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Main physiological criteria accounting for changes in gut structure and functionality in weaned pigs

We studied gut morphology, physiology and intestinal ecology during 15 d post-weaning in piglets in order to better understand gut disorders and to define gut health criteria. We investigated digestive tract characteristics, mucosal morphology, absorptive and secretory physiology, epithelial barrier function and bacterial populations along the intestines. After a 2 day-fast, the piglets were fed intragastrically six times daily, following a scheduled feed intake plan. The piglets were pair-fed either a wheat-based or a control diet and slaughtered kinetically.

Blood was collected for gastrin and CCK assays. Gut weight characteristics were recorded. Mucosa from small and large intestines was studied for absorptive, secretory and barrier function in Ussing chambers, and for morphometry and digestive enzyme activities and gene expression. Pancreas was collected for protein, trypsin and lipase activity determination. At days 0, 8 and 15, intestinal contents were collected for counting various types of bacteria. Data were subjected to analyse of variance (diet factor removed because non significant). In order to have a global view of weaning diet adaptation, 71 variables (excluding bacterial counts) measured on d 5-15 were analysed by principal component analysis.

The weight of stomach and large intestine relative to body weight were not affected by fasting at weaning, contrary to that of small intestine which was lighter at d2 than at day 0. After day 2, the relative weight of gut segments and digesta contents increased rapidly. The pancreas presented high protein and enzyme contents at d2, as compared to day 0. Between day 2 and day 5, all pancreatic parameters decreased sharply, but afterwards trypsin and amylase activities were stimulated. Villous atrophy was maximal at day 2 in the duodenum and at day 5 in the ileum.

Atrophy was the greatest in the duodenum and villous area was not fully recovered at d15 post-weaning. Weaning diet intake favoured an increase in ileal villous size up to values recorded at day 0. Crypt size was not changed with fasting but it increased sharply thereafter. At day 15, crypt length and surface were superior to values measured at day 0 and day 2. Expression of intestinal enzymes was highly modulated by weaning. At day2, fasting had depressed intestinal enzyme activities, but not specific mRNA. Duodenal enzyme expression (mRNA and activities) of maltase increased after re-feeding, whereas that of lactase decreased.

The basal short-circuit current in jejunum and colon, and glucose absorption in jejunum, were increased 2 day after weaning, whereas a dramatic drop of tissue resistance occurred in the jejunum. These parameters had returned to pre-weaning values by day 5. Jejunal responses to secretagogues and glucose absorption were decreased the second week after weaning. Ileal transmucosal resistance was higher on day 5 and stayed stable thereafter. Fluxes of macromolecules across the jejunal mucosa dropped on day 2 and stayed at this low level thereafter.

Gastrin and CCK levels were low after the fasting period and increased thereafter. In jejunal digesta, similar counts of bacteria were observed at day 0 and day 8. Afterwards, counts of total anaerobes and aerobes, enterobacteria and enterococci tended to decrease. In colonic digesta, counts of all bacterial types were higher on day 8 compared to day 0. Afterwards, they decreased between day 8 and 15, except for lactobacilli that did not change.
Principal component analysis was first performed with the 71 variables and then with the 12 non-redundant and most significant variables. The first three principal components explained 70% of the variability between piglets. Component 1 discriminated those slaughtered at day 5 and day 15 and could be interpreted as the axis of time post-weaning. It correlated with variables measuring gut weight characteristics. Component 2 was correlated with variables measuring structural and functional characteristics of ileal mucosa.

The global data analysis indicated that the post-weaning period could be divided into two periods. The early phase consisted in an acute deterioration of the structure and activities of the duodenal mucosa, probably in relation with fasting. By contrast, duodenal crypts and levels of mRNA coding for enzymes were not affected by fasting. At the ileum, consequences of fasting were globally less marked. Pancreatic juice secretion in the duodenum was transiently lowered while pancreas protein and enzymes were transiently increased.

The late post-weaning phase (day 5-15) corresponded to an adaptation of the gut to the weaning diet. The main factors of this adaptation were the re-feeding process and time, independently of the diet composition. Maturation was the major feature of the ileum. Duodenal structural characteristics, and more generally the weight characteristics of the gut could be considered as valuable gut health criteria. Variables measuring functional activities of the ileal mucosa could be considered as gut maturation criteria.

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