Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2014 Heat stress alters animal physiology and post- absorptive metabolism during pre- and postnatal development Jay Steven Johnson Iowa State University Follow this and additional works at:https://lib.dr.iastate.edu/etd Part of theAgriculture Commons,Animal Sciences Commons,Human and Clinical Nutrition Commons, and thePhysiology Commons Recommended Citation Johnson, Jay Steven, "Heat stress alters animal physiology and post-absorptive metabolism during pre- and postnatal development" (2014).Graduate Theses and Dissertations. 13982. https://lib.dr.iastate.edu/etd/13982 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please [email protected]. Heat stress alters animal physiology and post-absorptive metabolism during pre- and postnatal development by Jay Steven Johnson A dissertation submitted to the graduate faculty in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Major: Nutritional Sciences Program of Study Committee: Lance H. Baumgard, Major Professor Donald C. Beitz John F. Patience Jason W. Ross Hongwei Xin Iowa State University Ames, Iowa 2014 Copyright © Jay Steven Johnson, 2014. All rights reserved. ii TABLE OF CONTENTS LIST OF TABLES............................................................................................................ vi LIST OF FIGURES.......................................................................................................... ix LIST OF ABBREVIATIONS......................................................................................... xiii ACKNOWLEDGEMENTS............................................................................................. xv ABSTRACT.................................................................................................................... xvi CHAPTER I. LITERATURE REVIEW............................................................................ 1 Introduction......................................................................................................... 1 Global Impact of Heat Stress.............................................................................. 2 Climate Change....................................................................................... 2 Economic and Food Security Impacts of Heat Stress............................. 2 Heat-Related Illnesses in Humans and Animals..................................... 3 Management Strategies to Reduce Heat Load........................................ 4 Nutritional Strategies to Reduce Heat Load........................................... 5 Direct and Indirect Effects of Heat Stress.............................................. 7 Thermoregulatory Response to Heat Stress....................................................... 9 Thermoregulation................................................................................... 9 Conductive Exchange................................................................. 10 Convective Exchange................................................................. 11 Radiative Exchange.................................................................... 12 Evaporation............................................................................................. 13 Respiration.............................................................................................. 14 Feed Intake.................................................................................................. 15 Van’t Hoff Arrhenius Equation and the Q Effect................................. 16 10 Adaptation and Acclimation................................................................... 17 Nutrient Metabolism and Partitioning................................................................ 18 Carbohydrates......................................................................................... 19 Digestion and Absorption........................................................... 19 Synthesis and Oxidation............................................................. 20 Heat Stress and Carbohydrate Metabolism............................................ 21 Protein..................................................................................................... 24 Digestion and Absorption........................................................... 24 Synthesis and Degradation.......................................................... 25 Heat Stress and Protein Metabolism....................................................... 28 Lipid........................................................................................................ 30 Digestion and Absorption........................................................... 30 Synthesis and Oxidation............................................................. 31 Heat Stress and Lipid Metabolism.......................................................... 33 Bioenergetics........................................................................................... 35 Porcine Tissue Accretion ....................................................................... 36 Prenatal Insults.................................................................................................... 37 Epigenetics.............................................................................................. 38 Maternal Heat Stress............................................................................... 39 iii Maternal Nutrient Restriction................................................................. 41 Elevated Maternal Glucocorticoids......................................................... 43 Summary............................................................................................................. 45 Literature cited.................................................................................................... 47 CHAPTER II: EFFECTS OF MAMMALIAN IN UTERO HEAT STRESS ON ADOLESCENT BODY TEMPERATURE...................................................................... 66 Abstract........................................................................................................................... 66 Introduction..................................................................................................................... 67 Materials and Methods.................................................................................................... 68 Gestational Environments................................................................................... 68 Adolescent Environments................................................................................... 69 Statistics.............................................................................................................. 70 Results............................................................................................................................. 71 Thermal Indices................................................................................................... 71 Regression Analysis............................................................................................ 72 Growth Parameters.............................................................................................. 72 Discussion....................................................................................................................... 73 Conclusion...................................................................................................................... 77 References....................................................................................................................... 79 CHAPTER III: IN UTERO HEAT STRESS INCREASES POSTNATAL CORE BODY TEMPERATURE IN PIGS.................................................................................. 88 Abstract............................................................................................................................. 88 Introduction....................................................................................................................... 89 Materials and Methods...................................................................................................... 90 In utero environments........................................................................................... 90 Postnatal environments......................................................................................... 91 Blood sampling and analysis................................................................................ 93 Statistics................................................................................................................ 