Browse > Article
http://dx.doi.org/10.5713/ab.21.0562

Microbial short-chain fatty acids: a bridge between dietary fibers and poultry gut health - A review  

Ali, Qasim (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Ma, Sen (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
La, Shaokai (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Guo, Zhiguo (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Liu, Boshuai (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Gao, Zimin (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Farooq, Umar (Department of Poultry Science, University of Agriculture Faisalabad)
Wang, Zhichang (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Zhu, Xiaoyan (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Cui, Yalei (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Li, Defeng (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Shi, Yinghua (Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Henan Agricultural University)
Publication Information
Animal Bioscience / v.35, no.10, 2022 , pp. 1461-1478 More about this Journal
Abstract
The maintenance of poultry gut health is complex depending on the intricate balance among diet, the commensal microbiota, and the mucosa, including the gut epithelium and the superimposing mucus layer. Changes in microflora composition and abundance can confer beneficial or detrimental effects on fowl. Antibiotics have devastating impacts on altering the landscape of gut microbiota, which further leads to antibiotic resistance or spread the pathogenic populations. By eliciting the landscape of gut microbiota, strategies should be made to break down the regulatory signals of pathogenic bacteria. The optional strategy of conferring dietary fibers (DFs) can be used to counterbalance the gut microbiota. DFs are the non-starch carbohydrates indigestible by host endogenous enzymes but can be fermented by symbiotic microbiota to produce short-chain fatty acids (SCFAs). This is one of the primary modes through which the gut microbiota interacts and communicate with the host. The majority of SCFAs are produced in the large intestine (particularly in the caecum), where they are taken up by the enterocytes or transported through portal vein circulation into the bloodstream. Recent shreds of evidence have elucidated that SCFAs affect the gut and modulate the tissues and organs either by activating G-protein-coupled receptors or affecting epigenetic modifications in the genome through inducing histone acetylase activities and inhibiting histone deacetylases. Thus, in this way, SCFAs vastly influence poultry health by promoting energy regulation, mucosal integrity, immune homeostasis, and immune maturation. In this review article, we will focus on DFs, which directly interact with gut microbes and lead to the production of SCFAs. Further, we will discuss the current molecular mechanisms of how SCFAs are generated, transported, and modulated the pro-and anti-inflammatory immune responses against pathogens and host physiology and gut health.
Keywords
Dietary Fibers; G-protein-coupled Receptors; Gut Microbiota; Histone Deacetylases; Short-chain Fatty Acids;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Saqui-Salces M, Huang Z, Vila MF, et al. Modulation of intestinal cell differentiation in growing pigs is dependent on the fiber source in the diet. J Anim Sci 2017;95:1179-90. https://doi.org/10.2527/jas.2016.0947   DOI
2 McRorie Jr JW, McKeown NM. Understanding the physics of functional fibers in the gastrointestinal tract: an evidencebased approach to resolving enduring misconceptions about insoluble and soluble fiber. J Acad Nutr Diet 2017;117:25164. https://doi.org/10.1016/j.jand.2016.09.021   DOI
3 Wellington MO, Hamonic K, Krone JEC, Htoo JK, Van Kessel AG, Columbus DA. Effect of dietary fiber and threonine content on intestinal barrier function in pigs challenged with either systemic E. coli lipopolysaccharide or enteric Salmonella Typhimurium. J Anim Sci Biotechnol 2020;11:38. https://doi.org/10.1186/s40104-020-00444-3   DOI
