Changes of the glutathione redox system during the weaning transition in piglets, in relation to small intestinal morphology and barrier function

Abstract

Background: Weaning is known to result in barrier dysfunction and villus atrophy in the immediate post-weaning phase, and the magnitude of these responses is hypothesized to correlate with changes in the glutathione (GSH) redox system. Therefore, these parameters were simultaneously measured throughout the weaning phase, in piglets differing in birth weight category and weaning age, as these pre-weaning factors are important determinants for the weaning transition. Low birth weight (LBW) and normal birth weight (NBW) littermates were assigned to one of three weaning treatments; i.e. weaning at 3 weeks of age (3w), weaning at 4 weeks of age (4w) and removal from the sow at 3 d of age and fed a milk replacer until weaning at 3 weeks of age (3d3w). For each of these treatments, six LBW and six NBW piglets were euthanized at 0, 2, 5, 12 or 28 d post-weaning piglets, adding up 180 piglets. Results: Weaning increased the glutathione peroxidase activity on d 5 post-weaning in plasma, and duodenal and jejunal mucosa. Small intestinal glutathione-S-transferase activity gradually increased until d 12 post-weaning, and this was combined with a progressive rise of mucosal GSH up till d 12 post-weaning. Oxidation of the GSH redox status (GSH/GSSG E h) was only observed in the small intestinal mucosa of 3d3w weaned piglets at d 5 postweaning. These piglets also demonstrated increased fluorescein isothiocyanate dextran (FD4) and horseradish peroxidase fluxes in the duodenum and distal jejunum during the experiment, and specifically demonstrated increased FD4 fluxes at d 2 to d 5 post-weaning. On the other hand, profound villus atrophy was observed during the weaning transition for all weaning treatments. Finally, LBW and NBW piglets did not demonstrate notable differences in GSH redox status, small intestinal barrier function and histo-morphology throughout the experiment. Conclusion: Although moderate changes in the GSH redox system were observed upon weaning, the GSH redox status remained at a steady state level in 3w and 4w weaned piglets and was therefore not associated with weaning induced villus atrophy. Conversely, 3d3w weaned piglets demonstrated GSH redox imbalance in the small intestinal mucosa, and this co-occurred with a temporal malfunction of their intestinal barrier function.

Early step-down weaning of dairy calves from a high milk volume with glutamine supplementation

“…Our LMR revealed that an aggressive restriction of milk can increase PPE in calves, agreeing with increased PPE observed for feed restrictions in mature cows (Kvidera et al, 2017). Our results also highlighted a lag time (4-7 d) for the PPE response, which is in agreement with Degroote et al (2020). Those authors assessed PPE in the small intestine of weaned piglets and did not see a PPE increment until 5 d postweaning.…”

“…Those authors assessed PPE in the small intestine of weaned piglets and did not see a PPE increment until 5 d postweaning. Degroote et al (2020) also showed a markedly induced oxidative damage to the intestinal mucosa that was closely in line with the PPE response for weaning. Perhaps, the Gln supplementation mitigated the potential increase in PPE by alleviating oxidative damage to the intestinal mucosa of weaning calves (Ji et al, 2019).…”

“…Moreover, Duttlinger et al (2020) demonstrated a potential to replace antibiotics with Gln to alleviate weaning and transportation stresses. Data on weaning piglets indicate that Gln can positively affect intestinal health and development by improving the intestinal barrier function (Potsic et al, 2002;Qin et al, 2018), mitigating intestinal atrophy (Wu et al, 1996), and optimizing the redox status of the epithelium (Degroote et al, 2020). Because the physiology of neonatal calves is close to piglets, and van Keulen et al (2020) showed improved intestinal morphology for a Gln supplement in preweaning calves, similar effects of Gln on gut health can be assumed for weaning calves.…”

Dietary supplementation with potassium-magnesium sulfate modulates the antioxidant capacity, immunity, and gut microbiota in weaned piglets

“…Weaning stress leads to the excessive production of oxygen free radicals, resulting in lipid peroxidation and damage to the structure and function of biofilm ( Cao et al, 2018 ; Degroote et al, 2020 ; Novais et al, 2021 ). A previous study reported that the exogenous addition of magnesium can alleviate the decrease of GSH-Px activity in mitochondria of premature aging mice caused by oxidative stress ( Villa-Bellosta, 2020 ).…”

Effect of Weaning at 21 Days of Age on the Content of Bile Acids in Chyme of Cecum

“…The intestine is not only the largest digestive and absorption organ in animals, but also the largest immune organ in the body, and early weaning can affect intestinal health [ 5 , 6 ]. At present, there are more studies on the effect of weaning on piglets’ intestines, mainly focusing on the intestinal barrier, intestinal permeability, and the structure and diversity of microbiota in the intestine [ 7 , 8 ]. Bile acids (BAs), as metabolites of intestinal microorganisms, can promote nutrient absorption and play an important role in the regulation of intestinal physiology, and they are of great interest as participants in the metabolic pathway of the “hepatic-intestinal cycle” in animals [ 9 , 10 ].…”