Rice bran oil supplementation protects swine weanlings against diarrhea and lipopolysaccharide challenge

Abstract

Early weaned piglets suffer from oxidative stress and enteral infection, which usually results in gut microbial dysbiosis, serve diarrhea, and even death. Rice bran oil (RBO), a polyphenol-enriched by-product of rice processing, has been shown to have antioxidant and anti-inflammatory properties both in vivo and in vitro. Here, we ascertained the proper RBO supplementation level, and subsequently determined its effects on lipopolysaccharide (LPS)-induced intestinal dysfunction in weaned piglets. A total of 168 piglets were randomly allocated into four groups of seven replicates (42 piglets each group, (21±1) d of age, body weight (7.60±0.04) kg, and half males and half females) and were given basal diet (Ctrl) or basal diet supplemented with 0.01% (mass fraction) RBO (RBO1), 0.02% RBO (RBO2), or 0.03% RBO (RBO3) for 21 d. Then, seven piglets from the Ctrl and the RBO were treated with LPS (100 µg/kg body weight (BW)) as LPS group and RBO+LPS group, respectively. Meanwhile, seven piglets from the Ctrl were treated with the saline vehicle (Ctrl group). Four hours later, all treated piglets were sacrificed for taking samples of plasma, jejunum tissues, and feces. The results showed that 0.02% was the optimal dose of dietary RBO supplementation based on diarrhea, average daily gain, and average daily feed intake indices in early weaning piglets. Furthermore, RBO protected piglets against LPS-induced jejunal epithelium damage, which was indicated by the increases in villus height, villus height/crypt depth ratio, and Claudin-1 levels, as well as a decreased level of jejunal epithelium apoptosis. RBO also improved the antioxidant ability of LPS-challenged piglets, which was indicated by the elevated concentrations of catalase and superoxide dismutase, and increased total antioxidant capacity, as well as the decreased concentrations of diamine oxidase and malondialdehyde in plasma. Meanwhile, RBO improved the immune function of LPS-challenged weaned piglets, which was indicated by elevated immunoglobulin A (IgA), IgM, β-defensin-1, and lysozyme levels in the plasma. In addition, RBO supplementation improved the LPS challenge-induced dysbiosis of gut microbiota. Particularly, the indices of antioxidant capacity, intestinal damage, and immunity were significantly associated with the RBO-regulated gut microbiota. These findings suggested that 0.02% RBO is a suitable dose to protect against LPS-induced intestinal damage, oxidative stress, and jejunal microbiota dysbiosis in early weaned piglets.

摘要

早期断奶仔猪遭受氧化应激和肠道感染, 通常会导致肠道微生物失调、腹泻甚至死亡. 米糠油 (RBO) 是一种富含多酚的大米加工副产品, 在体内和体外都具有抗氧化和抗炎特性. 本研究中, 我们确定了早期断奶仔猪日粮中适当的RBO补充水平, 随后确定了它对脂多糖 (LPS) 诱导的断奶仔猪肠道功能障碍的影响. 将 168 头仔猪随机分 4 组, 每组 7 个重复 (42 头/组, (21±1) 日龄, 体重 (7.60±0.04) kg, 公母各半), 分别接受基础日粮 (Ctrl) 或补充基础日粮含 0.01% RBO (RBO1)、0.02% RBO (RBO2) 或 0.03% RBO(RBO3). 饲喂 21 天后, Ctrl 和 RBO 组的 7 头仔猪经 LPS (100 μg/kg BW) 处理 (分别为 LPS 组和 RBO+LPS 组). 同时将 Ctrl 组的 7 头仔猪用载体盐水处理作为对照 (Ctrl 组). 四小时后, 处死所有处理组仔猪并采集血浆、 空肠组织和粪便. 分别检测血浆中抗氧化和免疫指标, 评估空肠组织形态和屏障功能以及通过 16S rDNA 测序分析肠道微生物组成、 功能及多样性. 结果表明, 根据早期断奶仔猪的腹泻、 平均日增重和平均日采食量指标, 0.02% 是日粮中添加 RBO 的最佳剂量. 此外, RBO 可以缓解 LPS 诱导的仔猪空肠上皮损伤, 表现为绒毛高度、 绒毛高度/隐窝深度比和 Claudin-1 水平的增加, 以及空肠上皮细胞凋亡的改善. RBO 还提高了 LPS 应激仔猪的抗氧化能力, 表现为血浆中过氧化氢酶和超氧化物歧化酶浓度升高, 总抗氧化能力提升, 以及二胺氧化酶和丙二醛浓度降低. 同时, RBO 提高了 LPS 应激的断奶仔猪的免疫功能, 表现为血浆中 IgA、 IgM、 β-防御素-1 和溶菌酶升高. 此外, 补充 RBO 还改善了 LPS 应激引起的肠道菌群失调. 相关性分析结果发现, 仔猪抗氧化能力、 肠道损伤和免疫力指标分别与 RBO 调节的肠道微生物群显着相关. 综上所述, 0.02% RBO 是缓解 LPS 诱导的早期断奶仔猪肠道损伤、 氧化应激和空肠微生物群失调的适当剂量.