Hostname: page-component-7dd5485656-wjfd9 Total loading time: 0 Render date: 2025-10-31T01:31:40.612Z Has data issue: false hasContentIssue false
  • English
  • Français

Importance of release location on the mode of action of butyrate derivatives in the avian gastrointestinal tract

Published online by Cambridge University Press:  19 January 2016

P.C.A. MOQUET ,
L. ONRUST ,
F. VAN IMMERSEEL ,
R. DUCATELLE ,
W.H. HENDRIKS  and
R.P. KWAKKEL
P.C.A. MOQUET*
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
L. ONRUST
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
F. VAN IMMERSEEL
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
R. DUCATELLE
Affiliation:
Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
W.H. HENDRIKS
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
R.P. KWAKKEL
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
*
Corresponding author: pierre.moquet@wur.nl
Get access

Abstract

In the field of animal nutrition, butyrate is used as a zootechnical ingredient and can be used as an unprotected salt or in the form of protected derivatives such as butyrate glycerides or butyrate-loaded matrices. Dietary butyrate supplementation has been shown to improve growth performance and resilience of broiler chickens through distinct mechanisms, operating on both eukaryotic and prokaryotic cells. Firstly, butyrate influences endogenous avian cells in multiple ways: it is an agonist of free-fatty acid receptors, an inhibitor of pro-inflammatory pathways, an epigenetic modulating agent and acts as an energy source. Secondly, butyrate influences the microbiota residing in the avian gastrointestinal tract (GIT) as a result of its bacteriostatic properties. The responses, e.g. changes in growth performance, gut morphology, carcass traits or nutrient digestibility of chickens, to dietary butyrate supplementation are inconsistent with factors such as additive inclusion level, diet composition, age and health status of the bird modulating the effects of butyrate and its derivatives. For many derivatives, the precise GIT segment wherein butyrate is released is unclear. Release location may affect the observed responses to butyrate given the diversity of cell types and pH conditions encountered throughout the gastrointestinal tract of poultry, and the differences in microbiota composition in the different gut segments. As a consequence, our understanding of the mode of action of butyrate is hampered. Characterisation of existing derivatives and development of targeted-release formulations are, therefore, important to gain insight in the different physiological effects butyrate can elicit in broiler chickens.

Keywords

butyratebroilerrelease locationmode of action

Information

Type
Reviews
Information
World's Poultry Science Journal , Volume 72 , Issue 1 , March 2016 , pp. 61 - 80
Copyright
Copyright © World's Poultry Science Association 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

AGHAZADEH, A.M. and TAHA YAZDI, M. (2012) Effect of butyric acid supplementation and whole wheat inclusion on the performance and carcass traits of broilers. South African Journal of Animal Science 42: 241-248.CrossRefGoogle Scholar
ANDRIAMIHAJA, M., CHAUMONTET, C., TOME, D. and BLACHIER, F. (2009) Butyrate metabolism in human colon carcinoma cells: implications concerning its growth-inhibitory effect. Journal of Cellular Physiology 218: 58-65.CrossRefGoogle ScholarPubMed
