disturbance such as flatulence, meteorism and abdominal distention that occurs in a dose-dependent pattern (Hanefeld et al., 1991). Our results indicate that MC extract showed a marked inhibition against intestinal -glucosidase, especially for sucrose, whereas it had no inhibitory activity on pancreatic -amylase. Excessive inhibition of pancreatic -amylase causes gastrointestinal side effects related to abnormal bacterial fermentation of undigested carbohydrates in the large intestine (Kwon et al., 2008). It has been suggested that plant-based foods have lower inhibitory activity against pancreatic -amylase and stronger inhibitory activity against intestinal -glucosidase, indicating that they may be effective agents for the control of postprandial hyperglycemia with fewer side effects than acarbose (Kwon et al., 2008). It is noteworthy that polyphenols and flavonoids have been shown to inhibit intestinal -glucosidase activity in vitro (Koh et al., 2009; Fontana Pereira et al., 2011). The earlier studies report a strong correlation between the polyphenolic content in the extracts and the ability to inhibit intestinal -glucosidase (Mai et al., 2007; Ramkumar et al., 2010). According to the results


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obtained, the findings suggest that MC contains high polyphenolic compounds and flavonoids that may be related to its intestinal -glucosidase inhibitory activity. It has been shown recently that flavonoids inhibit the enzymes through hydrogen bonding interactions between the hydroxyl groups of the flavonoids and the catalytic residues of the binding site (Xiao et al., 2013). The molecular interaction of flavonoids in the extract on a specific binding site on intestinal -glucosidase remains unknown. However, it can be assumed that flavonoids in the MC extract may interact with enzymes via these interactions. Free radicals play an important role in the development of pathogenesis in several human diseases, such as rheumatoid arthritis, diabetes and its complications, cancer, and various neurodegenerative and pulmonary diseases (Bjelakovic et al., 2008). Antioxidants from human diets have the ability to neutralize free radicals and can protect the cells from damaging oxidation. The literature has documented antioxidant activity of Mesona procumbens Hemsl. (Hsian-tsao) through a thiocyanate method (Hung and Yen, 2002). In addition, the extract of Mesona procumbens leaf gum has also shown antioxidant activity including the radical-scavenging effects, FICP, and reducing power (Lai et al., 2001). The results showed that the extract was more effective in scavenging superoxide radicals than chelating ferrous ion or scavenging DPPH radicals. The current study was the comprehensive investigation to determine the antioxidant activity of MC extract, including DPPH radical scavenging activity, TEAC, FRAP, ORAC, hydroxyl, and superoxide radical scavenging activities, as well as metal chelating activity. Several studies reveal that phenolic compounds and flavonoids have been reported to be major phytochemicals responsible for antioxidant activity (Zheng and Wang, 2001; Palacios et al., 2011). In addition, flavonoids found in the edible plants act as antioxidants by trapping free radicals (Cao et al., 1997). Previous studies demonstrated the strong correlation between phenolic compounds, flavonoids, and antioxidant activity (Rice-Evans et al., 1996; Mäkynen et al., 2013). The findings show that MC contains high levels of phenolic compounds and flavonoids. These results appear to suggest that phenolic compounds and flavonoids in the extract may contribute to the antioxidant activity of MC. The increased oxidative stress in the overweight and obese plays a pivotal role in the pathogenesis of metabolic syndromes. Excessive free radicals generally cause the tissue damage and regulate the inflammatory status in adipocytes (Zhu et al., 2006). Being overweight and obesity are independent risk factors for plasma lipid peroxidation and poor glycemic control that can cause protein oxidation (Osawa and Kato, 2005; Ahmed et al., 2005). Interestingly, the consumption of carbohydrate-rich meals has been shown to increase postprandial glucose and oxidative stress by active oxidative metabolism and formation of reactive oxygen species induced oxidative stress (Hill and Prentice, 1995; Gregersen et al., 2012). An increase in oxidative stress has been associated with a corresponding increase in diverse diseases, including endothelial dysfunction, diabetic complications, atherosclerosis, and hypertension (Johnson, 2012; Popolo et al., 2013; Sun et al., 2013). A previous study reveals that the consumption of small amounts of antioxidant rich food has been associated with inadequate antioxidant defenses in Spanish obesity (Schröder et al., 2004). Additionally, the consumption of a HC meal results in a greater and more prolonged oxidative stress in obese subjects than in normal subjects