4 Tang Q, Tan P, Ma N, Ma X. Physiological functions of threonine in animals: beyond nutrition metabolism. Nutrients 2021;13:2592. https://doi.org/10.3390/nu13082592   DOI
5 Nursiam I, Ridla M, Hermana W, Nahrowi. Effect of fiber source on growth performance and gastrointestinal tract in broiler chickens. In: IOP Conference Series. Earth Environ Sci 2021;788:012058. https://doi.org/10.1088/1755-1315/788/1/012058   DOI
6 Chiou PW, Lu T, Hsu J, Yu B. Effect of different sources of fiber on the intestinal morphology of domestic geese. AsianAustralas J Anim Sci 1996;9:539-50. https://doi.org/10.5713/ajas.1996.539   DOI
7 Rehman H, Vahjen W, Kohl-Parisini A, Ijaz A, Zentek J. Influence of fermentable carbohydrates on the intestinal bacteria and enteropathogens in broilers. World's Poult Sci J 2009;65:75-90. https://doi.org/10.1017/S0043933909000063   DOI
8 Tetteh PW, Basak O, Farin HF, et al. Replacement of lost Lgr5-positive stem cells through plasticity of their enterocyte-lineage daughters. Cell Stem Cell 2016;18:203-13. https://doi.org/10.1016/j.stem.2016.01.001   DOI
9 Hansson GC, Johansson MEV. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes 2010;1:51-4. https://doi.org/10.4161/gmic.1.1.10470   DOI
10 Barker N, Van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-7. https://doi.org/10.1038/nature06196   DOI
11 Giepmans BNG, van IJzendoorn SCD. Epithelial cell-cell junctions and plasma membrane domains. Biochim Biophy Acta (BBA)-Biomembranes 2009;1788:820-31. https://doi.org/10.1016/j.bbamem.2008.07.015   DOI
12 Hossain Z, Hirata T. Molecular mechanism of intestinal permeability: interaction at tight junctions. Mol Biosyst 2008;4: 1181-5. https://doi.org/10.1039/b800402a   DOI
13 Cani PD, Possemiers S, Van de Wiele T, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009;58:1091-103. https://doi.org/10.1136/gut.2008.165886   DOI
14 Khurana S, George SP. Regulation of cell structure and function by actin-binding proteins: villin's perspective. FEBS Lett 2008;582:2128-39. https://doi.org/10.1016/j.febslet.2008.02.040   DOI
15 Mazzolini R, Dopeso H, Mateo-Lozano S, Arango D. Brush border myosin Ia has tumor suppressor activity in the intestine. Proc Natl Acad Sci USA 2012;109:1530-5. https://doi.org/10.1073/pnas.1108411109   DOI
16 Ben-Shahar Y, Abassi Z, Shefer HK, Pollak Y, Bhattacharya U, Sukhotnik I. Accelerated intestinal epithelial cell turnover correlates with stimulated bmp signaling cascade following intestinal ischemia-reperfusion in a rat. Eur J Pediatr Surg 2020;30:64-70. https://doi.org/10.1055/s-0039-1700550   DOI
17 Yamabhai M, Sak-Ubol S, Srila W, Haltrich D. Mannan biotechnology: from biofuels to health. Crit Rev Biotechnol 2016;36:32-42. https://doi.org/10.3109/07388551.2014.923372   DOI
18 De la Fuente G, Yanez-Ruiz DR, Seradj A, Balcells J, Belanche A. Methanogenesis in animals with foregut and hindgut fermentation: a review. Anim Prod Sci 2019;59:2109-22. https://doi.org/10.1071/AN17701   DOI
19 Schroeder BO, Birchenough GM, Stahlman M, et al. Bifidobacteria or fiber protects against diet-induced microbiotamediated colonic mucus deterioration. Cell Host Microb 2018;23:27-40. https://doi.org/10.1016/j.chom.2017.11.004   DOI
20 Yin L, Yang H, Li J, et al. Pig models on intestinal development and therapeutics. Amino Acids 2017;49:2099-106. https://doi.org/10.1007/s00726-017-2497-z   DOI
21 Rodriguez-Boulan E, Macara IG. Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 2014;15:225-42. https://doi.org/10.1038/nrm3775   DOI
22 Dhekne HS, Pylypenko O, Overeem AW, et al. MYO5B, STX3, and STXBP2 mutations reveal a common disease mechanism that unifies a subset of congenital diarrheal disorders: a mutation update. Hum Mutat 2018;39:333-44. https://doi.org/10.1002/humu.23386   DOI