ANTONGIOVANNI, M., BUCCIONI, A., PETACCHI, F., LEESON, S., MINIERI, S., MARTINI, A. and CECCHI, R. (2009) Butyric acid glycerides in the diet of broiler chickens: effects on gut histology and carcass composition. Italian Journal of Animal Science 6: 19-25.CrossRefGoogle Scholar
ASTBURY, S.M. and CORFE, B.M. (2012) Uptake and metabolism of the short-chain fatty acid butyrate, a critical review of the literature. Current Drug Metabolism 13: 815-821.CrossRefGoogle ScholarPubMed
BARCELO, A., CLAUSTRE, J., MORO, F., CHAYVIALLE, J.A., CUBER, J.C. and PLAISANCIE, P. (2000) Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 46: 218-224.CrossRefGoogle ScholarPubMed
BARNES, P.J. and KARIN, M. (1997) Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. The New England Journal of Medicine 336: 1066-1071.CrossRefGoogle ScholarPubMed
BARTHOLOME, A.L., ALBIN, D.M., BAKER, D.H., HOLST, J.J. and TAPPENDEN, K.A. (2004) Supplementation of total parenteral nutrition with butyrate acutely increases structural aspects of intestinal adaptation after an 80% jejunoileal resection in neonatal piglets. Journal of Parenteral and Enteral Nutrition 28: 210-222; discussion 222-223.CrossRefGoogle ScholarPubMed
BÖHMIG, G.A., KRIEGER, P.M., SAEMANN, M.D., ULLRICH, R., KARIMI, H., WEKERLE, T., MUHLBACHER, F. and ZLABINGER, G.J. (1999) Stable prodrugs of n-butyric acid: suppression of T cell alloresponses in vitro and prolongation of heart allograft survival in a fully allogeneic rat strain combination. Transplant Immunology 7: 221-227.CrossRefGoogle Scholar
BÖHMIG, G.A., KRIEGER, P.M., SÄEMANN, M.D., WENHARDT, C., POHANKA, E. and ZLABINGER, G.J. (1997) n-Butyrate downregulates the stimulatory function of peripheral blood-derived antigen-presenting cells: a potential mechanism for modulating T-cell responses by short-chain fatty acids. Immunology 92: 234-243.CrossRefGoogle ScholarPubMed
BORGSTRÖM, B. (1975) On the interactions between pancreatic lipase and colipase and the substrate, and the importance of bile salts. Journal of Lipid Research 16: 411-417.CrossRefGoogle ScholarPubMed
CANANI, R.B., COSTANZO, M.D., LEONE, L., PEDATA, M., MELI, R. and CALIGNANO, A. (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World Journal of Gastroenterology 17: 1519-1528.CrossRefGoogle ScholarPubMed
CASTILLO, M., MARTIN-ORUE, S.M., ROCA, M., MANZANILLA, E.G., BADIOLA, I., PEREZ, J.F. and GASA, J. (2006) The response of gastrointestinal microbiota to avilamycin, butyrate, and plant extracts in early-weaned pigs. Journal of Animal Sciences 84: 2725-2734.CrossRefGoogle ScholarPubMed
CERISUELO, A., MARIN, C., SANCHEZ-VIZCAINO, F., GOMEZ, E.A., DE LA FUENTE, J.M., DURAN, R. and FERNANDEZ, C. (2014) The impact of a specific blend of essential oil components and sodium butyrate in feed on growth performance and Salmonella counts in experimentally challenged broilers. Poultry Science 93: 599-606.CrossRefGoogle ScholarPubMed
CHERRINGTON, C.A., HINTON, M., PEARSON, G.R. and CHOPRA, I. (1991) Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. Journal of Applied Bacteriology 70: 161-165.CrossRefGoogle ScholarPubMed
CZERWINSKI, J., HOJBERG, O., SMULIKOWSKA, S., ENGBERG, R.M. and MIECZKOWSKA, A. (2012) Effects of sodium butyrate and salinomycin upon intestinal microbiota, mucosal morphology and performance of broiler chickens. Archives of Animal Nutrition 66: 102-116.CrossRefGoogle ScholarPubMed
