[en] Alginate oligosaccharides (AOSs), which are an attractive feed additive for animal production, exhibit pleiotropic bioactivities. In the present study, we investigated graded doses of AOS-mediated alterations in the physiological responses of piglets by determining the intestinal architecture, barrier function, and microbiota. A total of 144 weaned piglets were allocated into four dietary treatments in a completely random design, which included a control diet (CON) and three treated diets formulated with 250 mg/kg (AOS250), 500 mg/kg (AOS500), and 1000 mg/kg AOS (AOS1000), respectively. The trial was carried out for 28 days. Our results showed that AOS treatment reinforced the intestinal barrier function by increasing the ileal villus height, density, and fold, as well as the expression of tight junction proteins, especially at the dose of 500 mg/kg AOS. Meanwhile, supplementations with AOSs showed positive effects on enhancing antioxidant capacity and alleviating intestinal inflammation by elevating the levels of antioxidant enzymes and inhibiting excessive inflammatory cytokines. The DESeq2 analysis showed that AOS supplementation inhibited the growth of harmful bacteria Helicobacter and Escherichia_Shigella and enhanced the relative abundance of Faecalibacterium and Veillonella. Collectively, these findings suggested that AOSs have beneficial effects on growth performance, antioxidant capacity, and gut health in piglets.
Disciplines :
Agriculture & agronomy
Author, co-author :
Liu, Ming ; Université de Liège - ULiège > TERRA Research Centre ; Animal Science and Technology College, Beijing University of Agriculture, Beijing 102206, China ; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Deng, Xiong; Animal Science and Technology College, Beijing University of Agriculture, Beijing 102206, China
Zhao, Yong; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Everaert, Nadia ; Université de Liège - ULiège > Département GxABT > Animal Sciences (AS) ; Nutrition and Animal Microbiota Ecosystems Laboratory, Department of Biosystems, KU Leuven, 3001 Leuven, Belgium
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Xia, Bing ; Animal Science and Technology College, Beijing University of Agriculture, Beijing 102206, China
Schroyen, Martine ; Université de Liège - ULiège > TERRA Research Centre > Animal Sciences (AS)
Language :
English
Title :
Alginate Oligosaccharides Enhance Antioxidant Status and Intestinal Health by Modulating the Gut Microbiota in Weaned Piglets.
NSCF - National Natural Science Foundation of China
Funding text :
This research was funded by the National Natural Science Foundation of China (32302777), the Beijing University of Agriculture Science and Technology Innovation Sparkling Support Plan (Grant No. BUA-HHXD2023003), Young Elite Scientists Sponsorship Program by BAST (Grant No. BYESS2023194), Research and Innovation Ability Improvement Plan for Young Teachers of Beijing University of Agriculture (Grant No. QJKC-2022051), and Research and Technology Funding Project of Beijing University of Agriculture (Grant No. QNTJ-2023004).
Campbell J.M. Crenshaw J.D. Polo J. The biological stress of early weaned piglets J. Anim. Sci. Biotechnol. 2013 4 19 10.1186/2049-1891-4-19 23631414
Kalia V.C. Shim W.Y. Patel S.K.S. Gong C. Lee J.K. Recent developments in antimicrobial growth promoters in chicken health: Opportunities and challenges Sci. Total Environ. 2022 834 155300 10.1016/j.scitotenv.2022.155300 35447189
Paul S.S. Rama Rao S.V. Hegde N. Williams N.J. Chatterjee R.N. Raju M. Reddy G.N. Kumar V. Phani Kumar P.S. Mallick S. et al. Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes Front. Microbiol. 2022 13 905050 10.3389/fmicb.2022.905050 35783415