23 McConnell RE, Higginbotham JN, Shifrin DA, et al. The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 2009;185:1285-98. https://doi.org/10.1083/jcb.200902147   DOI
24 McConnell RE, Tyska MJ. Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J Cell Biol 2007;177:671-81. https://doi.org/10.1083/jcb.200701144   DOI
25 Shifrin DA, Jr, Tyska MJ. Ready...aim...fire into the lumen: a new role for enterocyte microvilli in gut host defense. Gut Microbes 2012;3:460-2. https://doi.org/10.4161/gmic.21247   DOI
26 Weerasooriya V, Rennie MJ, Anant S, Alpers DH, Patterson BW, Klein S. Dietary fiber decreases colonic epithelial cell proliferation and protein synthetic rates in human subjects. Am J physiol Endocrinol Metab 2006;290:E1104-8. https://doi.org/10.1152/ajpendo.00557.2005   DOI
27 Lavelle A, Sokol H. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 2020;17:223-37. https://doi.org/10.1038/s41575019-0258-z   DOI
28 Maki JJ, Bobeck EA, Sylte MJ, Looft T. Eggshell and environmental bacteria contribute to the intestinal microbiota of growing chickens. J Anim Sci Biotechnol 2020;11:60. https://doi.org/10.1186/s40104-020-00459-w   DOI
29 Meddings J. The significance of the gut barrier in disease. Gut 2008;57:438-40. https://doi.org/10.1136/gut.2007.143172   DOI
30 Kef S, Arslan S. The effects of different dietary fiber use on the properties of kefir produced with cow's and goat's milk. J Food Proc Preserv 2021;45:e15467. https://doi.org/10.1111/jfpp.15467   DOI
31 Brestoff JR, Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 2013; 14:676-84. https://doi.org/10.1038/ni.2640   DOI
32 Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Van Immerseel F. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr Res Rev 2010;23:366-84. https://doi.org/10.1017/s0954422410000247   DOI
33 Jozefiak D, Rutkowski A, Fratczak M, Boros D. The effect of dietary fibre fractions from different cereals and microbial enzyme supplementation on performance, ileal viscosity and short-chain fatty acid concentrations in the caeca of broiler chickens. J Anim Feed Sci 2004;13:487-96. https://doi.org/10.22358/jafs/67618/2004   DOI
34 Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 2004;447:61928. https://doi.org/10.1007/s00424-003-1067-2   DOI
35 van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Ann Rev Physiol 2009;71:241-60. https://doi.org/10.1146/annurev.physiol.010908.163145   DOI
36 Ragsdale SW, Pierce E. Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta Proteins Proteom 2008;1784:1873-98. https://doi.org/10.1016/j.bbapap.2008.08.012   DOI
37 Hadjiagapiou C, Schmidt L, Dudeja PK, Layden TJ, Ramaswamy K. Mechanism(s) of butyrate transport in Caco-2 cells: role of monocarboxylate transporter 1. Am J Physiol Gastrointest Liver Physiol 2000;279:G775-80. https://doi.org/10.1152/ajpgi.2000.279.4.G775   DOI
38 Jamroz D, Jakobsen K, Bach Knudsen KE, Wiliczkiewicz A, Orda J. Digestibility and energy value of non-starch polysaccharides in young chickens, ducks and geese, fed diets containing high amounts of barley. Comp Biochem Physiol A Mol Integr Physiol 2002;131:657-68. https://doi.org/10.1016/s10956433(01)00517-7   DOI
39 Miller TL, Wolin MJ. Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 1996;62:1589-92. https://doi.org/10.1128/aem.62.5.1589-1592.1996   DOI
40 Reichardt N, Duncan SH, Young P, et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 2014;8:1323-35. https:// doi.org/10.1038/ismej.2014.14   DOI
41 Vidyasagar S, Barmeyer C, Geibel J, Binder HJ, Rajendran VM. Role of short-chain fatty acids in colonic HCO3 secretion. Am J Physiol Gastrointest Liver Physiol 2005;288:G1217-26. https://doi.org/10.1152/ajpgi.00415.2004   DOI
42 Gracia MI, Sanchez J, Millan C, et al. Effect of feed form and whole grain feeding on gastrointestinal weight and the prevalence of campylobacter jejuni in broilers orally infected. PloS One 2016;11:e0160858. https://doi.org/10.1371/journal.pone.0160858   DOI