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(Patel et al., 2007). According to the results from in vitro, we assume that the consumption of MC extract together with a HC meal may decrease postprandial glucose and increase antioxidant status in overweight subjects. Our findings exhibited that MC extract markedly decreased postprandial glucose induced by a HC meal in overweight men. In healthy humans, the postprandial plasma glucose concentration typical peaks approximately 30– 60 min after intake of a HC meal. It consequently returns to baseline within 120–180 min (Brynes et al., 2003). The results showed that consumption of MC extract (1 g) could not attenuate the peak of postprandial plasma glucose within 30 min, but the postprandial plasma glucose was suppressed after 60 min of administration. It can be suggested that the underlying mechanism of MC extract on the postprandial plasma glucose lowering effect may be involved in the inhibition of -glucosidase in vitro. Hanhineva et al. (2010) suggested that dietary polyphenol may influence carbohydrate metabolism and glucose homeostasis at many levels. The possible mechanisms of dietary polyphenol include the inhibition of -glucosidase and glucose absorption in the small intestine, the stimulation of insulin secretion from pancreatic β-cell or the activation of glucose uptake via glucose transporter at adipose tissues and skeletal muscles (Rutter, 2001; Hanhineva et al., 2010; Nicolle et al., 2011). It is possible that MC extract may have other mechanisms on the plasma glucose lowering effect. Further studies are required to explore the extract responsible for the stimulation of insulin secretion and the activation of glucose uptake. Interesting reports have shown that the attenuated and prolonged postprandial plasma glucose reduces the independent risk factors for macrovascular complications (Ceriello, 2010). A previous study has shown that consumption of a HC meal results in increasing postprandial triglyceride concentrations after 3–4 h (Wolever et al., 2013). A HC meal can induce hypertriglyceridemia because it increases the production rate and decreases the clearance rate of VLDL particles. These results cause the alteration of serum lipid profiles (Hellerstein, 2002). The attenuation of carbohydrate-induced postprandial triglyceride may reduce the risk of cardiovascular disease via the reduction of VLDL particles (Parks, 2001). In the present study, postprandial triglyceride exhibited a similar pattern to a previous study. The rise in postprandial triglyceride was attenuated by the extract 3 h after consumption. Our data suggest that MC extract has beneficial effects on delaying postprandial triglyceride that may reduce the risk of developing macrovascular complications in overweight or obesity. The postprandial state has been described as pro-oxidative, with the magnitude of the oxidative stress response linked to a HC meal (Ceriello et al., 1999). The previous studies have demonstrated that the consumption of a HC diet markedly reduces postprandial endogenous antioxidant levels such as sulfhydryl (-SH) groups, uric acid and vitamin C, as well as plasma antioxidant status. Contrastingly, it can increase a marker of oxidative damage called as malondialdehyde (MDA) (Ceriello et al., 1999; Mah et al., 2011). Skulas-Ray et al. (2011) demonstrated that adding 14 g of high antioxidant spice blend to a meal exerted postprandial plasma FRAP and ORAC in overweight men. Moreover, Micallef et al. reported that the consumption of 400 mL/day of red wine enriched with anthocyanin significantly increased plasma thiol and decreased plasma MDA in young and old subjects (Micallef et al., 2007). Roussel et al. (2009) demonstrated that the


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consumption of polyphenol-rich extract of cinnamon significantly increased plasma thiol and FRAP levels associated with the reduction of plasma MDA concentration in the overweight and obese after 12 weeks of study. This evidence suggests that cinnamon extract has a protective effect against lipid and protein oxidation, together with an increasing antioxidant status (Roussel et al., 2009). The increasing postprandial oxidative stress may impair the pathogenesis and complications of several chronic diseases such as cardiovascular disease and diabetes mellitus. Interestingly, it has been reported that an increase in plasma antioxidant status associated with the reduction of lipid peroxidation may help to reduce the incidence of CVD in healthy adults (Ashfaq et al., 2006; Halliwell and Chirico, 1993). From the current study, consumption of MC together with a HC meal reduces postprandial glucose and increases antioxidant status as well as decreases MDA levels, suggesting that MC extract acts in protecting lipid oxidation. These findings raise the possibility that polyphenol-rich MC extract may therefore be a natural anti-atherosclerotic component of the diet. However, the limitation of this study was the relatively small sample size and the selection of only overweight men. Further study is needed to characterize these effects in long-term consumption, large sample sizes, and more diverse populations such as obesity and people with cardiovascular risk factors.

