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      Assessing the effect of starch digestion characteristics on ileal brake activation in broiler chickens

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          Abstract

          The objective of this research was to evaluate activation of the ileal brake in broiler chickens using diets containing semi-purified wheat (WS; rapidly and highly digested) and pea (PS; slowly and poorly digested) starch. Diets were formulated to contain six WS:PS ratios (100:0, 80:20, 60:40, 40:60, 20:80, 0:100) and each starch ratio was fed to 236 Ross 308 male broilers housed in 4 litter floor pens. At 28 d of age, the effect of PS concentration was assessed on starch digestion, digestive tract morphology, and digesta pH and short-chain fatty acid (SCFA) concentration. Glucagon-like peptide-1 (GLP-1) and peptide tyrosine-tyrosine (PYY) status were assessed in serum (ELISA) and via gene expression in jejunal and ileal tissue (proglucagon for GLP-1). Data were analyzed using regression analyses, and significance was accepted at P ≤ 0.05. Increasing dietary PS resulted in reduced starch digestibility in the small intestine, but had no effect in the colon. Crop content pH responded quadratically to PS level with an estimated minimum at 55% PS. Total SCFA increased linearly in the crop with PS level, but changed in a quadratic fashion in the ileum (estimated maximum at 62% PS). Ceacal SCFA concentrations were highest for the 80 and 100% PS levels. The relative empty weight (crop, small intestine, colon), length (small intestine) and content (crop jejunum, Ileum) of digestive tract sections increased linearly with increasing PS concentration. Dietary treatment did not affect serum GLP-1 or PYY or small intestine transcript abundance. In conclusion, feeding PS increased the presence of L-cell activators (starch, SCFA) and increased trophic development and content of the digestive tract, suggestive of L-cell activation. However, no direct evidence of ileal brake activation was found by measuring venous blood levels of GLP-1 or PYY or corresponding gene expression in small intestine tissue.

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          Technical note: a procedure for the preparation and quantitative analysis of samples for titanium dioxide.

          A procedure was developed for the rapid analysis of titanium dioxide (TiO2) concentrations in feed and fecal samples. Samples were digested in concentrated H2SO4 for 2 h, followed by addition of 30% H2O2, and absorbance was measured at 410 nm. Standards were prepared by spiking blanks with increasing amounts of TiO2, resulting in a linear standard curve. Complete analysis using this procedure can typically be accomplished within 4.5 h. This procedure was compared to a previously published dry-ash procedure for the analysis of TiO2 in bovine fecal samples. Three sources of OM devoid of TiO2 (a forage sample, a bovine fecal sample without Cr2O3, and a bovine fecal sample containing Cr2O3) were spiked with graded amounts (0, 2, 4, 6, 8, or 10 mg) of TiO2. With our procedure, TiO2 recoveries averaged 96.7, 97.5, and 98.5%, for the three OM sources, respectively, vs. 74.3, 83.8, and 53.1% for the same samples analyzed using the dry-ash method. These results suggest that our procedure is a rapid and accurate alternative to dry-ash procedures for the determination of TiO2.
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            Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells.

            Satiety and other core physiological functions are modulated by sensory signals arising from the surface of the gut. Luminal nutrients and bacteria stimulate epithelial biosensors called enteroendocrine cells. Despite being electrically excitable, enteroendocrine cells are generally thought to communicate indirectly with nerves through hormone secretion and not through direct cell-nerve contact. However, we recently uncovered in intestinal enteroendocrine cells a cytoplasmic process that we named neuropod. Here, we determined that neuropods provide a direct connection between enteroendocrine cells and neurons innervating the small intestine and colon. Using cell-specific transgenic mice to study neural circuits, we found that enteroendocrine cells have the necessary elements for neurotransmission, including expression of genes that encode pre-, post-, and transsynaptic proteins. This neuroepithelial circuit was reconstituted in vitro by coculturing single enteroendocrine cells with sensory neurons. We used a monosynaptic rabies virus to define the circuit's functional connectivity in vivo and determined that delivery of this neurotropic virus into the colon lumen resulted in the infection of mucosal nerves through enteroendocrine cells. This neuroepithelial circuit can serve as both a sensory conduit for food and gut microbes to interact with the nervous system and a portal for viruses to enter the enteric and central nervous systems.
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              Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents.

              Glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) are anti-diabetes/obesity hormones secreted from the gut after meal ingestion. We have shown that dietary-resistant starch (RS) increased GLP-1 and PYY secretion, but the mechanism remains unknown. RS is a fermentable fiber that lowers the glycemic index of the diet and liberates short-chain fatty acids (SCFAs) through fermentation in the gut. This study investigates the two possible mechanisms by which RS stimulates GLP-1 and PYY secretion: the effect of a meal or glycemic index, and the effect of fermentation. Because GLP-1 and PYY secretions are stimulated by nutrient availability in the gut, the timing of blood sample collections could influence the outcome when two diets with different glycemic indexes are compared. Thus we examined GLP-1 and PYY plasma levels at various time points over a 24-h period in RS-fed rats. In addition, we tested proglucagon (a precursor to GLP-1) and PYY gene expression patterns in specific areas of the gut of RS-fed rats and in an enteroendocrine cell line following exposure to SCFAs in vitro. Our findings are as follows. 1) RS stimulates GLP-1 and PYY secretion in a substantial day-long manner, independent of meal effect or changes in dietary glycemia. 2) Fermentation and the liberation of SCFAs in the lower gut are associated with increased proglucagon and PYY gene expression. 3) Glucose tolerance, an indicator of increased active forms of GLP-1 and PYY, was improved in RS-fed diabetic mice. We conclude that fermentation of RS is most likely the primary mechanism for increased endogenous secretions of total GLP-1 and PYY in rodents. Thus any factor that affects fermentation should be considered when dietary fermentable fiber is used to stimulate GLP-1 and PYY secretion.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 February 2020
                2020
                : 15
                : 2
                : e0228647
                Affiliations
                [001]Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
                University of New England, AUSTRALIA
                Author notes

                Competing Interests: We have the following competing interests: This study was funded in part by Aviagen North America, Sofina Foods Inc., Prairie Pride Natural Foods Ltd., Chicken Farmers of Saskatchewan, Canadian Poultry Research Council, Poultry Industry Council (Canada), Saskatchewan Broiler Hatching Egg Producer's Marketing Board, Saskatchewan Egg Producers and Saskatchewan Turkey Producers' Marketing Board. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.

                Author information
                http://orcid.org/0000-0001-6630-5673
                Article
                PONE-D-19-31629
                10.1371/journal.pone.0228647
                7006927
                32032378
                b83fb31c-af3a-46c4-b1c5-fde93f68c383
                © 2020 Herwig et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 November 2019
                : 20 January 2020
                Page count
                Figures: 0, Tables: 11, Pages: 20
                Funding
                Funded by: Aviagen North America
                Award ID: 414702
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008681, Canadian Poultry Research Council;
                Award ID: 414703
                Award Recipient :
                Funded by: Chicken Farmers of Saskatchewan
                Award ID: 414704
                Award Recipient :
                Funded by: Sofina Foods Inc.
                Award ID: 414705
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008776, Poultry Industry Council;
                Award ID: 414706
                Award Recipient :
                Funded by: Prairie Pride Natural Foods Ltd.
                Award ID: 414707
                Award Recipient :
                Funded by: Saskatchewan Broiler Hatching Egg Producer's Marketing Board
                Award ID: 414708
                Award Recipient :
                Funded by: Saskatchewan Egg Producers
                Award ID: 414709
                Award Recipient :
                Funded by: Saskatchewan Turkey Producers' Marketing Board
                Award ID: 414710
                Award Recipient :
                Funded by: University of Saskatchewan
                Award ID: 414739
                Award Recipient :
                Funded by: Natural Science and Engineering Research Council
                Award ID: 414764
                Award Recipient :
                HLC - Grant # 414702 Aviagen North America http://en.aviagen.com/ HLC - Grant # 414703 Canadian Poultry Research Council http://cp-rc.ca/ HLC - Grant # 414704 Chicken Farmers of Saskatchewan http://www.saskatchewanchicken.ca/ HLC - Grant # 414705 Sofina Foods Inc. https://www.sofinafoods.com/ HLC - Grant # 414706 Poultry Industry Council https://www.poultryindustrycouncil.ca/ HLC - Grant # 414707 Prairie Pride Natural Foods Ltd. No website - 3535 Millar Avenue Saskatoon, SK S7P 0A2 HLC - Grant # 414708 Saskatchewan Broiler Hatching Egg Producer's Marketing Board No website - 224 Pacific Ave., Suite 201 Saskatoon, SK, S7K 1N9 HLC - Grant # 414709 Saskatchewan Egg Producers http://www.saskegg.ca/ HLC - Grant # 414710 Saskatchewan Turkey Producers' Marketing Board https://www.saskturkey.com/ HLC - Grant # 414739 University of Saskatchewan https://www.usask.ca/ HLC - Grant # 414764 NSERC https://www.nserc-crsng.gc.ca/index_eng.asp
                Categories
                Research Article
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Carbohydrates
                Starches
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Carbohydrates
                Starches
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Ileum
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Ileum
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Legumes
                Peas
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Jejunum
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Jejunum
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Small Intestine
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Small Intestine
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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