43 Brufau MT, Martin-Venegas R, Guerrero-Zamora AM, et al. Dietary β-galactomannans have beneficial effects on the intestinal morphology of chickens challenged with Salmonella enterica serovar Enteritidis. J Anim Sci 2015;93:238-46. https://doi.org/10.2527/jas.2014-7219   DOI
44 Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Advan Immunol 2014;121:91-119. https://doi.org/10.1016/b978-0-12-800100-4.00003-9   DOI
45 Walugembe M, Hsieh JC, Koszewski NJ, Lamont SJ, Persia ME, Rothschild MF. Effects of dietary fiber on cecal shortchain fatty acid and cecal microbiota of broiler and layinghen chicks. Poult Sci 2015;94:2351-9. https://doi.org/10.3382/ps/pev242   DOI
46 Kearney JM, McElhone S. Perceived barriers in trying to eat healthier-results of a pan-EU consumer attitudinal survey. Br J Nutr 1999;81:S133-S7. https://doi.org/10.1017/S0007114599000987   DOI
47 Liu H, Ivarsson E, Dicksved J, Lundh T, Lindberg JE. Inclusion of chicory (Cichorium intybus L.) in pigs' diets affects the intestinal microenvironment and the gut microbiota. Appl Environ Microbiol 2012;78:4102-9. https://doi.org/10.1128/AEM.07702-11   DOI
48 Trompette A, Gollwitzer ES, Yadava K, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014;20:159-66. https://doi.org/10.1038/nm.3444   DOI
49 Mahmood T, Guo Y. Dietary fiber and chicken microbiome interaction: Where will it lead to? Anim Nutr 2020;6:1-8. https://doi.org/10.1016/j.aninu.2019.11.004   DOI
50 Jozefiak D, Rutkowski A, Kaczmarek S, Jensen BB, Engberg RM, Hojberg O. Effect of β-glucanase and xylanase supplementation of barley-and rye-based diets on caecal microbiota of broiler chickens. Br Poult Sci 2010;51:546-57. https://doi.org/10.1080/00071668.2010.507243   DOI
51 Deehan EC, Duar RM, Armet AM, Perez-Munoz ME, Jin M, Walter J. Modulation of the gastrointestinal microbiome with nondigestible fermentable carbohydrates to improve human health. Microb Spect 2017;5:5.5.04. https://doi.org/10.1128/microbiolspec.BAD-0019-2017   DOI
52 Song J, Li Q, Everaert N, et al. Effects of inulin supplementation on intestinal barrier function and immunity in specific pathogen-free chickens with Salmonella infection. J Anim Sci 2020;98:skz396. https://doi.org/10.1093/jas/skz396   DOI
53 Qin S, Zhang K, Applegate TJ, et al. Dietary administration of resistant starch improved caecal barrier function by enhancing intestinal morphology and modulating microbiota composition in meat duck. Br J Nutr 2020;123:172-81. https://doi.org/10.1017/S0007114519002319   DOI
54 Ahallil H, Abdullah A, Maskat MY, Sarbini SR. Fermentation of gum arabic by gut microbiota using in vitro colon model. In: AIP Conference Proceedings. AIP Publishing LLC; 2019. p. 050004. https://doi.org/10.1063/1.5111252   DOI
55 Azcarate-Peril MA, Butz N, Cadenas MB, et al. An attenuated Salmonella enterica serovar Typhimurium strain and galactooligosaccharides accelerate clearance of Salmonella infections in poultry through modifications to the gut microbiome. Appl Environ Microbiol 2018;84:e02526-17. https://doi.org/10.1128/AEM.02526-17   DOI
56 Pourabedin M, Zhao X. Prebiotics and gut microbiota in chickens. FEMS Microbiol Lett 2015;362:fnv122. https://doi.org/10.1093/femsle/fnv122   DOI
57 Fu X, Li R, Zhang T, Li M, Mou H. Study on the ability of partially hydrolyzed guar gum to modulate the gut microbiota and relieve constipation. J Food Biochem 2019;43:e12715. https://doi.org/10.1111/jfbc.12715   DOI
58 Ganapathy V, Gopal E, Miyauchi S, Prasad PD. Biological functions of SLC5A8, a candidate tumour suppressor. Biochem Soc Trans 2005;33:237-40. https://doi.org/10.1042/bst0330237   DOI
59 Shin HJ, Anzai N, Enomoto A, et al. Novel liver-specific organic anion transporter OAT7 that operates the exchange of sulfate conjugates for short chain fatty acid butyrate. Hepatology 2007;45:1046-55. https://doi.org/10.1002/hep.21596   DOI
60 Sellin JH. SCFAs: The enigma of weak electrolyte transport in the colon. News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society 1999;14:58-64. https://doi.org/10.1152/physiologyonline.1999.14.2.58   DOI
