Gastric Infusion of Short-Chain Fatty Acids Improves Health via Enhance Liver and Intestinal Immune Response and Antioxidant Capacity in Goats

Abstract

In the present study, we comprehensively investigated the impacts of the infusion of three short-chain fatty acids (SCFAs), sodium acetate (SA), propionate (SP), and butyrate (SB), to examine their respective roles in the gastrointestinal tract (GIT) health and innate immunity of twenty adult Guanzhong milk goats of 1.5 years of age. Infusion of SCFAs resulted in upregulating the activity of certain antioxidant enzymes in comparison with the control group. The SA group significantly (p < 0.05) increased the activity of the catalase (CAT) in the liver, glutathione peroxidase (GSH-Px) and superoxide dismutase (SOD) in the colon, and maleic dialdehyde (MDA) in the jejunum. SP significantly (p < 0.05) upregulated the activity of the total antioxidant capacity (T-AOC) in the ileum, CAT and MDA in the jejunum, CAT in the colon, and SOD in the liver. SB was significantly (p < 0.05) upregulated the activity of the T-AOC in the ileum, CAT in the jejunum, and T-AOC, CAT, SOD, and GSH-Px in the colon. Infusion of SCFAs resulted in significant (p < 0.05) increases in pro-inflammatory and anti-inflammatory cytokines in the intestine compared to the control group. We found that the SA group significantly (p < 0.05) upregulated the level of interleukin-1 beta (IL-1β) in the ileum and jejunum, as well as the levels of IL-6 and TNF-α in the colon, while the SP group significantly (p < 0.05) increased the level of IL-1β in the jejunum and the level of interleukin-10 (IL-10) in the colon. Furthermore, the SB group significantly (p < 0.05) upregulated levels of IL-1β in the jejunum, interleukin-6 (IL-6), tumor necrosis factor alpha (TNF-α) in the colon, and IL-10 in the cecum. Furthermore, some intestinal tight-junction proteins were significantly increased by SCFA infusion. SA significantly (p < 0.05) increased the claudin level in the ileum and occludin in the colon, while the SP group significantly (p < 0.05) upregulated the level of occludin in the jejunum and the claudin level in the ileum. Moreover, SB significantly (p < 0.05) increased the occludin level in the jejunum, claudin level in the ileum, and zonula occludens-1 (ZO-1) level in the colon and cecum. There are many positive associations among antioxidant, inflammatory cytokine, and tight-junction protein indexes in the liver and intestine. In conclusion, our results suggest that the gastric infusion of SA, SP, and SB might improve goat intestinal health through the positive influence on the antioxidant capacity, pro-inflammatory and anti-inflammatory cytokines, and tight-junction proteins.

Keywords: antioxidant; gastrointestinal tract; immune; short-chain fatty acids.

Figure 1

The effects of gastric infusion of SCFAs on T-AOC activities in the liver (A) and intestine (jejunum (B), ileum (C), colon (D), and cecum (E)) of goats. Different letters above the bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; T-AOC, total antioxidant capacity.

Figure 2

The effects of gastric infusion of SCFAs on CAT and SOD activities in the liver and intestine of goats. (A–E): Representative charts of the effects of gastric infusion of SCFAs on CAT in the liver, jejunum, ileum, colon, and cecum, respectively. (F–J): Representative charts of the effects of gastric infusion of SCFAs on SOD in the liver, jejunum, ileum, colon, and cecum, respectively. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; CAT, catalase; SOD, superoxide dismutase.

Figure 3

The effects of gastric infusion of SCFAs on GSH-Px and GSH activities in the liver and intestine of goats. (A–E): Representative charts of the effects of gastric infusion of SCFAs on GSH-Px in the liver, jejunum, ileum, colon, and cecum, respectively. (F–J): Representative charts of the effects of gastric infusion of SCFAs on GSH in the liver, jejunum, ileum, colon, and cecum, respectively. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; GSH-Px, glutathione peroxidase; GSH, glutathione.

Figure 4

The effects of gastric infusion of SCFAs on MDA activities in the liver (A) and intestine (jejunum (B), ileum (C), colon (D), and cecum (E)) of goats. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; MDA, maleic dialdehyde.

Figure 5

Effect of gastric infusion of SCFAs on cytokine concentration (IL-1β (A), IL-6 (B), IL-10 (C), and TNF-α (D)) in the liver of goats. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; IL-1β, interleukin-1 beta; IL-6, interleukin-6; IL-10, interleukin-10; TNF-α, tumor necrosis factor alpha.

Figure 6

Effect of gastric infusion of SCFAs on cytokine concentration in the jejunum (A), ileum (B), colon (C), and cecum (D) of goats. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate; IL-1β, interleukin-1 beta; IL-6, interleukin-6; IL-10, interleukin-10; TNF-α, tumor necrosis factor alpha.

Figure 7

Effect of gastric infusion of SCFAs on the intestinal tight-junction proteins in the jejunum (A), ileum (B), cecum (C), and colon (D) of goats. Different letters above bars represent different groups that showed significant differences (p < 0.05); values are presented as the mean ± SE. Note: NC, control group; SA, sodium acetate; sodium propionate; sodium butyrate.

Figure 8

Relationship among intestinal antioxidant, inflammatory cytokine, and tight-junction protein indexes in the liver (A), jejunum (B), ileum (C), colon (D), and cecum (E). Note: IL-1β, interleukin-1 beta; IL-6, interleukin-6; IL-10, interleukin-10; TNF-α, tumor necrosis factor alpha; ZO-1, zonula occludens-1; T-AOC, total antioxidant capacity; CAT, catalase; SOD, superoxide dismutase; GSH-Px, glutathione peroxidase; GSH, glutathione; MDA, maleic dialdehyde.