DE BRABANDER, C., VERVAET, C., FIERMANS, L. and REMON, J.P. (2000) Matrix mini-tablets based on starch/microcrystalline wax mixtures. International Journal of Pharmaceutics 199: 195-203.CrossRefGoogle ScholarPubMed
DENBOW, D.M. (2015) Chapter 14 - Gastrointestinal Anatomy and Physiology, in: SCANES, C.G. (Ed) Sturkie's Avian Physiology (Sixth Edition), pp. 337-66 (San Diego, Academic Press).Google Scholar
DOREAU, M. and CHILLIARD, Y. (1997) Digestion and metabolism of dietary fat in farm animals. British Journal of Nutrition 78 Suppl 1: S15-35.CrossRefGoogle ScholarPubMed
DUMOULIN, V., MORO, F., BARCELO, A., DAKKA, T. and CUBER, J.C. (1998) Peptide YY, glucagon-like peptide-1, and neurotensin responses to luminal factors in the isolated vascularly perfused rat ileum. Endocrinology 139: 3780-3786.CrossRefGoogle ScholarPubMed
ENGELSTOFT, M.S., EGEROD, K.L., HOLST, B. and SCHWARTZ, T.W. (2008) A gut feeling for obesity: 7TM sensors on enteroendocrine cells. Cell Metabolism 8: 447-449.CrossRefGoogle ScholarPubMed
FRANKEL, W.L., ZHANG, W., SINGH, A., KLURFELD, D.M., DON, S., SAKATA, T., MODLIN, I. and ROMBEAU, J.L. (1994) Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology 106: 375-380.CrossRefGoogle ScholarPubMed
GAUDIER, E., JARRY, A., BLOTTIERE, H.M., DE COPPET, P., BUISINE, M.P., AUBERT, J.P., LABOISSE, C., CHERBUT, C. and HOEBLER, C. (2004) Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. American Journal of Physiology - Gastrointestinal and Liver Physiology 287: G1168-1174.CrossRefGoogle ScholarPubMed
GUILLOTEAU, P., MARTIN, L., EECKHAUT, V., DUCATELLE, R., ZABIELSKI, R. and VAN IMMERSEEL, F. (2010a) From the gut to the peripheral tissues: the multiple effects of butyrate. Nutrition Research Reviews 23: 366-384.CrossRefGoogle Scholar
GUILLOTEAU, P., SAVARY, G., JAGUELIN-PEYRAULT, Y., ROME, V., LE NORMAND, L. and ZABIELSKI, R. (2010b) Dietary sodium butyrate supplementation increases digestibility and pancreatic secretion in young milk-fed calves. Journal of Dairy Science 93: 5842-5850.CrossRefGoogle ScholarPubMed
HAMER, H.M., JONKERS, D., VENEMA, K., VANHOUTVIN, S., TROOST, F.J. and BRUMMER, R.J. (2008) Review article: the role of butyrate on colonic function. Alimentary Pharmacology & Therapeutics 27: 104-119.CrossRefGoogle ScholarPubMed
HAMER, H.M., JONKERS, D.M., BAST, A., VANHOUTVIN, S.A., FISCHER, M.A., KODDE, A., TROOST, F.J., VENEMA, K. and BRUMMER, R.J. (2009) Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clinical Nutrition 28: 88-93.CrossRefGoogle ScholarPubMed
HAUTEKIET, V., COLLET, P., VAN HAMME, V., GOETHALS, L. and SCHÄUBLIN, H. (2011) Influence of an additive based on encapsulated calcium butyrate in two nutritional profiles on growth performance of broiler chickens. Neuvièmes Journées de la Recherche Avicole, Tours, pp. 247-250.Google Scholar
HU, Z. and GUO, Y. (2007) Effects of dietary sodium butyrate supplementation on the intestinal morphological structure, absorptive function and gut flora in chickens. Animal Feed Science and Technology 132: 240-249.CrossRefGoogle Scholar
ICHIKAWA, H., SHINEHA, R., SATOMI, S. and SAKATA, T. (2002) Gastric or rectal instillation of short-chain fatty acids stimulates epithelial cell proliferation of small and large intestine in rats. Digestive Diseases and Sciences 47: 1141-1146.CrossRefGoogle ScholarPubMed