61 Pluznick J. A novel SCFA receptor, the microbiota, and blood pressure regulation. Gut Microbes 2014;5:202-7. https://doi.org/10.4161/gmic.27492   DOI
62 Digby JE, Martinez F, Jefferson A, et al. Anti-inflammatory effects of nicotinic acid in human monocytes are mediated by GPR109A dependent mechanisms. Arterioscler Thromb Vasc Biol 2012;32:669-76. https://doi.org/10.1161/ATVBAHA.111.241836   DOI
63 Singh N, Thangaraju M, Prasad PD, et al. Blockade of dendritic cell development by bacterial fermentation products butyrate and propionate through a transporter (Slc5a8)-dependent inhibition of histone deacetylases. J Biol Chem 2010;285: 27601-8. https://doi.org/10.1074/jbc.M110.102947   DOI
64 M'Sadeq SA, Wu S, Swick RA, Choct M. Towards the control of necrotic enteritis in broiler chickens with in-feed antibiotics phasing-out worldwide. Anim Nutr 2015;1:1-11. https://doi.org/10.1016/j.aninu.2015.02.004   DOI
65 Vermeulen K, Verspreet J, Courtin CM, et al. Reduced-particlesize wheat bran is efficiently colonized by a lactic acid-producing community and reduces levels of Enterobacteriaceae in the cecal microbiota of broilers. Appl Environ Microbiol 2018;84:e01343-18. https://doi.org/10.1128/AEM.01343-18   DOI
66 Brown AJ, Goldsworthy SM, Barnes AA, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003;278:11312-9. https://doi.org/10.1074/jbc.M211609200   DOI
67 Takebe K, Nio J, Morimatsu M, et al. Histochemical demonstration of a Na+-coupled transporter for short-chain fatty acids (Slc5a8) in the intestine and kidney of the mouse. Biomed Res 2005;26:213-21. https://doi.org/10.2220/biomedres.26.213   DOI
68 Ohira H, Fujioka Y, Katagiri C, et al. Butyrate attenuates inflammation and lipolysis generated by the interaction of adipocytes and macrophages. J Atheroscler Thromb 2013;20: 425-42. https://doi.org/10.5551/jat.15065   DOI
69 Singh Y, Molan AL, Ravindran V. Influence of the method of whole wheat inclusion on performance and caecal microbiota profile of broiler chickens. J Appl Anim Nutr 2019;7:E4. https://doi.org/10.1017/jan.2019.3   DOI
70 Galan JE, Curtiss R, 3rd. Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 1990;58:1879-85. https://doi.org/10.1128/iai.58.6.1879-1885.1990   DOI
71 Huang W, Zhou L, Guo H, Xu Y, Xu Y. The role of short-chain fatty acids in kidney injury induced by gut-derived inflammatory response. Metabolism 2017;68:20-30. https://doi.org/10.1016/j.metabol.2016.11.006   DOI
72 Kim CH. Microbiota or short-chain fatty acids: which regulates diabetes? Cell Mol Immunol 2018;15:88-91. https://doi.org/10.1038/cmi.2017.57   DOI
73 Borthakur A, Priyamvada S, Kumar A, et al. A novel nutrient sensing mechanism underlies substrate-induced regulation of monocarboxylate transporter-1. Am J Physiol Gastrointest Liver Physiol 2012;303:G1126-G33. https://doi.org/10.1152/ajpgi.00308.2012   DOI
74 Aune D, Chan DS, Lau R, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and doseresponse meta-analysis of prospective studies. BMJ 2011; 343:d6617. https://doi.org/10.1136/bmj.d6617   DOI
75 Bailey JS, Blankenship LC, Cox NA. Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poult Sci 1991;70:2433-8. https://doi.org/10.3382/ps.0702433   DOI
76 Wu J, Zhou Z, Hu Y, Dong S. Butyrate-induced GPR41 activation inhibits histone acetylation and cell growth. J Genet Genomics 2012;39:375-84. https://doi.org/10.1016/j.jgg.2012.05.008   DOI
77 Smith PM, Howitt MR, Panikov N, Michaud M, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569-73. https://doi.org/10.1126/science.1241165   DOI
78 Halnes I, Baines KJ, Berthon BS, MacDonald-Wicks LK, Gibson PG, Wood LG. Soluble fibre meal challenge reduces airway inflammation and expression of GPR43 and GPR41 in asthma. Nutrients 2017;9:57. https://doi.org/10.3390/nu9010057   DOI
