Physiological responses of Holstein calves to heat stress and dietary supplementation with a postbiotic from Aspergillus oryzae

Abstract

Increased ambient temperature causes heat stress in mammals, which affects physiological and molecular functions. We have recently reported that the dietary administration of a postbiotic from Aspergillus oryzae (AO) improves tolerance to heat stress in fruit flies and cattle. Furthermore, heat-induced gut dysfunction and systemic inflammation have been ameliorated in part by nutritional interventions. The objective of this study was to characterize the phenotypic response of growing calves to heat stress compared to thermoneutral ad libitum fed and thermoneutral feed-restricted counterparts and examining the physiologic alterations associated with the administration of the AO postbiotic to heat-stressed calves with emphasis on intestinal permeability. In this report, we expand previous work by first demonstrating that heat stress reduced partial energetic efficiency of growth in control (45%) but not in AO-fed calves (62%) compared to thermoneutral animals (66%). While heat stress increased 20% the permeability of the intestine, AO postbiotic and thermoneutral treatments did not affect this variable. In addition, AO postbiotic reduced fecal water content relative to thermoneutral and heat stress treatments. Heat stress increased plasma concentrations of serum amyloid A, haptoglobin and lipocalin-2, and administration of AO postbiotic did not ameliorate this effect. In summary, our findings indicated that heat stress led to reduced nutrient-use efficiency and increased systemic inflammation. Results suggest that the AO postbiotic improved energy-use efficiency, water absorption, and the intestinal permeability in heat stress-mediated increase in gut permeability but did not reduce heat stress-mediated rise in markers of systemic inflammation.

Figure 1

Mean (A) and maximum (B) rectal temperature of Holstein bull calves. Results denote least squares means + standard error of the mean (TN thermoneutral, TNR thermoneutral feed-restricted, HS heat stress, HSP heat stress and dietary supplementation with 3 g of AO postbiotic; n = 8 per treatment). P ≤ 0.01 denoted by *(compared against TN), ^#(compared against TNR), or ∞ (compared against HS). (A) Mean rectal temperature in HSP treatment differs compared with TN, TNR, or HS; treatment by h interaction (P < 0.001). Mean rectal temperature in TNR treatment differs compared with TN. (B) Maximal rectal temperature of HS and HSP treatments differ compared with TN and TNR. Mean respiration rate (C) of HS and HSP treatments differ compared with TN and TNR; treatment by day interaction (P < 0.001). Mean respiration rate (D) of HS and HSP treatments differ compared with TN and TNR; treatment by day interaction (P < 0.001).

Figure 2

(A) Mean rectal temperature and (B) respiration rate of Holstein bull calves exposed to thermoneutral (TN), thermoneutral feed-restricted (TNR), heat stress (HS), and heat stress and dietary supplementation with 3 g of AO postbiotic (HSP) plotted against ambient temperature (n = 8 per treatment). Linear relationship is denoted in rectal temperature for HS and HSP, 37.05 + 0.07x (R² = 0.30) and 37.12 + 0.06x (R² = 0.28), with ambient temperature (P < 0.0001). (B) Linear relationship is shown in respiration rate for HS and HSP, 39.1 − 4.2x (R² = 0.59) and 37.1 − 4.1x (R² = 0.65), with ambient temperature (P < 0.0001). (C) Linear relationship is shown in respiration rate for HS and HSP, − 1485 + 40x (R² = 0.52) and − 1469 + 39.6x (R² = 0.59), and rectal temperature (P < 0.0001). Dark gray shaded area shows the 95% mean confidence interval and the (dashed lines) light gray represent the 95% prediction limits.

Figure 3

(A) HS and HSP treatments increased plasma glucose concentrations (treatment by day interaction; P < 0.005; SEM = 7.47 mg/dL; TN thermoneutral, TNR thermoneutral feed-restricted, HS heat stress, HSP heat stress and dietary supplementation with 3 g of AO postbiotic; n = 8 Holstein bull calves per treatment). (B) HS and HSP treatments increased plasma NEFA concentrations (treatment by day interaction; P < 0.033; SEM = 0.021 mM). (C) The TNR treatment decreased plasma PUN concentrations (13.8 mg/dL) relative to HS, HSP, and TN (P ≤ 0.007). (D) Plasma l-lactate concentrations were not affected by treatments (SEM = 0.07 mM).