94 Results............................................................................................................................... 97 Thermal indices..................................................................................................... 97 Core temperature....................................................................................... 97 Respiration rate......................................................................................... 98 Skin temperature....................................................................................... 98 Growth parameters................................................................................................ 99 Blood parameters.................................................................................................. 99 Discussion....................................................................................................................... 100 Perspectives and significance......................................................................................... 105 References....................................................................................................................... 107 iv CHAPTER IV: EFFECTS OF IN UTERO HEAT STRESS AND CORE BODY TEMPERATURE ON TISSUE ACCRETION DURING THE GROWING PHASE (30 TO 60 KG) IN PIGS................................................................................... 120 Abstract........................................................................................................................... 120 Introduction..................................................................................................................... 121 Materials and Methods.................................................................................................... 122 In utero environments......................................................................................... 122 Postnatal environments....................................................................................... 123 Blood sampling and analysis.............................................................................. 124 Serial slaughter and sub-sample analysis............................................................ 125 Statistical analysis............................................................................................... 127 Results............................................................................................................................. 128 Thermal indices.................................................................................................. 128 Growth performance........................................................................................... 128 Organ and carcass weight................................................................................... 129 Tissue composition and accretion....................................................................... 129 Blood analysis..................................................................................................... 129 Discussion....................................................................................................................... 130 Conclusion...................................................................................................................... 136 References....................................................................................................................... 137 CHAPTER V: IN UTERO HEAT STRESS ALTERS BODY COMPOSITION DURING THE EARLY FINISHING PHASE (60 TO 80 KG) IN PIGS....................... 152 Abstract........................................................................................................................... 152 Introduction..................................................................................................................... 153 Materials and Methods.................................................................................................... 155 In utero environments......................................................................................... 155 Postnatal environments....................................................................................... 155 Blood sampling and analysis.............................................................................. 157 Serial slaughter and sub-sample analysis............................................................ 158 Statistical analysis............................................................................................... 159 Results............................................................................................................................. 160 Thermal indices................................................................................................... 160 Growth performance........................................................................................... 160 Organ and carcass weight................................................................................... 161 Tissue composition and accretion....................................................................... 162 Blood analysis..................................................................................................... 162 Discussion....................................................................................................................... 163 Conclusion...................................................................................................................... 169 References....................................................................................................................... 171 v CHAPTER VI: THE IMPACT OF IN UTERO HEAT STRESS AND NUTRIENT RESTRICTION ON PROGENY BODY COMPOSITION........................................... 186 Abstract........................................................................................................................... 186 Introduction..................................................................................................................... 187 Materials and Methods.................................................................................................... 189 Maternal environment......................................................................................... 189 Postnatal environment......................................................................................... 190 Tissue collection................................................................................................. 191 Histology............................................................................................................. 191 Statistics.............................................................................................................. 191 Results............................................................................................................................. 192 Maternal phase.................................................................................................... 192 Thermal indices....................................................................................... 192 Growth variables..................................................................................... 192 Offspring variables.............................................................................................. 193 Growth.................................................................................................... 193 Tissue composition and accretion........................................................... 193 Organ and tissue weights........................................................................ 194 Histology................................................................................................. 195 Discussion....................................................................................................................... 195 Perspectives and significance......................................................................................... 199 References....................................................................................................................... 202 CHAPTER VII: SUMMARY......................................................................................... 218 APPENDIX..................................................................................................................... 223 vi LIST OF TABLES Table 1.1: Symptoms of heat-related illnesses from mild (1) to severe (5)...................... 4 Table 1.2: Euthermic rectal temperature (T ) of multiple species.................................. 