JERZSELE, A., SZEKER, K., CSIZINSZKY, R., GERE, E., JAKAB, C., MALLO, J.J. and GALFI, P. (2012) Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination, and Bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. Poultry Science 91: 837-843.CrossRefGoogle ScholarPubMed
KATO, S., SATO, K., CHIDA, H., ROH, S.G., OHWADA, S., SATO, S., GUILLOTEAU, P. and KATOH, K. (2011) Effects of Na-butyrate supplementation in milk formula on plasma concentrations of GH and insulin, and on rumen papilla development in calves. Journal of Endocrinology 211: 241-248.CrossRefGoogle ScholarPubMed
KIEN, C.L., BLAUWIEKEL, R., BUNN, J.Y., JETTON, T.L., FRANKEL, W.L. and HOLST, J.J. (2007) Cecal infusion of butyrate increases intestinal cell proliferation in piglets. Journal of Nutrition 137: 916-922.CrossRefGoogle ScholarPubMed
KLASING, K.C. and JOHNSTONE, B.J. (1991) Monokines in growth and development. Poultry Science 70: 1781-1789.CrossRefGoogle ScholarPubMed
KLASING, K.C., LAURIN, D.E., PENG, R.K. and FRY, D.M. (1987) Immunologically mediated growth depression in chicks: influence of feed intake, corticosterone and interleukin-1. Journal of Nutrition 117: 1629-1637.CrossRefGoogle ScholarPubMed
KOTUNIA, A., WOLINSKI, J., LAUBITZ, D., JURKOWSKA, M., ROME, V., GUILLOTEAU, P. and ZABIELSKI, R. (2004) Effect of sodium butyrate on the small intestine development in neonatal piglets fed [correction of feed] by artificial sow. Journal of Physiology and Pharmacology 55 Suppl 2: 59-68.Google ScholarPubMed
LAL, S., KIRKUP, A.J., BRUNSDEN, A.M., THOMPSON, D.G. and GRUNDY, D. (2001) Vagal afferent responses to fatty acids of different chain length in the rat. American Journal of Physiology - Gastrointestinal and Liver Physiology 281: G907-915.CrossRefGoogle ScholarPubMed
LAWHON, S.D., MAURER, R., SUYEMOTO, M. and ALTIER, C. (2002) Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Molecular Microbiology 46: 1451-1464.CrossRefGoogle ScholarPubMed
LEESON, S., NAMKUNG, H., ANTONGIOVANNI, M. and LEE, E.H. (2005) Effect of butyric acid on the performance and carcass yield of broiler chickens. Poultry Science 84: 1418-1422.CrossRefGoogle ScholarPubMed
LEWIS, K., LUTGENDORFF, F., PHAN, V., SODERHOLM, J.D., SHERMAN, P.M. and MCKAY, D.M. (2010) Enhanced translocation of bacteria across metabolically stressed epithelia is reduced by butyrate. Inflammatory Bowel Diseases 16: 1138-1148.CrossRefGoogle ScholarPubMed
LIN, H.V., FRASSETTO, A., KOWALIK, E.J., Jr, NAWROCKI, A.R., LU, M.M., KOSINSKI, J.R., HUBERT, J.A., SZETO, D., YAO, X., FORREST, G. and MARSH, D.J. (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE 7: e35240.CrossRefGoogle Scholar
LIOU, A.P. (2013) Digestive physiology of the pig symposium: G protein-coupled receptors in nutrient chemosensation and gastrointestinal hormone secretion. Journal of Animal Science 91: 1946-1956.CrossRefGoogle ScholarPubMed
MA, X., FAN, P.X., LI, L.S., QIAO, S.Y., ZHANG, G.L. and LI, D.F. (2012) Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions. Journal of Animal Science 90 Suppl 4: 266-268.CrossRefGoogle ScholarPubMed
MAA, M.C., CHANG, M.Y., HSIEH, M.Y., CHEN, Y.J., YANG, C.J., CHEN, Z.C., LI, Y.K., YEN, C.K., WU, R.R. and LEU, T.H. (2010) Butyrate reduced lipopolysaccharide-mediated macrophage migration by suppression of Src enhancement and focal adhesion kinase activity. Journal of Nutritional Biochemistry 21: 1186-1192.CrossRefGoogle ScholarPubMed