Wang F. Lu Y. Cao J. Dynamics impacts of oxytetracycline on growth performance, intestinal health and antibiotic residue of grouper in exposure and withdrawal treatment Ecotoxicol. Environ. Saf. 2022 247 114203 10.1016/j.ecoenv.2022.114203 36279634
Bi D. Yang X. Lu J. Xu X. Preparation and potential applications of alginate oligosaccharides Crit. Rev. Food Sci. Nutr. 2022 63 10130 10147 10.1080/10408398.2022.2067832 35471191
Khan B.M. Qiu H.-M. Xu S.-Y. Liu Y. Cheong K.-L. Physicochemical characterization and antioxidant activity of sulphated polysaccharides derived from Porphyra haitanensis Int. J. Biol. Macromol. 2020 145 1155 1161 10.1016/j.ijbiomac.2019.10.040 31730957
Lu S. Na K. Wei J. Zhang L. Guo X. Alginate oligosaccharides: The structure-function relationships and the directional preparation for application Carbohydr. Polym. 2022 284 119225 10.1016/j.carbpol.2022.119225 35287920
Liu M. Liu L. Zhang H.-f. Yi B. Everaert N. Alginate oligosaccharides preparation, biological activities and their application in livestock and poultry J. Integr. Agric. 2021 20 24 34 10.1016/S2095-3119(20)63195-1
Zhang Y. Qin S. Song Y. Yuan J. Hu S. Chen M. Li L. Alginate Oligosaccharide Alleviated Cisplatin-Induced Kidney Oxidative Stress via Lactobacillus Genus-FAHFAs-Nrf2 Axis in Mice Front. Immunol. 2022 13 857242 10.3389/fimmu.2022.857242
Tusi S.K. Khalaj L. Ashabi G. Kiaei M. Khodagholi F. Alginate oligosaccharide protects against endoplasmic reticulum- and mitochondrial-mediated apoptotic cell death and oxidative stress Biomaterials 2011 32 5438 5458 10.1016/j.biomaterials.2011.04.024 21543116
Zhao Y. Feng Y. Liu M. Chen L. Meng Q. Tang X. Wang S. Liu L. Li L. Shen W. et al. Single-cell RNA sequencing analysis reveals alginate oligosaccharides preventing chemotherapy-induced mucositis Mucosal Immunol. 2020 13 437 448 10.1038/s41385-019-0248-z
He N. Yang Y. Wang H. Liu N. Yang Z. Li S. Unsaturated alginate oligosaccharides (UAOS) protects against dextran sulfate sodium-induced colitis associated with regulation of gut microbiota J. Funct. Foods 2021 83 104536 10.1016/j.jff.2021.104536
Lu S. Na K. Wei J. Tao T. Zhang L. Fang Y. Li X. Guo X. Alginate oligosaccharide structures differentially affect DSS-induced colitis in mice by modulating gut microbiota Carbohydr. Polym. 2023 312 120806 10.1016/j.carbpol.2023.120806 37059538
Zhang C. Xiong B. Chen L. Ge W. Yin S. Feng Y. Sun Z. Sun Q. Zhao Y. Shen W. et al. Rescue of male fertility following faecal microbiota transplantation from alginate oligosaccharide-dosed mice Gut 2021 70 2213 2215 10.1136/gutjnl-2020-323593 33443023
Wan J. Zhang J. Chen D. Yu B. Mao X. Zheng P. Yu J. Huang Z. Luo J. Luo Y. et al. Alginate oligosaccharide alleviates enterotoxigenic Escherichia coli-induced intestinal mucosal disruption in weaned pigs Food Funct. 2018 9 6401 6413 10.1039/C8FO01551A 30457630
Wan J. Zhang J. Xu Q. Yin H. Chen D. Yu B. He J. Alginate oligosaccharide protects against enterotoxigenic Escherichia coli-induced porcine intestinal barrier injury Carbohydr. Polym. 2021 270 118316 10.1016/j.carbpol.2021.118316 34364589
Allen H.K. Trachsel J. Looft T. Casey T.A. Finding alternatives to antibiotics Ann. N. Y. Acad. Sci. 2014 1323 91 100 10.1111/nyas.12468
Zhang X. Yang H. Zheng J. Jiang N. Sun G. Bao X. Lin A. Liu H. Chitosan oligosaccharides attenuate loperamide-induced constipation through regulation of gut microbiota in mice Carbohydr. Polym. 2021 253 117218 10.1016/j.carbpol.2020.117218