79 Halas D, Hansen CF, Hampson DJ, Mullan BP, Wilson RH, Pluske JR. Effect of dietary supplementation with inulin and/or benzoic acid on the incidence and severity of postweaning diarrhoea in weaner pigs after experimental challenge with enterotoxigenic Escherichia coli. Arch Anim Nutr 2009; 63:267-80. https://doi.org/10.1080/17450390903020414   DOI
80 Kim JC, Mullan BP, Hampson DJ, Pluske JR. Addition of oat hulls to an extruded rice-based diet for weaner pigs ameliorates the incidence of diarrhoea and reduces indices of protein fermentation in the gastrointestinal tract. Br J Nutr 2008;99:1217-25. https://doi.org/10.1017/S0007114507868462   DOI
81 Chen H, Mao X, He J, et al. Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets. Br J Nutr 2013;110:1837-48. https://doi.org/10.1017/s0007114513001293   DOI
82 Wan R, Camandola S, Mattson MP. Intermittent food deprivation improves cardiovascular and neuroendocrine responses to stress in rats. J Nutr 2003;133:1921-9. https://doi.org/10.1093/jn/133.6.1921   DOI
83 Kendrick SF, O'Boyle G, Mann J, et al. Acetate, the key modulator of inflammatory responses in acute alcoholic hepatitis. Hepatology 2010;51:1988-97. https://doi.org/10.1002/hep.23572   DOI
84 Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA 2014;111:2247-52. https://doi.org/10.1073/pnas.1322269111   DOI
85 Borrelli L, Coretti L, Dipineto L, et al. Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens. Sci Rep 2017;7:16269. https://doi.org/10.1038/s41598-017-16560-6   DOI
86 Denyer MP, Pinheiro DY, Garden OA, Shepherd AJ. Missed, not missing: phylogenomic evidence for the existence of avian FoxP3. PLoS One 2016;11:e0150988. https://doi.org/10.1371/journal.pone.0150988   DOI
87 De Maesschalck C, Eeckhaut V, Maertens L, et al. Amorphous cellulose feed supplement alters the broiler caecal microbiome. Poult Sci 2019;98:3811-7. https://doi.org/10.3382/ps/pez090   DOI
88 Tian D, Xu X, Peng Q, et al. In vitro fermentation of arabinoxylan from oat (Avena sativa L.) by Pekin duck intestinal microbiota. 3 Biotech 2019;9:54. https://doi.org/10.1007/s13205-019-1571-5   DOI
89 Mateos GG, Jimenez-Moreno E, Serrano MP, Lazaro RP. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. J Appl Poult Res 2012;21:156-74. https://doi.org/10.3382/japr.2011-00477   DOI
90 Lucas JL, Mirshahpanah P, Haas-Stapleton E, Asadullahb K, Zollnerb TM, Numerof RP. Induction of Foxp3+ regulatory T cells with histone deacetylase inhibitors. Cell Immunol 2009;257:97-104. https://doi.org/10.1016/j.cellimm.2009.03.004   DOI
91 Friedman M, Juneja VK. Review of antimicrobial and antioxidative activities of chitosans in food. J Food Prot 2010;73: 1737-61. https://doi.org/10.4315/0362-028X-73.9.1737   DOI
92 Schedle K, Plitzner C, Ettle T, Zhao L, Domig KJ, Windisch W. Effects of insoluble dietary fibre differing in lignin on performance, gut microbiology, and digestibility in weanling piglets. Arch Anim Nutr 2008;62:141-51. https://doi.org/10.1080/17450390801892617   DOI
93 Usami M, Kishimoto K, Ohata A, et al. Butyrate and trichostatin A attenuate nuclear factor kappaB activation and tumor necrosis factor alpha secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutr Res (New York, NY) 2008;28:321-8. https://doi.org/10.1016/j.nutres.2008.02.012   DOI
94 Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009;461:1282-6. https://doi.org/10.1038/nature08530   DOI
95 Hansen CF, Phillips ND, La T, et al. Diets containing inulin but not lupins help to prevent swine dysentery in experimentally challenged pigs. J Anim Sci 2010;88:3327-36. https://doi.org/10.2527/jas.2009-2719   DOI
96 Biasato I, Ferrocino I, Biasibetti E, et al. Modulation of intestinal microbiota, morphology and mucin composition by dietary insect meal inclusion in free-range chickens. BMC Vet Res 2018;14:383. https://doi.org/10.1186/s12917-0181690-y   DOI
97 Wu J, Ma N, Johnston LJ, Ma X. Dietary nutrients mediate intestinal host defense peptide expression. Advan Nutr 2020; 11:92-102. https://doi.org/10.1093/advances/nmz057   DOI
