Long-term impacts of late-gestation maternal heat stress on growth performance, blood hormones and metabolites of newborn calves independent of maternal reduced feed intake

https://doi.org/10.1016/j.domaniend.2019.106433Get rights and content

Highlights

  • Maternal heat stress could impair immune function of the offspring in bovine but its effect was not independent of maternal reduced feed intake.

  • Maternal exposure to heat stress negatively affects birth body weight and height of dairy calves, independent of maternal reduced feed intake.

  • The starter feed intake and weight gain are less critical in terms of detrimental effects of prenatal heat stress.

Abstract

The objective of this study was to evaluate the effects of heat stress in late gestation independent of maternal reduced feed intake on performance, blood hormones and metabolites, and immune responses of dairy calves from birth through weaning. A total of 30 multiparous Holstein cows at 45 d before expected calving were randomly assigned to one of 3 groups: (1) thermal neutral (CL, n = 10) conditions with ad libitum feed intake (10% of refusals on an as-fed basis); (2) pair-fed thermal neutral (CLPF, n = 10) conditions to reduce feed intake to levels similar to the heat stress (HS) group while reared under thermoneutral conditions (80% of the CL group); or (3) heat stress (HS, n = 10) conditions with ad libitum feed intake. Pair-feeding was conducted to quantify the confounding effects of dissimilar feed intake. Calves (10/group) born to cows that were exposed to cooling (IU-CL), pair-feeding (IU-CLPF), or heat stress (IU-HS) were used from birth through weaning. After birth, all the calves were managed under identical conditions. IU-HS calves had lower birth weight, and hip height at birth and 14 d of age. Compared with IU-CL and IU-CLPF calves, IU-HS calves had lower serum concentration of IgG and apparent efficiency of IgG absorption but higher serum insulin concentrations. Cortisol concentration in serum was higher in IU-HS and IU-CLPF calves compared to IU-CL calves. The neutrophil percentage was lower in IU-CL calves than in IU-HS and IU-CLPF calves. Neutrophil-lymphocyte ratio was higher in IU-HS calves compared to IU-CLPF and IU-CL calves. The mRNA expression of TNFα of IU-HS calves was downregulated compared with IU-CL and IU-CLPF calves. In summary, maternal HS during late gestation reduces calf birth weight and dramatically alters blood hormones and metabolites, but its effect on immune system function was not independent of maternal reduced feed intake.

Introduction

Heat stress (HS) induces behavioral and metabolic changes in cattle exposed to HS conditions to reduce feed intake, activity, and metabolic rate in an attempt to reduce internal metabolic heat production [1]. However, HS during pregnancy not only is affecting the performance of the cow but also can likely cause impaired performance of calves later in life [[2], [3], [4]]. In utero (IU) HS can have a lasting imprint on offspring growth, behavior, and metabolism and was shown to also impair the future HS response in a study that used pigs [5]. Programming results from adaptive alterations in gene expression patterns that occur in response to stressors and causes altered growth of specific organs and systems during their most critical time of development [6].

The IU exposure of calves to HS has been shown to induce fetal growth retardation by decreasing uterine blood flow [7] and placental weight [8]. In dairy cattle, calves born to cows under HS during late gestation were lighter at birth and through puberty [2,9,10], exhibited compromised passive immunity [2,3], and expressed lower peripheral blood mononuclear cell proliferation [2] compared to those born to cooled cows. Maternal HS also alters the inflammatory response of calves in early life [11]. Strong et al [4] reported that in utero HS calves had decreased mRNA expression of tumor necrosis factor α (TNF α) and toll-like receptor 2 (TLR2) compared with control calves. A recent study on the role of epigenetic modifications in developmental programming reported that maternal HS alters the DNA methylation of key regulatory gene pathways in the liver and mammary gland and programs their morphology in postnatal life, which may contribute to the reduced performance of prenatally heat stressed calves [12].

Heat stress has been widely shown to compromise feed intake of dairy cows [13] and many of the changes due to HS appear to be directly mediated by reduced feed consumption. Although the importance of late gestation HS has been documented in dairy calves, studies investigating the impacts of maternal HS independent of reduced feed intake are limited. Thus, the objectives of the present study were to investigate the effects of maternal HS independent of maternal reduced feed intake on growth performance, blood metabolites and hormones, and mRNA expression of genes involved in immune responses in Holstein dairy calves. Our hypothesis was that maternal HS independent of reduced feed intake during late gestation alters offspring growth, metabolic and hormonal responses from birth through weaning.

Section snippets

Materials and methods

The present study was conducted from 45 d before calving until 2 wk after weaning of calves, according to the guidelines of the Iranian Council of Animal Care [14] in a commercial dairy farm (ETKA Agri. Dairy Production Co., Gorgan, Iran), located 46 km from North of Gorgan, Iran (37° 8′ 2.98″ N 54° 37′ 8.73″ E), between August and December, 2017.

Prepartum period

Figure 1 represents the minimum, average, and maximum THI data during the prenatal period (45 d before birth) and postnatal life (birth to 2 wk after weaning). Heat-stressed cows had a higher RT (39.37 ± 0.32 vs 38.84 ± 0.30 and 38.77 ± 0.61°C; P < 0.01), and respiratory rate (81.58, vs 62.20 and 62.04 breaths/min; P < 0.01) than CLPF and CL cows. As compared with the CL cows (mean ± SD), heat-stressed cows showed reduced (P < 0.01) DMI during the experiment (12.37 ± 1.58 vs 10.47 ± 1.08 kg/d,

Discussion

All dry cows in our experiment were exposed to the same environmental HS during the prepartum period, but according to our results, the evaporative cooling system improved RT and respiratory rate of CL cows. These differences in physiological indicators of HS suggest that the experimental model produced a maternal uterine environment with hyperthermia [2], and therefore, an effective HS and undernutrition were achieved. In the present study, calves exposed to IU HS had a significantly lower

Conclusions

In conclusion, maternal HS significantly impairs the birth weight of neonate calves independent of reduced maternal feed intake. Calves from CL cows, independent of reduced maternal feed intake, were larger and had more IgG in the circulation compared with those calves born to heat-stressed cows. Maternal HS during the dry period reduced the AEA of immunoglobulins in the neonatal calves, but its effect was not independent of maternal reduced feed intake. The results from the metabolic variables

CRediT authorship contribution statement

S.M.M. Seyed. Almoosavi: Conceptualization, Data curation, Writing - original draft. T. Ghoorchi: Conceptualization, Investigation, Supervision. A.A. Naserian: Conceptualization, Investigation, Supervision. S.S. Ramezanpor: Methodology. M.H. Ghaffari: Writing - review & editing.

Acknowledgments

This work was funded by Gorgan University of Agricalture and Natural Resources (Gorgan, Iran). The authors would like to thank ETKA's Agricultural, Animal Husbandry and Fishery CO. (Gorgan, Iran) for their skillful assistance and excellent technical support. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

S.M.M. Seyed Almoosavi was a visiting Ph.D. student at the Institute of Animal Science, Physiology and Hygiene Unit,

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