Gao H. Sun F. Lin G. Guo Y. Zhao J. Molecular actions of different functional oligosaccharides on intestinal integrity, immune function and microbial community in weanling pigs Food Funct. 2022 13 12303 12315 10.1039/D2FO02243E
Wan J. Zhang J. Chen D. Yu B. He J. Effects of alginate oligosaccharide on the growth performance, antioxidant capacity and intestinal digestion-absorption function in weaned pigs Anim. Feed. Sci. Tech. 2017 234 118 127 10.1016/j.anifeedsci.2017.09.006
Duan Q. Chen D. Yu B. Huang Z. Luo Y. Zheng P. Mao X. Yu J. Luo J. Yan H. et al. Effect of sialyllactose on growth performance and intestinal epithelium functions in weaned pigs challenged by enterotoxigenic Escherichia coli J. Anim. Sci. Biotechnol. 2022 13 30 10.1186/s40104-022-00673-8 35236420
Chen Y. Xie Y. Zhong R. Han H. Liu L. Chen L. Zhang H. Beckers Y. Everaert N. Effects of graded levels of xylo-oligosaccharides on growth performance, serum parameters, intestinal morphology, and intestinal barrier function in weaned piglets J. Anim. Sci. 2021 99 skab183 10.1093/jas/skab183 34097723
Okrathok S. Sirisopapong M. Mermillod P. Khempaka S. Modified dietary fiber from cassava pulp affects the cecal microbial population, short-chain fatty acid, and ammonia production in broiler chickens Poult. Sci. 2023 102 102265 10.1016/j.psj.2022.102265
Frazer L.C. Good M. Intestinal epithelium in early life Mucosal Immunol. 2022 15 1181 1187 10.1038/s41385-022-00579-8
Montagne L. Boudry G. Favier C. Le Huerou-Luron I. Lalles J.P. Seve B. Main intestinal markers associated with the changes in gut architecture and function in piglets after weaning Br. J. Nutr. 2007 97 45 57 10.1017/S000711450720580X
Xia B. Zhong R. Meng Q. Wu W. Chen L. Zhao X. Zhang H. Multi-omics unravel the compromised mucosal barrier function linked to aberrant mucin O-glycans in a pig model Int. J. Biol. Macromol. 2022 207 952 964 10.1016/j.ijbiomac.2022.03.173
Hu C. Xiao K. Luan Z. Song J. Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs J. Anim. Sci. 2013 91 1094 1101 10.2527/jas.2012-5796 23230104
Zha A. Tu R. Qi M. Wang J. Tan B. Liao P. Wu C. Yin Y. Mannan oligosaccharides selenium ameliorates intestinal mucosal barrier, and regulate intestinal microbiota to prevent Enterotoxigenic Escherichia coli-induced diarrhea in weaned piglets Ecotoxicol. Environ. Saf. 2023 264 115448 10.1016/j.ecoenv.2023.115448
Wang Q. Wang F. Zhou Y. Li X. Xu S. Jin Q. Li W. Bacillus amyloliquefaciens SC06 Relieving Intestinal Inflammation by Modulating Intestinal Stem Cells Proliferation and Differentiation via AhR/STAT3 Pathway in LPS-Challenged Piglets J. Agric. Food Chem. 2024 72 6096 6109 10.1021/acs.jafc.3c05956
Wang X. Xiao K. Yu C. Wang L. Liang T. Zhu H. Xu X. Liu Y. Xylooligosaccharide attenuates lipopolysaccharide-induced intestinal injury in piglets via suppressing inflammation and modulating cecal microbial communities Anim. Nutr. Zhongguo Xu Mu Shou Yi Xue Hui 2021 7 609 620 10.1016/j.aninu.2020.11.008 34377847
Xie W. Song L. Wang X. Xu Y. Liu Z. Zhao D. Wang S. Fan X. Wang Z. Gao C. et al. A bovine lactoferricin-lactoferrampin-encoding Lactobacillus reuteri CO21 regulates the intestinal mucosal immunity and enhances the protection of piglets against enterotoxigenic Escherichia coli K88 challenge Gut Microbes 2021 13 1956281 10.1080/19490976.2021.1956281 34369287
Wan J. Zhang J. Chen D. Yu B. Mao X. Zheng P. Yu J. Luo J. He J. Alginate oligosaccharide-induced intestinal morphology, barrier function and epithelium apoptosis modifications have beneficial effects on the growth performance of weaned pigs J. Anim. Sci. Biotechnol. 2018 9 58 10.1186/s40104-018-0273-x 30128148
