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Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers

BACKGROUND: High stocking density (HSD) stress has detrimental effects on growth performance, intestinal barrier function, and intestinal microbiota in intensive animal production. Organic acids (OA) are widely used as feed additives for their ability to improve growth performance and intestinal hea...

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Autores principales: Dai, Dong, Qi, Guanghai, Wang, Jing, Zhang, Haijun, Qiu, Kai, Han, Yanming, Wu, Yuanyuan, Wu, Shugeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9661804/
https://www.ncbi.nlm.nih.gov/pubmed/36372893
http://dx.doi.org/10.1186/s40104-022-00776-2
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author Dai, Dong
Qi, Guanghai
Wang, Jing
Zhang, Haijun
Qiu, Kai
Han, Yanming
Wu, Yuanyuan
Wu, Shugeng
author_facet Dai, Dong
Qi, Guanghai
Wang, Jing
Zhang, Haijun
Qiu, Kai
Han, Yanming
Wu, Yuanyuan
Wu, Shugeng
author_sort Dai, Dong
collection PubMed
description BACKGROUND: High stocking density (HSD) stress has detrimental effects on growth performance, intestinal barrier function, and intestinal microbiota in intensive animal production. Organic acids (OA) are widely used as feed additives for their ability to improve growth performance and intestinal health in poultry. However, whether dietary OA can ameliorate HSD stress-induced impaired intestinal barrier in broilers remains elusive. In this study, a total of 528 one-day-old male Arbor Acres broilers were randomly allocated into 3 treatments with 12 replicates per treatment including 10 birds for normal stocking density and 17 birds for HSD. The dietary treatments were as follows: 1) Normal stocking density + basal diet; 2) HSD + basal diets; 3) HSD + OA. RESULTS: HSD stress can induce increased levels of serum corticosterone, lipopolysaccharides, interleukin-1β, tumor necrosis factor-α, and down-regulated mRNA expression of ZO-1, resulting in compromised growth performance of broilers (P < 0.05). Dietary OA could significantly reduce levels of serum corticosterone, lipopolysaccharides, interleukin-1β, and tumor necrosis factor-α, which were accompanied by up-regulated interleukin-10, mRNA expression of ZO-1, and growth performance (P < 0.05). Moreover, OA could down-regulate the mRNA expression of TLR4 and MyD88 to inhibit the NF-κB signaling pathway (P < 0.05). Additionally, HSD stress significantly decreased the abundance of Bacteroidetes and disturbed the balance of microbial ecosystems, whereas OA significantly increased the abundance of Bacteroidetes and restored the disordered gut microbiota by reducing competitive and exploitative interactions in microbial communities (P < 0.05). Meanwhile, OA significantly increased the content of acetic and butyric acids, which showed significant correlations with intestinal inflammation indicators (P < 0.05). CONCLUSIONS: Dietary OA ameliorated intestinal inflammation and growth performance of broilers through restoring the disordered gut microbial compositions and interactions induced by HSD and elevating short-chain fatty acid production to inhibit the TLR4/NF-κB signaling pathway. These findings demonstrated the critical role of intestinal microbiota in mediating the HSD-induced inflammatory responses, contributing to exploring nutritional strategies to alleviate HSD-induced stress in animals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00776-2.
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spelling pubmed-96618042022-11-15 Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers Dai, Dong Qi, Guanghai Wang, Jing Zhang, Haijun Qiu, Kai Han, Yanming Wu, Yuanyuan Wu, Shugeng J Anim Sci Biotechnol Research BACKGROUND: High stocking density (HSD) stress has detrimental effects on growth performance, intestinal barrier function, and intestinal microbiota in intensive animal production. Organic acids (OA) are widely used as feed additives for their ability to improve growth performance and intestinal health in poultry. However, whether dietary OA can ameliorate HSD stress-induced impaired intestinal barrier in broilers remains elusive. In this study, a total of 528 one-day-old male Arbor Acres broilers were randomly allocated into 3 treatments with 12 replicates per treatment including 10 birds for normal stocking density and 17 birds for HSD. The dietary treatments were as follows: 1) Normal stocking density + basal diet; 2) HSD + basal diets; 3) HSD + OA. RESULTS: HSD stress can induce increased levels of serum corticosterone, lipopolysaccharides, interleukin-1β, tumor necrosis factor-α, and down-regulated mRNA expression of ZO-1, resulting in compromised growth performance of broilers (P < 0.05). Dietary OA could significantly reduce levels of serum corticosterone, lipopolysaccharides, interleukin-1β, and tumor necrosis factor-α, which were accompanied by up-regulated interleukin-10, mRNA expression of ZO-1, and growth performance (P < 0.05). Moreover, OA could down-regulate the mRNA expression of TLR4 and MyD88 to inhibit the NF-κB signaling pathway (P < 0.05). Additionally, HSD stress significantly decreased the abundance of Bacteroidetes and disturbed the balance of microbial ecosystems, whereas OA significantly increased the abundance of Bacteroidetes and restored the disordered gut microbiota by reducing competitive and exploitative interactions in microbial communities (P < 0.05). Meanwhile, OA significantly increased the content of acetic and butyric acids, which showed significant correlations with intestinal inflammation indicators (P < 0.05). CONCLUSIONS: Dietary OA ameliorated intestinal inflammation and growth performance of broilers through restoring the disordered gut microbial compositions and interactions induced by HSD and elevating short-chain fatty acid production to inhibit the TLR4/NF-κB signaling pathway. These findings demonstrated the critical role of intestinal microbiota in mediating the HSD-induced inflammatory responses, contributing to exploring nutritional strategies to alleviate HSD-induced stress in animals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-022-00776-2. BioMed Central 2022-11-14 /pmc/articles/PMC9661804/ /pubmed/36372893 http://dx.doi.org/10.1186/s40104-022-00776-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Dai, Dong
Qi, Guanghai
Wang, Jing
Zhang, Haijun
Qiu, Kai
Han, Yanming
Wu, Yuanyuan
Wu, Shugeng
Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title_full Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title_fullStr Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title_full_unstemmed Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title_short Dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
title_sort dietary organic acids ameliorate high stocking density stress-induced intestinal inflammation through the restoration of intestinal microbiota in broilers
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9661804/
https://www.ncbi.nlm.nih.gov/pubmed/36372893
http://dx.doi.org/10.1186/s40104-022-00776-2
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