Resistant Maltodextrin Alleviates Dextran Sulfate Sodium-Induced Intestinal Inflammatory Injury by Increasing Butyric Acid to Inhibit Proinflammatory Cytokine Levels

Abstract

Inflammatory bowel disease (IBD), one kind of intestinal chronic inflammatory disease, is characterized by colonic epithelial barrier injury, overproduction of proinflammatory cytokines, and fewer short-chain fatty acids (SCFAs). The present study is aimed at testing the hypothesis that resistant maltodextrin (RM), a soluble dietary fiber produced by starch debranching, alleviated dextran sulfate sodium- (DSS-) induced colitis in mice. Female C57BL/6 mice with or without oral administration of 50 mg/kg RM for 19 days were challenged with 3% DSS in drinking water to induce colitis (from day 14 to day 19). Although RM could not reverse DSS-induced weight loss or colon shortening, it reduced inflammatory cell infiltration and epithelial damage in colon tissue, as well as the transfer of intestinal permeability indicators including serum diamine oxidase (DAO) and D-lactic acid (D-LA). ELISA analysis indicated that RM significantly suppressed the increase of Th1 cytokines induced by DSS in the colon such as tumor necrosis factor-α (TNF-α) and interferon-γ (IFN-γ). The levels of proinflammatory cytokines interleukin-1β (IL-1β), IL-17, and IL-8 in the DSS group were significantly higher than those in the control group and RM group, but no significant difference was observed in the RM-DSS group compared with the RM group. Interestingly, IL-10 levels of the DSS group were significantly higher than those of the other groups. With respect to SCFAs, DSS administration significantly decreased the concentration of faecal butyric acid while the RM-DSS group showed a tendency to increase (P = 0.08). In general, RM alleviated dextran sulfate sodium-induced intestinal inflammation through increasing the level of butyric acid and subsequently inhibiting the expression of proinflammatory cytokines.

Figure 1

Animal model experimental procedure. RM was administered for the whole period. From day 14 to day 19, DSS (3% (w/v)) was added to drinking water to induce colitis. n = 10 mice/group.

Figure 2

Symptoms of DSS-induced colitis: (a) body weight change, (b) disease activity index (DAI), (c) colon length, and (d) macroscopic pictures of colons. The data are mean ± SEM of n = 10 mice/group. Without the same letter indicated P < 0.05, which means there were significant differences between two groups. CON: group provided water; DSS: group provided 3% DSS (w/v) solution with distilled water; RM: group provided resistant maltodextrin (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage; RM-DSS: group provided with 3% DSS (w/v) solution with distilled water and RM (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage.

Figure 3

Effect of RM on histological and morphological damage in DSS-treated mice: (a) histological examination (the scale bars are 500 μm and 100 μm, individually), (b) colonic histological score, (c) D-LA, and (d) DAO. The data are shown by mean ± SEM of n = 10 mice/group. Different letters indicated P < 0.05, which means there were significant differences between the two groups. CON: group provided water; DSS: group provided 3% DSS (w/v) solution with distilled water; RM: group provided resistant maltodextrin (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage; RM-DSS: group provided with 3% DSS (w/v) solution with distilled water and RM (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage.

Figure 4

Effect of RM on the inflammatory cytokine production in the colons of mice with dextran sulfate sodium- (DSS-) induced chronic colitis. Protein was isolated from the colon tissues for ELISA analysis of TNF-α (a), IFN-γ (b), IL-1β (c), IL-10 (d), IL-17 (e), and IL-8 (f) levels. The data are mean ± SEM of n = 10 mice/group. Without the same letter indicated P < 0.05, and there were significant differences between the two groups. CON: group provided water; DSS: group provided 3% DSS (w/v) solution with distilled water; RM: group provided resistant maltodextrin (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage; RM-DSS: group provided with 3% DSS (w/v) solution with distilled water and RM (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage.

Figure 5

Effect of RM on faecal lactic acid and SCFAs of mice with dextran sulfate sodium- (DSS-) induced chronic colitis. Lactic acid (a), acetic acid (b), propionic acid (c), and butyric acid (d) levels. The data are mean ± SEM of n = 10 mice/group. Without the same letter indicated P < 0.05, and there were significant differences between the two groups. The P value between the DSS and RM-DSS groups was 0.08. CON: group provided water; DSS: group provided 3% DSS (w/v) solution with distilled water; RM: group provided resistant maltodextrin (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage; RM-DSS: group provided with 3% DSS (w/v) solution with distilled water and RM (50 mg/kg body weight/day) dissolving in 100 μL PBS by gavage.