98 Plesea Condratovici C, Bacarea V, Pique N. Xyloglucan for the treatment of acute gastroenteritis in children: results of a randomized, controlled, clinical trial. Gastroenterol Res Pract 2016; 2016: 6874207. https://doi.org/10.1155/2016/6874207   DOI
99 De Angelis M, Montemurno E, Vannini L, et al. Effect of whole-grain barley on the human fecal microbiota and metabolome. Appl Environ Microbiol 2015;81:7945-56. https:// doi.org/10.1128/AEM.02507-15   DOI
100 Li H, Zhao L, Liu S, Zhang Z, Wang X, Lin H. Propionate inhibits fat deposition via affecting feed intake and modulating gut microbiota in broilers. Poult Sci 2021;100:235-45. https://doi.org/10.1016/j.psj.2020.10.009   DOI
101 Prakatur I, Miskulin M, Pavic M, et al. Intestinal morphology in broiler chickens supplemented with propolis and bee pollen. Animals 2019;9:301. https://doi.org/10.3390/ani9060301   DOI
102 Goto Y. Epithelial cells as a transmitter of signals from commensal bacteria and host immune cells. Front Immunol 2019;10:2057. https://doi.org/10.3389/fimmu.2019.02057   DOI
103 Blank B, Schlecht E, Susenbeth A. Effect of dietary fibre on nitrogen retention and fibre associated threonine losses in growing pigs. Arch Anim Nutr 2012;66:86-101. https://doi.org/10.1080/1745039X.2012.663669   DOI
104 Pellegrini N, Vittadini E, Fogliano V. Designing food structure to slow down digestion in starch-rich products. Curr Opin Food Sci 2020;32:50-7. https://doi.org/10.1016/j.cofs.2020.01.010   DOI
105 Haenen D, Zhang J, Souza da Silva C, et al. A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. J Nutr 2013;143:274-83. https://doi.org/10.3945/jn.112.169672   DOI
106 Pluznick JL, Protzko RJ, Gevorgyan H, et al. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Nat Acad Sci 2013;110:4410-5. https://doi.org/10.1073/pnas.1215927110   DOI
107 Rezaei M, Karimi Torshizi M, Wall H, Ivarsson E. Body growth, intestinal morphology and microflora of quail on diets supplemented with micronised wheat fibre. Br Poult Sci 2018;59:422-9. https://doi.org/10.1080/00071668.2018.1460461   DOI
108 Teimouri Yansari A. Chemical composition, physical characteristics, rumen degradability of NDF and NDF fractionation in rice straw as an effective fibre in ruminants. Ir J Appl Anim Sci 2017;7:221-8.
109 Pourabedin M, Guan L, Zhao X. Xylo-oligosaccharides and virginiamycin differentially modulate gut microbial composition in chickens. Microbiome 2015;3:15. https://doi.org/10.1186/s40168-015-0079-4   DOI
110 Kim MH, Kang SG, Park JH, Yanagisawa M, Kim CH. Shortchain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013;145:396-406. e10. https://doi.org/10.1053/j.gastro.2013.04.056   DOI
111 Duangnumsawang Y, Zentek J, Boroojeni FG. Development and functional properties of intestinal mucus layer in poultry. Front Immunol 2021;12: 745849. https://doi.org/10.3389/fimmu.2021.745849   DOI
112 Umu OC, Frank JA, Fangel JU, et al. Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations. Microbiome 2015;3:16. https://doi.org/10.1186/s40168-015-0078-5   DOI
113 Liu G, Zhao Y, Cao S, et al. Relative bioavailability of selenium yeast for broilers fed a conventional corn-soybean meal diet. J Anim Physiol Anim Nutr 2020;104:1052-66. https://doi.org/10.1111/jpn.13262   DOI
114 Shang Y, Kumar S, Thippareddi H, Kim WK. Effect of dietary fructooligosaccharide (FOS) supplementation on ileal microbiota in broiler chickens. Poult Sci 2018;97:3622-34. https://doi.org/10.3382/ps/pey131   DOI
115 Ebrahimi SH, Valizadeh R, Heidarian Miri V. Rumen microbial community of Saanen goats adapted to a high-fiber diet in the Northeast of Iran. Iran J Appl Anim Sci 2018;8:271-9.
116 Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ. Extensive microbial and functional diversity within the chicken cecal microbiome. PloS One 2014;9:e91941. https://doi.org/10.1371/journal.pone.0091941   DOI
117 Idan F. The role of feed processing and fiber addition on improving the nutrition and growth performance of broilers. Manhattan, KS, USA: Kansas State University; 2019.