Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota

Abstract Background Subclinical necrotic enteritis (SNE), a common intestinal disease of broiler caused by Clostridium perfringens, could reduce production performance of broilers by chronic intestinal damage and poor absorption of nutrients. Ellagic acid (EA) has been reported to present antioxidan...

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Main Authors: Yu Tang, Xinyue Zhang, Yanan Wang, Yongpeng Guo, Peiqi Zhu, Guiguan Li, Jianyun Zhang, Qiugang Ma, Lihong Zhao
Format: Article
Language:English
Published: BMC 2022-04-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:https://doi.org/10.1186/s40104-022-00694-3
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author Yu Tang
Xinyue Zhang
Yanan Wang
Yongpeng Guo
Peiqi Zhu
Guiguan Li
Jianyun Zhang
Qiugang Ma
Lihong Zhao
author_facet Yu Tang
Xinyue Zhang
Yanan Wang
Yongpeng Guo
Peiqi Zhu
Guiguan Li
Jianyun Zhang
Qiugang Ma
Lihong Zhao
author_sort Yu Tang
collection DOAJ
description Abstract Background Subclinical necrotic enteritis (SNE), a common intestinal disease of broiler caused by Clostridium perfringens, could reduce production performance of broilers by chronic intestinal damage and poor absorption of nutrients. Ellagic acid (EA) has been reported to present antioxidant and anti-inflammatory properties on human and animals in many aspects. This study was conducted to evaluate the effect and mechanism of EA in relieving SNE in broilers induced by C. perfringens. Results C. perfringens challenge decreased body weight (BW), average daily gain (ADG), jejunal villi height/crypt depth (V/C) ratio, the activity of catalase (CAT) and the mRNA expression of zonula occludens 1 (ZO-1) in jejunal mucosa of broilers. While feed conversion ratios (FCR), jejunal crypt depth (CD), the activities of myeloperoxidase (MPO) and diamine oxidase (DAO), as well as the concentrations of interleukin 6 (IL-6), C-reactive protein (CRP) and procalcitonin (PCT) in serum, the activities of inducible nitric oxide synthase (iNOS) and lysozyme (LZM), the concentration of malondialdehyde (MDA), and the mRNA expressions of claudin-2, TNF-α, IL-1β, TLR-4, TLR-2, NF-κB, JAK3, STAT6 and iNOS in jejunal mucosa of broilers were increased by C. perfringens challenge. Dietary EA supplement relieved these adverse effects, and heightened jejunal villi height (VH), the concentration of D-xylose in plasma, activity of superoxide dismutase (SOD), and the mRNA expression of occludin in jejunal mucosa of broilers. The alpha diversity of cecal microbiota indicated that dietary EA supplement increased observed species and Shannon index. C. perfringens challenge increased the relative abundance of Firmicutes and decreased the relative abundance of Desulfobacterota in cecal microbiota. EA increased the relative abundance of Firmicutes in cecal microbiota. LEfSe analysis showed that C. perfringens challenge triggered the imbalance of cecal microbiota in broilers, dietary EA supplementation led to a small beneficial effect on microbiota, while the simultaneous effect of them seemed to stimulate the immune function of broilers by improving the microbiota balance. Conclusions Dietary EA ameliorated C. perfringens-induced SNE in broilers via regulating jejunal inflammation signaling pathways TLR/NF-κB and JAK3/STAT6, relieving jejunal oxidative stress and balancing cecal microbiota to inhibit intestinal barrier damage, prevent systemic inflammatory response and improve nutrient absorption capacity, finally protect and enhance growth performance of broilers.