MAHDAVI, R. and TORKI, M. (2009) Study on usage period of dietary protected butyric acid on performance, carcass characteristics, serum metabolite levels and humoral immune response of broiler chickens. Journal of Animal and Veterinary Advances 8: 1702-1709.Google Scholar
MAIER, T., GÜELL, M. and SERRANO, L. (2009) Correlation of mRNA and protein in complex biological samples. FEBS Letters 583: 3966-3973.CrossRefGoogle ScholarPubMed
MALLO, J.J., BALFAGON, A., GRACIA, M.I., HONRUBIA, P. and PUYALTO, M. (2012) Evaluation of different protections of butyric acid aiming for release in the last part of the gastrointestinal tract of piglets. Journal of Animal Sciences 90 Suppl 4: 227-229.CrossRefGoogle ScholarPubMed
MANZANILLA, E.G., NOFRARIAS, M., ANGUITA, M., CASTILLO, M., PEREZ, J.F., MARTIN-ORUE, S.M., KAMEL, C. and GASA, J. (2006) Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. Journal of Animal Sciences 84: 2743-2751.CrossRefGoogle Scholar
MAZZONI, M., LE GALL, M., DE FILIPPI, S., MINIERI, L., TREVISI, P., WOLINSKI, J., LALATTA-COSTERBOSA, G., LALLES, J.P., GUILLOTEAU, P. and BOSI, P. (2008) Supplemental sodium butyrate stimulates different gastric cells in weaned pigs. Journal of Nutrition 138: 1426-1431.CrossRefGoogle ScholarPubMed
MEIJER, K., DE VOS, P. and PRIEBE, M.G. (2010) Butyrate and other short-chain fatty acids as modulators of immunity: what relevance for health? Current Opinion in Clinical Nutrition and Metabolic Care 13: 715-721.CrossRefGoogle ScholarPubMed
MENTSCHEL, J. and CLAUS, R. (2003) Increased butyrate formation in the pig colon by feeding raw potato starch leads to a reduction of colonocyte apoptosis and a shift to the stem cell compartment. Metabolism 52: 1400-1405.CrossRefGoogle Scholar
MOEINIAN, M., FARNAZ GHASEMI-NIRI, S., MOZAFFARI, S. and ABDOLLAHI, M. (2013) Synergistic effect of probiotics, butyrate and l-Carnitine in treatment of IBD. Journal of Medical Hypotheses and Ideas 7: 50-53.CrossRefGoogle Scholar
MOREAU, H., GARGOURI, Y., LECAT, D., JUNIEN, J.L. and VERGER, R. (1988) Screening of preduodenal lipases in several mammals. Biochimica et Biophysica Acta 959: 247-252.CrossRefGoogle ScholarPubMed
NOHR, M.K., PEDERSEN, M.H., GILLE, A., EGEROD, K.L., ENGELSTOFT, M.S., HUSTED, A.S., SICHLAU, R.M., GRUNDDAL, K.V., POULSEN, S.S., HAN, S., JONES, R.M., OFFERMANNS, S. and SCHWARTZ, T.W. (2013) GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology154: 3552-3564.CrossRefGoogle ScholarPubMed
PANDA, A.K., RAO, S.V.R., RAJU, M.V.L.N. and SUNDER, G.S. (2009) Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Sciences 22: 1026-1031.CrossRefGoogle Scholar
PENG, L., LI, Z.R., GREEN, R.S., HOLZMAN, I.R. and LIN, J. (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. Journal of Nutrition 139: 1619-1625.CrossRefGoogle ScholarPubMed
PLAISANCIE, P., DUMOULIN, V., CHAYVIALLE, J.A. and CUBER, J.C. (1995) Luminal glucagon-like peptide-1(7-36) amide-releasing factors in the isolated vascularly perfused rat colon. Journal of Endocrinology 145: 521-526.CrossRefGoogle ScholarPubMed
PLAISANCIE, P., DUMOULIN, V., CHAYVIALLE, J.A. and CUBER, J.C. (1996) Luminal peptide YY-releasing factors in the isolated vascularly perfused rat colon. Journal of Endocrinology 151: 421-429.CrossRefGoogle ScholarPubMed
PLOGER, S., STUMPFF, F., PENNER, G.B., SCHULZKE, J.D., GABEL, G., MARTENS, H., SHEN, Z., GUNZEL, D. and ASCHENBACH, J.R. (2012) Microbial butyrate and its role for barrier function in the gastrointestinal tract. Annals of the New York Academy of Sciences 1258: 52-59.CrossRefGoogle ScholarPubMed