Conclusions MC (Chinese mesona) extract demonstrates beneficial effects on intestinal -glucosidase inhibitory activities as well as antioxidant activity. MC also reduces postprandial glucose and increases antioxidant status in a HC meal of overweight people. The available evidence appears to suggest that MC could be a potential alternative for food and pharmaceutical applications for the prevention of cardiovascular diseases and diabetes and its complications.

Acknowledgments We wish to thank Amway Thailand for the partial financial support (Amway for Nutrition Research Grant). The authors would also like to thank the Special Task Force for Activating Research (STAR) under 100 years Chulalongkorn University Fund and the Research Group of Herbal Medicine for Prevention and Therapeutic of Metabolic Diseases for financial support. References Adisakwattana, S., P. Jiphimai, P. Prutanopajai, B. Chanathong, S. Sapwarobol and T. Ariyapitipan. Evaluation of -glucosidase, -amylase and protein glycation inhibitory activities of edible plants. Int. J. Food Sci. Nutr. 61: 295–305, 2010. Adisakwattana, S., O. Lerdsuwankij, U. Poputtachai, A. Minipun and C. Suparpprom. Inhibitory activity of cinnamon bark species and their combination effect with acarbose against intestinal -glucosidase and pancreatic -amylase. Plant Food Hum. Nutr. 66: 143–148, 2011.



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Carbohydrate-last meal pattern lowers postprandial glucose and insulin excursions in type 2 diabetes.

Resistance Exercise Attenuates High-Fructose, High-Fat-Induced Postprandial Lipemia.

Orange juice intake during a fatty meal consumption reduces the postprandial low-grade inflammatory response in healthy subjects.

Blood pressure, heart rate and neuroendocrine responses to a high carbohydrate and a high fat meal in healthy young subjects.

Proprietary tomato extract improves metabolic response to high-fat meal in healthy normal weight subjects.

Contribution of postprandial insulin and glucose to glucose disposal in normal and insulin-resistant obese subjects.

Mechanism of growth hormone-induced postprandial carbohydrate intolerance in humans.

Postprandial plasma lipoprotein responses to a mixed meal in subjects with hyperapobetalipoproteinaemia.

Effect of different protein types on second meal postprandial glycaemia in normal weight and normoglycemic subjects.

Mulberry leaf extract improves postprandial glucose response in prediabetic subjects: a randomized, double-blind placebo-controlled trial.

Combined Supplementation with Grape Pomace and Omija Fruit Ethanol Extracts Dose-Dependently Improves Body Composition, Plasma Lipid Profiles, Inflammatory Status, and Antioxidant Capacity in Overweight and Obese Subjects.

Fruit Fiber Consumption Specifically Improves Liver Health Status in Obese Subjects under Energy Restriction.

Effect of acarbose on postprandial blood glucose concentrations in healthy cats fed low and high carbohydrate diets.

Weight loss enhances hepatic antioxidant status in a NAFLD model induced by high fat diet.

Asiatic acid attenuates renin-angiotensin system activation and improves vascular function in high-carbohydrate, high-fat diet fed rats.

Acute ingestion of catechin-rich green tea improves postprandial glucose status and increases serum thioredoxin concentrations in postmenopausal women.

A meal replacement regimen improves blood glucose levels in prediabetic healthy individuals with impaired fasting glucose.

Fuzi attenuates diabetic neuropathy in rats and protects schwann cells from apoptosis induced by high glucose.

Alpha-lipoic acid attenuates insulin resistance and improves glucose metabolism in high fat diet-fed mice.

Alteration of postprandial glucose and insulin concentrations with meal frequency and composition.

Hepatic carboxylesterase 1 is induced by glucose and regulates postprandial glucose levels.

Chamnamul [Pimpinella brachycarpa (Kom.) Nakai] ameliorates hyperglycemia and improves antioxidant status in mice fed a high-fat, high-sucrose diet.

Mesona Chinensis Benth extract prevents AGE formation and protein oxidation against fructose-induced protein glycation in vitro.

Actinidia chinensis Planch. Improves the Indices of Antioxidant and Anti-Inflammation Status of Type 2 Diabetes Mellitus by Activating Keap1 and Nrf2 via the Upregulation of MicroRNA-424.