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spelling doaj.art-a04ec887b03f426e9482950b7557fbdd2022-12-22T00:08:05ZengBMCJournal of Animal Science and Biotechnology2049-18912022-04-0113111810.1186/s40104-022-00694-3Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiotaYu Tang0Xinyue Zhang1Yanan Wang2Yongpeng Guo3Peiqi Zhu4Guiguan Li5Jianyun Zhang6Qiugang Ma7Lihong Zhao8State Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityJiangsu Lihua animal husbandry Co.COFCO feed Co., LtdState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, Poultry Nutrition and Feed Technology Innovation Team, College of Animal Science and Technology, China Agricultural UniversityAbstract Background Subclinical necrotic enteritis (SNE), a common intestinal disease of broiler caused by Clostridium perfringens, could reduce production performance of broilers by chronic intestinal damage and poor absorption of nutrients. Ellagic acid (EA) has been reported to present antioxidant and anti-inflammatory properties on human and animals in many aspects. This study was conducted to evaluate the effect and mechanism of EA in relieving SNE in broilers induced by C. perfringens. Results C. perfringens challenge decreased body weight (BW), average daily gain (ADG), jejunal villi height/crypt depth (V/C) ratio, the activity of catalase (CAT) and the mRNA expression of zonula occludens 1 (ZO-1) in jejunal mucosa of broilers. While feed conversion ratios (FCR), jejunal crypt depth (CD), the activities of myeloperoxidase (MPO) and diamine oxidase (DAO), as well as the concentrations of interleukin 6 (IL-6), C-reactive protein (CRP) and procalcitonin (PCT) in serum, the activities of inducible nitric oxide synthase (iNOS) and lysozyme (LZM), the concentration of malondialdehyde (MDA), and the mRNA expressions of claudin-2, TNF-α, IL-1β, TLR-4, TLR-2, NF-κB, JAK3, STAT6 and iNOS in jejunal mucosa of broilers were increased by C. perfringens challenge. Dietary EA supplement relieved these adverse effects, and heightened jejunal villi height (VH), the concentration of D-xylose in plasma, activity of superoxide dismutase (SOD), and the mRNA expression of occludin in jejunal mucosa of broilers. The alpha diversity of cecal microbiota indicated that dietary EA supplement increased observed species and Shannon index. C. perfringens challenge increased the relative abundance of Firmicutes and decreased the relative abundance of Desulfobacterota in cecal microbiota. EA increased the relative abundance of Firmicutes in cecal microbiota. LEfSe analysis showed that C. perfringens challenge triggered the imbalance of cecal microbiota in broilers, dietary EA supplementation led to a small beneficial effect on microbiota, while the simultaneous effect of them seemed to stimulate the immune function of broilers by improving the microbiota balance. Conclusions Dietary EA ameliorated C. perfringens-induced SNE in broilers via regulating jejunal inflammation signaling pathways TLR/NF-κB and JAK3/STAT6, relieving jejunal oxidative stress and balancing cecal microbiota to inhibit intestinal barrier damage, prevent systemic inflammatory response and improve nutrient absorption capacity, finally protect and enhance growth performance of broilers.https://doi.org/10.1186/s40104-022-00694-3BroilerClostridium perfringensEllagic acidIntestinal microbiotaSubclinical necrotic enteritis
spellingShingle Yu Tang
Xinyue Zhang
Yanan Wang
Yongpeng Guo
Peiqi Zhu
Guiguan Li
Jianyun Zhang
Qiugang Ma
Lihong Zhao
Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
Journal of Animal Science and Biotechnology
Broiler
Clostridium perfringens
Ellagic acid
Intestinal microbiota
Subclinical necrotic enteritis
title Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
title_full Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
title_fullStr Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
title_full_unstemmed Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
title_short Dietary ellagic acid ameliorated Clostridium perfringens-induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
title_sort dietary ellagic acid ameliorated clostridium perfringens induced subclinical necrotic enteritis in broilers via regulating inflammation and cecal microbiota
topic Broiler
Clostridium perfringens
Ellagic acid
Intestinal microbiota
Subclinical necrotic enteritis
url https://doi.org/10.1186/s40104-022-00694-3
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