Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs

Abstract

Excessive heat exposure reduces intestinal integrity and post-absorptive energetics that can inhibit wellbeing and be fatal. Therefore, our objectives were to examine how acute heat stress (HS) alters intestinal integrity and metabolism in growing pigs. Animals were exposed to either thermal neutral (TN, 21°C; 35-50% humidity; n=8) or HS conditions (35°C; 24-43% humidity; n=8) for 24 h. Compared to TN, rectal temperatures in HS pigs increased by 1.6°C and respiration rates by 2-fold (P<0.05). As expected, HS decreased feed intake by 53% (P<0.05) and body weight (P<0.05) compared to TN pigs. Ileum heat shock protein 70 expression increased (P<0.05), while intestinal integrity was compromised in the HS pigs (ileum and colon TER decreased; P<0.05). Furthermore, HS increased serum endotoxin concentrations (P=0.05). Intestinal permeability was accompanied by an increase in protein expression of myosin light chain kinase (P<0.05) and casein kinase II-α (P=0.06). Protein expression of tight junction (TJ) proteins in the ileum revealed claudin 3 and occludin expression to be increased overall due to HS (P<0.05), while there were no differences in claudin 1 expression. Intestinal glucose transport and blood glucose were elevated due to HS (P<0.05). This was supported by increased ileum Na(+)/K(+) ATPase activity in HS pigs. SGLT-1 protein expression was unaltered; however, HS increased ileal GLUT-2 protein expression (P=0.06). Altogether, these data indicate that HS reduce intestinal integrity and increase intestinal stress and glucose transport.

Figure 1. The effects of 24 hours of either constant thermal neutral conditions (TN; 21°C) or heat stress conditions (HS; 35°C) on a) rectal temperature, b) respiration rates, c) cumulative feed intake, and d) change in body weight in growing pigs.

^a,b P<0.05, n = 8/trt.

Figure 2. Heat stress augments ileum protein expression of TJ protein regulatory machinery; a) Myosin light chain kinase (MLCK), b) Casein kinase (CK) II-α, c) c-Src, and d) Mast cell tryptase (MCT) in growing pigs.

Pigs were exposed for 24 hours to either constant thermal neutral conditions (TN; 21°C) or heat stress conditions (HS; 35°C). n = 8/trt.

Figure 3. Heat stress conditions (HS; 35°C) increases serum endotoxin compared to pigs reared in thermal neutral conditions (TN; 21°C) for 24 hours.

^a,b P<0.05, n = 8/trt.

Figure 4. Heat stress conditions (HS; 35°C) alters expression and localization of TJ proteins compared to pigs reared in thermal neutral conditions (TN; 21°C) for 24 hours.

Supplemental figure in support of Table 2.

Figure 5. The effects of 24 hours of either constant thermal neutral conditions (TN; 21°C) or heat stress conditions (HS; 35°C) on a) blood glucose, b) active glucose transport, c) GLUT-2 expression, and d) SGLT-1 expression in growing pigs.

n = 8/trt.

Figure 6. Heat stress conditions (HS; 35°C) increase Na⁺/K⁺ ATPase activity compared to pigs reared in thermal neutral conditions (TN; 21°C) for 24 hours.

^a,b P<0.05, n = 8/trt.

Figure 7. The effects of 24 hours of either constant thermal neutral conditions (TN; 21°C) or heat stress conditions (HS; 35°C) on a) mucosal HSP70 expression or b) mucosal HIF-1α protein expression in growing pigs.

^a,b P<0.05, n = 8/trt.