Zeisel M.B. Dhawan P. Baumert T.F. Tight junction proteins in gastrointestinal and liver disease Gut 2019 68 547 561 10.1136/gutjnl-2018-316906 30297438
Bao X. Wu J. Impact of food-derived bioactive peptides on gut function and health Food Res. Int. 2021 147 110485 10.1016/j.foodres.2021.110485 34399481
Zhao L. Luo L. Jia W. Xiao J. Huang G. Tian G. Li J. Xiao Y. Serum diamine oxidase as a hemorrhagic shock biomarker in a rabbit model PLoS ONE 2014 9 e102285 10.1371/journal.pone.0102285 25144315
Chen J. Song Z. Ji R. Liu Y. Zhao H. Liu L. Li F. Chlorogenic acid improves growth performance of weaned rabbits via modulating the intestinal epithelium functions and intestinal microbiota Front. Microbiol. 2022 13 1027101 10.3389/fmicb.2022.1027101 36419414
Fang J. Wang H. Zhou Y. Zhang H. Zhou H. Zhang X. Slimy partners: The mucus barrier and gut microbiome in ulcerative colitis Exp. Mol. Med. 2021 53 772 787 10.1038/s12276-021-00617-8 34002011
Gustafsson J.K. Johansson M.E.V. The role of goblet cells and mucus in intestinal homeostasis Nat. Rev. Gastroenterol. Hepatol. 2022 19 785 803 10.1038/s41575-022-00675-x
Paone P. Cani P.D. Mucus barrier, mucins and gut microbiota: The expected slimy partners? Gut 2020 69 2232 2243 10.1136/gutjnl-2020-322260
Xia B. Zhong R. Wu W. Luo C. Meng Q. Gao Q. Zhao Y. Chen L. Zhang S. Zhao X. et al. Mucin O-glycan-microbiota axis orchestrates gut homeostasis in a diarrheal pig model Microbiome 2022 10 139 10.1186/s40168-022-01326-8 36045454
Wu A. Gao Y. Kan R. Ren P. Xue C. Kong B. Tang Q. Alginate Oligosaccharides Prevent Dextran-Sulfate-Sodium-Induced Ulcerative Colitis via Enhancing Intestinal Barrier Function and Modulating Gut Microbiota Foods 2023 12 220 10.3390/foods12010220 36613442
Lee A. Mansbridge S.C. Liang L. Connerton I.F. Mellits K.H. Galacto-Oligosaccharides Increase the Abundance of Beneficial Probiotic Bacteria and Improve Gut Architecture and Goblet Cell Expression in Poorly Performing Piglets, but Not Performance Animals 2023 13 230 10.3390/ani13020230 36670770
Xie Z. Zeng Z. Chen G. Dong W. Peng Y. Xu W. Sun Y. Zeng X. Liu Z. Intracellular Polysaccharides of Aspergillus cristatus from Fuzhuan Brick Tea Leverage the Gut Microbiota and Repair the Intestinal Barrier to Ameliorate DSS-Induced Colitis in Mice J. Agric. Food Chem. 2023 71 8023 8037 10.1021/acs.jafc.3c00611 37203140
Schreurs R. Baumdick M.E. Sagebiel A.F. Kaufmann M. Mokry M. Klarenbeek P.L. Schaltenberg N. Steinert F.L. van Rijn J.M. Drewniak A. et al. Human Fetal TNF-α-Cytokine-Producing CD4(+) Effector Memory T Cells Promote Intestinal Development and Mediate Inflammation Early in Life Immunity 2019 50 462 476.e8 10.1016/j.immuni.2018.12.010 30770246
Bergstrom K. Liu X. Zhao Y. Gao N. Wu Q. Song K. Cui Y. Li Y. McDaniel J.M. McGee S. et al. Defective Intestinal Mucin-Type O-Glycosylation Causes Spontaneous Colitis-Associated Cancer in Mice Gastroenterology 2016 151 152 164.e11 10.1053/j.gastro.2016.03.039 27059389
Wang X. He Q. Zhou C. Xu Y. Liu D. Fujiwara N. Kubota N. Click A. Henderson P. Vancil J. et al. Prolonged hypernutrition impairs TREM2-dependent efferocytosis to license chronic liver inflammation and NASH development Immunity 2022 56 58 77.e11 10.1016/j.immuni.2022.11.013 36521495
Li T. Huang S. Wang J. Yin P. Liu H. Sun C. Alginate oligosaccharides protect against fumonisin B1-induced intestinal damage via promoting gut microbiota homeostasis Food Res. Int. 2022 152 110927 10.1016/j.foodres.2021.110927