QAISRANI, S.N. (2014) Improving performance of broilers fed lower digestible protein diets. Ph. D. Thesis, Wageningen University, Wageningen, The Netherlands.Google Scholar
REILLY, K.J., FRANKEL, W.L., BAIN, A.M. and ROMBEAU, J.L. (1995) Colonic short chain fatty acids mediate jejunal growth by increasing gastrin. Gut 37: 81-86.CrossRefGoogle ScholarPubMed
RIBEIRO, J., GASPAR, S., PINHO, M., FREIRE, J.P.B. and FALCÃO-E-CUNHA, L. (2012) Sodium butyrate in growing and fattening diets for early-weaned rabbits. World Rabbit Science 20: 199-207.CrossRefGoogle Scholar
RUSSELL, J.B. and DIEZ-GONZALEZ, F. (1998) The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 39: 205-234.CrossRefGoogle ScholarPubMed
SAKATA, T. (1989) Stimulatory effect of short-chain fatty acids on epithelial cell proliferation of isolated and denervated jejunal segment of the rat. Scandinavian Journal of Gastroenterology 24: 886-890.CrossRefGoogle ScholarPubMed
SAYRAFI, R., SOLTANALINEJAD, F., SHAHROOZ, R. and RAHIMI, S. (2011) Comparative study of the effect of alternative and antibiotic feed additives on the performance and intestinal histomorphometrical parameters of broiler chickens. African Journal of Agricultural Research 6: 2794-2799.Google Scholar
SCHEPPACH, W. and WEILER, F. (2004) The butyrate story: old wine in new bottles? Current Opinion in Clinical Nutrition and Metabolic Care 7: 563-567.CrossRefGoogle ScholarPubMed
SCHNEEBERGER, E.E. and LYNCH, R.D. (2004) The tight junction: a multifunctional complex. The American Journal of Physiology - Cell Physiology 286: C1213-1228.CrossRefGoogle ScholarPubMed
SEGAIN, J.P., RAINGEARD DE LA BLETIERE, D., BOURREILLE, A., LERAY, V., GERVOIS, N., ROSALES, C., FERRIER, L., BONNET, C., BLOTTIERE, H.M. and GALMICHE, J.P. (2000) Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47: 397-403.CrossRefGoogle ScholarPubMed
SENGUPTA, S., MUIR, J.G. and GIBSON, P.R. (2006) Does butyrate protect from colorectal cancer? Journal Gastroenterology and Hepatology 21: 209-218.CrossRefGoogle ScholarPubMed
SKLAN, D., SHACHAF, B., BARON, J. and HURWITZ, S. (1978) Retrograde movement of digesta in the duodenum of the chick: extent, frequency, and nutritional implications. Journal of Nutrition 108: 1485-1490.CrossRefGoogle ScholarPubMed
SMITH, D.J., BARRI, A., HERGES, G., HAHN, J., YERSIN, A.G. and JOURDAN, A. (2012) In vitro dissolution and in vivo absorption of calcium [1-(14)c]butyrate in free or protected forms. Journal of Agricultural and Food Chemistry 60: 3151-3157.CrossRefGoogle ScholarPubMed
SMITH, J.G., YOKOYAMA, W.H. and GERMAN, J.B. (1998) Butyric acid from the diet: actions at the level of gene expression. Critical Reviews in Food Science and Nutrition 38: 259-297.CrossRefGoogle ScholarPubMed
SMULIKOWSKA, S., CZERWINSKI, J., MIECZKOWSKA, A. and JANKOWIAK, J. (2009) The effect of fat-coated organic acid salts and a feed enzyme on growth performance, nutrient utilisation, microflora activity, and morphology of the small intestine in broiler chickens. Journal of Animal and Feed Sciences 18: 478-489.CrossRefGoogle Scholar
SOSSAI, P. (2012) Butyric acid: what is the future for this old substance? Swiss Medical Weekly 142: w13596.Google ScholarPubMed
SUNKARA, L.T., ACHANTA, M., SCHREIBER, N.B., BOMMINENI, Y.R., DAI, G., JIANG, W., LAMONT, S., LILLEHOJ, H.S., BEKER, A., TEETER, R.G. and ZHANG, G. (2011) Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS ONE 6: e27225.CrossRefGoogle Scholar
