Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig
Abstract Background A. muciniphila (AKK) has attracted extensive research interest as a potential next-generation probiotics, but its role in intestinal pathology is remains unclear. Herein, this study was conducted to investigate the effects of A. muciniphila DSM 22,959 on growth performance, intes...
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2025-01-01
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Online Access: | https://doi.org/10.1186/s42523-024-00375-8 |
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author | Kunhong Xie Weidong Cai Lingjie Li Bing Yu Yuheng Luo Zhiqing Huang Xiangbing Mao Jie Yu Ping Zheng Hui Yan Hua Li Jun He |
author_facet | Kunhong Xie Weidong Cai Lingjie Li Bing Yu Yuheng Luo Zhiqing Huang Xiangbing Mao Jie Yu Ping Zheng Hui Yan Hua Li Jun He |
author_sort | Kunhong Xie |
collection | DOAJ |
description | Abstract Background A. muciniphila (AKK) has attracted extensive research interest as a potential next-generation probiotics, but its role in intestinal pathology is remains unclear. Herein, this study was conducted to investigate the effects of A. muciniphila DSM 22,959 on growth performance, intestinal barrier function, microecology and inflammatory response of weaned piglets stimulated by dextran sulfate sodium salt (DSS). Method Twenty-four Duroc × Landrace × Yorkshire (DLY) weaned piglets used for a 2 × 2 factorial arrangement of treatments were divided into four groups with six piglets in each group. From 1 to 15 d, the CA and DA groups were orally fed with 1.0 × 1011 colony-forming units A. muciniphila per day, while the CON and DCON groups were received gastric infusion of anaerobic sterile saline per day. The pigs were orally challenged (DCON, DA) or not (CON, CA) with DSS from day 9 to the end of the experiment and slaughtered on day 16. Results Presence of A. muciniphila in DSS-challenged weaned pigs resulted in numerically increased diarrhea rate, blood neutrophilic granulocyte, serum C-reactive protein and immunoglobulin M levels, and numerically reduced final weight, average daily feed intake and average daily gain. The decrease in intestinal villus height, villous height: crypt depth ratio and digestibility was accompanied by lower expression of ZO1, ZO2, Claudin1, DMT1, CAT1, SGLT1 and PBD114 genes, as well as decreased enzyme activities of intestinal alkaline phosphatase, lactase, sucrase and maltase of piglets in DA group compared to piglets in DCON group. The abundance of Bifdobacterium, Lactobacillus, A. muciniphila, Ruminococcus gnavus was numerically higher in digesta of pigs in DA group than those in DCON group. The inflammatory responses of piglets were dramatically changed by the simultaneous presence of A. muciniphila and DSS: expression level of IL17A, IL17F, IL23, RORγt, Stat3 was elevated in DA pigs compared to the other pig groups. Conclusions Our result showed that the oral A. muciniphila aggravates DSS-induced health damage of weaned piglet, which may attribute to the deteriorating intestinal morphology, dysbiosis of microbiota and inflammatory response disorders. |
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spelling | doaj-art-cb53b554f0174bcc81e308afebba956b2025-01-19T12:40:14ZengBMCAnimal Microbiome2524-46712025-01-017111710.1186/s42523-024-00375-8Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pigKunhong Xie0Weidong Cai1Lingjie Li2Bing Yu3Yuheng Luo4Zhiqing Huang5Xiangbing Mao6Jie Yu7Ping Zheng8Hui Yan9Hua Li10Jun He11Institute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityInstitute of Animal Nutrition, Sichuan Agricultural UniversityAbstract Background A. muciniphila (AKK) has attracted extensive research interest as a potential next-generation probiotics, but its role in intestinal pathology is remains unclear. Herein, this study was conducted to investigate the effects of A. muciniphila DSM 22,959 on growth performance, intestinal barrier function, microecology and inflammatory response of weaned piglets stimulated by dextran sulfate sodium salt (DSS). Method Twenty-four Duroc × Landrace × Yorkshire (DLY) weaned piglets used for a 2 × 2 factorial arrangement of treatments were divided into four groups with six piglets in each group. From 1 to 15 d, the CA and DA groups were orally fed with 1.0 × 1011 colony-forming units A. muciniphila per day, while the CON and DCON groups were received gastric infusion of anaerobic sterile saline per day. The pigs were orally challenged (DCON, DA) or not (CON, CA) with DSS from day 9 to the end of the experiment and slaughtered on day 16. Results Presence of A. muciniphila in DSS-challenged weaned pigs resulted in numerically increased diarrhea rate, blood neutrophilic granulocyte, serum C-reactive protein and immunoglobulin M levels, and numerically reduced final weight, average daily feed intake and average daily gain. The decrease in intestinal villus height, villous height: crypt depth ratio and digestibility was accompanied by lower expression of ZO1, ZO2, Claudin1, DMT1, CAT1, SGLT1 and PBD114 genes, as well as decreased enzyme activities of intestinal alkaline phosphatase, lactase, sucrase and maltase of piglets in DA group compared to piglets in DCON group. The abundance of Bifdobacterium, Lactobacillus, A. muciniphila, Ruminococcus gnavus was numerically higher in digesta of pigs in DA group than those in DCON group. The inflammatory responses of piglets were dramatically changed by the simultaneous presence of A. muciniphila and DSS: expression level of IL17A, IL17F, IL23, RORγt, Stat3 was elevated in DA pigs compared to the other pig groups. Conclusions Our result showed that the oral A. muciniphila aggravates DSS-induced health damage of weaned piglet, which may attribute to the deteriorating intestinal morphology, dysbiosis of microbiota and inflammatory response disorders.https://doi.org/10.1186/s42523-024-00375-8A. muciniphilaWeaned pigsGrowth performanceIntestinal morphologyMicrobiotaInflammatory response |
spellingShingle | Kunhong Xie Weidong Cai Lingjie Li Bing Yu Yuheng Luo Zhiqing Huang Xiangbing Mao Jie Yu Ping Zheng Hui Yan Hua Li Jun He Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig Animal Microbiome A. muciniphila Weaned pigs Growth performance Intestinal morphology Microbiota Inflammatory response |
title | Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig |
title_full | Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig |
title_fullStr | Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig |
title_full_unstemmed | Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig |
title_short | Probiotic administration aggravates dextran sulfate sodium salt-induced inflammation and intestinal epithelium disruption in weaned pig |
title_sort | probiotic administration aggravates dextran sulfate sodium salt induced inflammation and intestinal epithelium disruption in weaned pig |
topic | A. muciniphila Weaned pigs Growth performance Intestinal morphology Microbiota Inflammatory response |
url | https://doi.org/10.1186/s42523-024-00375-8 |
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