Colostrum insulin supplementation to neonatal Holstein bulls affects small intestinal histomorphology, mRNA expression, and enzymatic activity with minor influences on peripheral metabolism

Abstract

The objectives of this study were to evaluate how varying colostral insulin concentrations influenced small intestinal development and peripheral metabolism in neonatal Holstein bulls. Insulin was supplemented to approximately 5× (70.0 μg/L; n = 16) or 10× (149.7 μg/L; n = 16) the basal colostrum insulin (12.9 μg/L; BI, n = 16) concentration to maintain equivalent macronutrient intake (crude fat: 4.1 ± 0.06%; crude protein: 11.7 ± 0.05%; and lactose: 1.9 ± 0.01%) among treatments. Colostrum was fed at 2, 14, and 26 h postnatal and blood metabolites and insulin concentration were measured at 0, 30, 60, 90, 120, 180, 240, 360, 480, and 600 min postprandial respective to the first and second colostrum meal. At 30 h postnatal, a subset of calves (n = 8/treatment) were killed to excise the gastrointestinal and visceral tissues. Gastrointestinal and visceral gross morphology and dry matter and small intestinal histomorphology, gene expression, and carbohydrase activity were assessed. Insulin supplementation tended to linearly reduce the glucose clearance rate following the first meal, whereas after the second meal, supplementation linearly increased the rate of glucose absorption and nonesterified fatty acid clearance rate, decreased the time to maximum glucose concentrations, and decreased the time to reach minimum nonesterified fatty acid concentrations. Additionally, insulin clearance rate was linearly increased by insulin supplementation following the second colostrum feeding. However, there were no overall differences between treatments in the concentrations of glucose, nonesterified fatty acids, or insulin in plasma or serum. With respect to macroscopic intestinal development, dry rumen tissue mass linearly decreased when insulin was supplemented in colostrum, and supplementation linearly increased duodenal dry tissue density (g dry matter/cm) while tending to increase duodenal dry tissue weight. Increasing the colostrum insulin concentration improved small intestinal histomorphological development in the distal small intestine, as ileal villi height and mucosal-serosal surface area index were increased by supplementing insulin. Lactase enzymatic activity linearly increased in the proximal jejunum while ileal isomaltase activity linearly decreased with insulin supplementation. These data indicate that changes in colostrum insulin concentrations rapidly affect gastrointestinal growth prioritization and carbohydrase activity. The changes in gastrointestinal ontology result in minor changes in postprandial metabolite availability and clearance.