Luissint A.C. Parkos C.A. Nusrat A. Inflammation and the Intestinal Barrier: Leukocyte-Epithelial Cell Interactions, Cell Junction Remodeling, and Mucosal Repair Gastroenterology 2016 151 616 632 10.1053/j.gastro.2016.07.008
Cui C. Wu C. Wang J. Ma Z. Zheng X. Zhu P. Wang N. Zhu Y. Guan W. Chen F. Restored intestinal integrity, nutrients transporters, energy metabolism, antioxidative capacity and decreased harmful microbiota were associated with IUGR piglet’s catch-up growth before weanling J. Anim. Sci. Biotechnol. 2022 13 129 10.1186/s40104-022-00770-8
Su W. Jiang Z. Wang C. Zhang Y. Gong T. Wang F. Jin M. Wang Y. Lu Z. Co-fermented defatted rice bran alters gut microbiota and improves growth performance, antioxidant capacity, immune status and intestinal permeability of finishing pigs Anim. Nutr. Zhongguo Xu Mu Shou Yi Xue Hui 2022 11 413 424 10.1016/j.aninu.2022.07.008 36382202
Amorim R. Simões I.C.M. Teixeira J. Cagide F. Potes Y. Soares P. Carvalho A. Tavares L.C. Benfeito S. Pereira S.P. et al. Mitochondria-targeted anti-oxidant AntiOxCIN(4) improved liver steatosis in Western diet-fed mice by preventing lipid accumulation due to upregulation of fatty acid oxidation, quality control mechanism and antioxidant defense systems Redox Biol. 2022 55 102400 10.1016/j.redox.2022.102400
Zhu L.H. Zhao K.L. Chen X.L. Xu J.X. Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs J. Anim. Sci. 2012 90 2581 2589 10.2527/jas.2011-4444
Xia Y. Luo Q. Huang C. Shi L. Jahangir A. Pan T. Wei X. He J. Liu W. Shi R. et al. Ferric citrate-induced colonic mucosal damage associated with oxidative stress, inflammation responses, apoptosis, and the changes of gut microbial composition Ecotoxicol. Environ. Saf. 2022 249 114364 10.1016/j.ecoenv.2022.114364 36508806
Fang J. Yin H. Yang Z. Tan M. Wang F. Chen K. Zuo Z. Shu G. Cui H. Ouyang P. et al. Vitamin E protects against cadmium-induced sub-chronic liver injury associated with the inhibition of oxidative stress and activation of Nrf2 pathway Ecotoxicol. Environ. Saf. 2021 208 111610 10.1016/j.ecoenv.2020.111610
Kirkman H.N. Gaetani G.F. Mammalian catalase: A venerable enzyme with new mysteries Trends Biochem. Sci. 2007 32 44 50 10.1016/j.tibs.2006.11.003 17158050
Ho E. Karimi Galougahi K. Liu C.-C. Bhindi R. Figtree G.A. Biological markers of oxidative stress: Applications to cardiovascular research and practice Redox Biol. 2013 1 483 491 10.1016/j.redox.2013.07.006
Duan Q. Yu B. Huang Z. Luo Y. Zheng P. Mao X. Yu J. Luo J. Yan H. He J. Protective effect of sialyllactose on the intestinal epithelium in weaned pigs upon enterotoxigenic Escherichia coli challenge Food Funct. 2022 13 11627 11637 10.1039/D2FO02066A
Tao W. Wang G. Pei X. Sun W. Wang M. Chitosan Oligosaccharide Attenuates Lipopolysaccharide-Induced Intestinal Barrier Dysfunction through Suppressing the Inflammatory Response and Oxidative Stress in Mice Antioxidants 2022 11 1384 10.3390/antiox11071384
Wang Q. Wang X.F. Xing T. Li J.L. Zhu X.D. Zhang L. Gao F. The combined impact of xylo-oligosaccharides and gamma-irradiated astragalus polysaccharides on the immune response, antioxidant capacity, and intestinal microbiota composition of broilers Poult. Sci. 2022 101 101996 10.1016/j.psj.2022.101996
Wan T. Wang Y. He K. Zhu S. Microbial sensing in the intestine Protein Cell 2023 14 824 860 10.1093/procel/pwad028 37191444
Ng K.M. Ferreyra J.A. Higginbottom S.K. Lynch J.B. Kashyap P.C. Gopinath S. Naidu N. Choudhury B. Weimer B.C. Monack D.M. et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens Nature 2013 502 96 99 10.1038/nature12503
Shin N.R. Whon T.W. Bae J.W. Proteobacteria: Microbial signature of dysbiosis in gut microbiota Trends Biotechnol. 2015 33 496 503 10.1016/j.tibtech.2015.06.011