10 re Table 1.3: The impact of heat stress (HS) on dry matter intake (DMI) of various species.................................................................................................................. 16 Table 1.4: Glucose transporters and their function......................................................... 20 Table 1.5: The impact of heat stress on parameters of carbohydrate metabolism.......... 23 Table 1.6: The impact of heat stress on blood biomarkers of proteolysis...................... 29 Table 1.7: The impact of heat stress on biomarkers of lipid metabolism....................... 34 Table 1.8: The impact of in utero heat stress on postnatal phenotypes.......................... 41 Table 1.9: Phenotypic consequences of maternal nutrient restriction exposure during early, mid, and late gestation................................................................................. 42 Table 1.10: The impact of in utero glucocorticoids on postnatal phenotypes................ 45 Table 2.1: Effects of gestational and adolescent thermal environments on body temperature indices in growing pigs................................................................................. 83 Table 2.2: Effects of gestational and adolescent thermal environments on production parameters in growing pigs............................................................................. 84 Table 3.1: Effects of in utero heat stress on core body temperature in growing pigs... 112 Table 3.2: Effects of in utero heat stress on thermoregulation parameters in growing pigs.................................................................................................................... 113 Table 3.3: Effects of in utero heat stress on growth parameters in growing pigs.................................................................................................................................. 114 Table 3.4: Effects of postnatal heat stress on bioenergetic parameters in growing pigs.................................................................................................................................. 115 Table 4.1: Ingredients and chemical composition of diet for growing pigs (as-fed basis)............................................................................................................................... 144 Table 4.2: Effect of in utero and postnatal environment on growth parameters in growing pigs............................................................................................................... 145 vii Table 4.3: Effect of in utero and postnatal environment on carcass and organ weights of growing pigs.................................................................................................. 146 Table 4.4: Effect of in utero and postnatal environment on tissue accretion in growing pigs.................................................................................................................... 147 Table 4.5: Effect of in utero and postnatal environment on blood parameters in growing pigs.................................................................................................................... 148 Table 5.1: Ingredients and chemical composition of diet for growing pigs (as-fed basis)............................................................................................................................... 179 Table 5.2: Effect of in utero and postnatal environment on growth parameters in growing pigs.................................................................................................................... 180 Table 5.3: Effect of in utero and postnatal environment on carcass and organ weights of growing pigs.................................................................................................. 181 Table 5.4: Effect of in utero and postnatal environment on carcass composition and tissue accretion in growing pigs............................................................................... 182 Table 5.5: Effect of in utero and postnatal environments on blood parameters in growing pigs.................................................................................................................... 183 Table 6.1: Effect of environmental treatment on maternal variables............................ 208 Table 6.2: Effect of in utero environment on rat offspring growth.............................. 209 Table 6.3: Effect of in utero environment on postnatal body composition in rat offspring.......................................................................................................................... 210 Table 6.4: Effect of in utero environment on postnatal tissue accretion in rat offspring.......................................................................................................................... 211 Table 6.5: Effect of in utero environment on postnatal carcass components in rat offspring.......................................................................................................................... 212 Table 7.1: The biological consequences of heat stress.................................................. 222 Table A-3.1. Ingredients and chemical composition of diet for growing pigs (as-fed basis)................................................................................................................... 223 Table A-3.2: Effects of in utero heat stress on bioenergetic parameters in pigs........... 224 Table A-6.1. Relevant nutrient content of Harlan 2018 rodent diet (as-fed basis)........ 225 viii Table A-6.2: Effect of in utero environment on bioenergetic variables of fasted rats.................................................................................................................................. 226 ix LIST OF FIGURES Figure 1.1: Protein turnover............................................................................................ 28 Figure 1.2: Lipogenesis................................................................................................... 32 Figure 1.3: Schematic of energy utilization.................................................................... 36 Figure 2.1: Effects of gestational and adolescent thermal environments on the temporal changes in respiration rate, rectal temperature (T ), and T averaged by re re gestational and adolescent environment in growing pigs................................................. 85 Figure 2.2: Effects of gestational and adolescent thermal environments on the temporal changes in ear skin temperature, shoulder skin temperature, rump skin temperature and tail skin temperature in growing pigs................................................... 86 Figure 2.3: Linear regression (y = mx +b) of respiration rate as a function of rectal temperature for gestational thermal neutral and gestational heat stress exposed pigs, regardless of adolescent environment............................................................................. 87 Figure 3.1: Ambient temperature (T ) by day of study................................................. 116 a Figure 3.2: Effects of in utero environment on the temporal changes in core body temperature (T ) averaged by in utero treatment and day of study in growing core pigs.................................................................................................................................. 117 Figure 3.3: Linear regression (y = mx + b) of core temperature (T ) as a function core of hour (0800-1500h)...................................................................................................... 118 Figure 3.4: Effects of in utero environment on the temporal changes in feed intake (kg) averaged by in utero treatment and day of study in growing pigs............... 119 Figure 4.1: Effects of in utero and postnatal thermal environments on (A) respiration rate (RR), and (B) rectal temperature (T ) averaged by in utero and postnatal re environment in growing pigs.......................................................................................... 149 Figure 4.2: Effect of postnatal thermal environments on protein accretion (g/d) and adipose accretion (g/d) in growing pigs.......................................................................... 150 Figure 4.3: Linear regression (y = mx + b) of (A) average daily gain (ADG) as a function of feed intake (FI), (B) protein accretion (g/d) as a function of FI, (C) adipose accretion (g/d) as a function of FI, and (D) the ratio of adipose to protein accretion/d as a function of FI........................................................... 151