SWIATKIEWICZ, S., ARCZEWSKA-WLOSEK, A. and JOZEFIAK, D. (2014) Feed enzymes, probiotic, or chitosan can improve the nutritional efficacy of broiler chicken diets containing a high level of distillers dried grains with solubles. Livestock Science 163: 110-119.CrossRefGoogle Scholar
SYKARAS, A.G., DEMENIS, C., CASE, R.M., MCLAUGHLIN, J.T. and SMITH, C.P. (2012) Duodenal enteroendocrine I-cells contain mRNA transcripts encoding key endocannabinoid and fatty acid receptors. PLoS ONE 7: e42373.CrossRefGoogle Scholar
ULLUWISHEWA, D., ANDERSON, R.C., MCNABB, W.C., MOUGHAN, P.J., WELLS, J.M. and ROY, N.C. (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. Journal of Nutrition 141: 769-776.CrossRefGoogle ScholarPubMed
VAN DIJK, J., HUISMAN, J. and KONINKX, J. (2002) Structural and functional aspects of a healthy gastrointestinal tract, in: BLOC, M.C., VAHL, H.A., DE LANGE, L., VAN DE BRAAK, A.E., HEMKE, G. & HESSING, M. (Eds) Nutrition and health of the gastrointestinal tract, pp. 71-92 (Wageningen, Wageningen Academic Publishers).Google Scholar
VAN IMMERSEEL, F., BOYEN, F., GANTOIS, I., TIMBERMONT, L., BOHEZ, L., PASMANS, F., HAESEBROUCK, F. and DUCATELLE, R. (2005) Supplementation of coated butyric acid in the feed reduces colonisation and shedding of Salmonella in poultry. Poultry Science 84: 1851-1856.CrossRefGoogle ScholarPubMed
VERVAECK, A., SAERENS, L., DE GEEST, B.G., DE BEER, T., CARLEER, R., ADRIAENSENS, P., REMON, J.P. and VERVAET, C. (2013) Prilling of fatty acids as a continuous process for the development of controlled release multiparticulate dosage forms. European Journal of Pharmaceutics and Biopharmaceutics 85: 587-596.CrossRefGoogle ScholarPubMed
VIDRINE, K., YE, J., MARTIN, R.J., MCCUTCHEON, K.L., RAGGIO, A.M., PELKMAN, C., DURHAM, H.A., ZHOU, J., SENEVIRATHNE, R.N., WILLIAMS, C., GREENWAY, F., FINLEY, J., GAO, Z., GOLDSMITH, F. and KEENAN, M.J. (2014) Resistant starch from high amylose maize (HAM-RS2) and dietary butyrate reduce abdominal fat by a different apparent mechanism. Obesity 22: 344-348.CrossRefGoogle ScholarPubMed
WANG, H.B., WANG, P.Y., WANG, X., WAN, Y.L. and LIU, Y.C. (2012) Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein Claudin-1 transcription. Digestive Diseases and Sciences 57: 3126-3135.CrossRefGoogle ScholarPubMed
WATFORD, M., LUND, P. and KREBS, H.A. (1979) Isolation and metabolic characteristics of rat and chicken enterocytes. Biochemical Journal 178: 589-596.CrossRefGoogle ScholarPubMed
WILLEMSEN, L.E., KOETSIER, M.A., VAN DEVENTER, S.J. and VAN TOL, E.A. (2003) Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 52: 1442-1447.CrossRefGoogle Scholar
YILMAZ, A., SHEN, S., ADELSON, D.L., XAVIER, S. and ZHU, J.J. (2005) Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 56: 743-753.CrossRefGoogle ScholarPubMed
ZHANG, W.H., GAO, F., ZHU, Q.F., LI, C., JIANG, Y., DAI, S.F. and ZHOU, G.H. (2011a) Dietary sodium butyrate alleviates the oxidative stress induced by corticosterone exposure and improves meat quality in broiler chickens. Poultry Science 90: 2592-2599.CrossRefGoogle ScholarPubMed
ZHANG, W.H., JIANG, Y., ZHU, Q.F., GAO, F., DAI, S.F., CHEN, J. and ZHOU, G.H. (2011b) Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens. British Poultry Science 52: 292-301.CrossRefGoogle ScholarPubMed