Ralser A. Dietl A. Jarosch S. Engelsberger V. Wanisch A. Janssen K.P. Middelhoff M. Vieth M. Quante M. Haller D. et al. Helicobacter pylori promotes colorectal carcinogenesis by deregulating intestinal immunity and inducing a mucus-degrading microbiota signature Gut 2023 72 1258 1270 10.1136/gutjnl-2022-328075
He J. He Y. Pan D. Cao J. Sun Y. Zeng X. Associations of Gut Microbiota with Heat Stress-Induced Changes of Growth, Fat Deposition, Intestinal Morphology, and Antioxidant Capacity in Ducks Front. Microbiol. 2019 10 903 10.3389/fmicb.2019.00903 31105682
Liu B. Yu D. Ge C. Luo X. Du L. Zhang X. Hui C. Combined effects of microplastics and chlortetracycline on the intestinal barrier, gut microbiota, and antibiotic resistome of Muscovy ducks (Cairina moschata) Sci. Total Environ. 2023 887 164050 10.1016/j.scitotenv.2023.164050
Wang Y. Ren K. Tan J. Mao Y. Alginate oligosaccharide alleviates aging-related intestinal mucosal barrier dysfunction by blocking FGF1-mediated TLR4/NF-κB p65 pathway Phytomedicine 2023 116 154806 10.1016/j.phymed.2023.154806
Sokol H. Pigneur B. Watterlot L. Lakhdari O. Bermúdez-Humarán L.G. Gratadoux J.-J. Blugeon S. Bridonneau C. Furet J.-P. Corthier G. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients Proc. Natl. Acad. Sci. USA 2008 105 16731 16736 10.1073/pnas.0804812105 18936492
Gu Q. Xia C. Liu N. Chen Z. Zhou Q. Li P. Lactobacillus plantarum ZJ316 alleviates ulcerative colitis by inhibiting inflammation and regulating short-chain fatty acid levels and the gut microbiota in a mouse model Food Funct. 2023 14 3982 3993 10.1039/D2FO02567A
Koh A. De Vadder F. Kovatcheva-Datchary P. Bäckhed F. From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites Cell 2016 165 1332 1345 10.1016/j.cell.2016.05.041
Thursby E. Juge N. Introduction to the human gut microbiota Biochem. J. 2017 474 1823 1836 10.1042/BCJ20160510 28512250
Li Y. Zhang Y. Wei K. He J. Ding N. Hua J. Zhou T. Niu F. Zhou G. Shi T. et al. Review: Effect of gut microbiota and its metabolite SCFAs on radiation-induced intestinal injury Front. Cell Infect. Microbiol. 2021 11 577236 10.3389/fcimb.2021.577236 34307184
Ríos-Covián D. Ruas-Madiedo P. Margolles A. Gueimonde M. de Los Reyes-Gavilán C.G. Salazar N. Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health Front. Microbiol. 2016 7 185 10.3389/fmicb.2016.00185 26925050
Zhao J. Yao Y. Li D. Zhu W. Xiao H. Xie M. Xiong Y. Wu J. Ni Q. Zhang M. et al. Metagenome and metabolome insights into the energy compensation and exogenous toxin degradation of gut microbiota in high-altitude rhesus macaques (Macaca mulatta) npj Biofilms Microbiomes 2023 9 20 10.1038/s41522-023-00387-3 37081021
Zhang Y. Deng X. Liu T. Hu B. Yu B. Jiang L. Wu Z. Schroyen M. Liu M. Alginate oligosaccharides improve hepatic metabolic disturbance via regulating the gut microbiota Food Hydrocoll. 2024 153 109980 10.1016/j.foodhyd.2024.109980
ISO 9831:1998 Animal feeding stuffs, animal products, and faeces or urine –Determination of gross calorific value–Bomb calorimeter method. ISO 9831:1998(E) International Organization for Standardization Geneva, Switzerland 1998
GB/T6432 Determination of crude protein in feeds-Kjeldahl method (GB/T 6432-2018) State Administration for Market Regulation, Standardization Administration of the People’s Republic of China Beijing, China 2018
Xia B. Wu W. Zhang L. Wen X. Xie J. Zhang H. Gut microbiota mediates the effects of inulin on enhancing sulfomucin production and mucosal barrier function in a pig model Food Funct. 2021 12 10967 10982 10.1039/D1FO02582A
