Endocrine And Metabolic Adaptations Of Calves To Extra-Uterine Life

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Abstract

The transition from intra- to extra-uterine life is one of the greatest physiological challenges that occur in the life of animals. Immediately after birth, newborn calves have to adapt to new environmental and feeding conditions. Namely, at birth a break of the thermal balance occurs, since calves abruptly pass from a 38.8°C temperature in utero to an environmental temperature that is generally lower than 20°C. Additionally, at birth, the energy intake shifts from a continuous parenteral supply of nutrients (mainly glucose) to discontinuous colostrum and milk intake with lactose and fat as the main energy sources. Therefore, the most important issues related to metabolic changes during the transition from intra- to extra-uterine life are related to maintaining the homoeothermic conditions and control of energy metabolism. Those metabolic adaptations are under control of the endocrine system that is relatively mature at birth, but still requires morphological and functional changes after birth. Key hormones whose concentrations are significantly changed around birth and are involved in an adequate adaptation of calves to extra-uterine life are those related to stress at birth (cortisol and cathecholamines), glucoregulatory processes (insulin and glucagon), thermogenesis (thyroid hormones) and growth (IGF axis).

1. Mee JF: Newborn dairy calf management. Vet Clin North Am 2008, 24:1–17.

2. Silva del Río N, Stewart S, Rapnicki P, Chang YM, Fricke PM: An observational analysis of twin births, calf sex ratio, and calf mortality in Holstein dairy cattle. J Dairy Sci 2007, 90:1255–1264.

3. Uetake K: Newborn calf welfare: a review focusing on mortality rates. Anim Sci J 2013, 84(2):101-105.

4. Raboisson D, Delor F, Cahuzac E, Gendre C, Sans P, Allaire G: Perinatal, neonatal, and rearing period mortality of dairy calves and replacement heifers in France. J Dairy Sci 2013, 96(5):2913-2924.

5. USDA, Heifer Calf Health and Management Practices on U.S. Dairy Operations, USDA:APHIS:VS, CEAH. Fort Collins, CO; 2007.

6. MacFarlane JA, Grove-White DH, Royal MD, Smith RF: Identification and quantification of factors affecting neonatal immunological transfer in dairy calves in the UK, Vet Rec 2015, 176(24):625.

7. Cortese VS: Neonatal immunology. Vet Clin North Am Food Anim Pract 2009, 25(1):221-227.

8. Chase CC, Hurley DJ, Reber AJ: Neonatal immune development in the calf and its impact on vaccine response. Vet Clin North Am Food Anim Pract 2008, 24(1):87-104.

9. Sangild PT: Uptake of colostral immunoglobulins by the compromised newborn farm animal. Acta Vet Scand Suppl 2003, 98:105-122.

10. Weaver DM, Tyler JW, VanMetre DC, Hostetler DE, Barrington GM: Passive transfer of colostral immunoglobulins in calves. J Vet Intern Med 2000, 14(6):569-577.

11. Hammon HM, Steinhoff-Wagner J, Schönhusen U, Metges CC, Blum JW: Energy metabolism in the newborn farm animal with emphasis on the calf: endocrine changes and responses to milk-born and systemic hormones. Domest Anim Endocrinol 2012, 43(2):171-185.

12. Blum JW, Hammon H: Endocrine and metabolic aspects in milk-fed calves. Domest Anim Endocrinol 1999, 17(2-3):219-230.

13. Vannucchi CI, Rodrigues JA, Silva LC, Lúcio CF, Veiga GA, Furtado PV, Oliveira CA, Nichi M: Association between birth conditions and glucose and cortisol profiles of periparturient dairy cows and neonatal calves. Vet Rec 2015, 176(14):358.

14. Chung HR: Adrenal and thyroid function in the fetus and preterm infant. Korean J Pediatr 2014, 57(10):425-433.

15. Aurich JE, Dobrinski I, Petersen A, Grunert E, Rausch WD, Chan WW: Influence of labor and neonatal hypoxia on sympathoadrenal activation and methionine enkephalin release in calves. Am J Vet Res 1993, 54(8):1333-1338.

16. Donkin SS, Armentano LE: Regulation of gluconeogenesis by insulin and glucagon in the neonatal bovine. Am J Physiol 1994, 266:1229-1237.

17. Mullur R, Liu YY, Brent GA: Thyroid hormone regulation of metabolism. Physiol Rev 2014, 94(2):355-382.

18. Blum JW, Baumrucker CR: Insulin-like growth factors (IGFs), IGF binding proteins, and other endocrine factors in milk: role in the newborn. Adv Exp Med Biol 2008, 606:397-422.

19. Yang K, Fraser M, Yu M, Krkosek M, Challis JR, Lamming GE, Campbell LE, Darnel A: Pattern of 11 beta-hydroxysteroid dehydrogenase type 1 messenger ribonucleic acid expression in the ovine uterus during the estrous cycle and pregnancy. Biol Reprod 1996, 55(6):1231-1236.

20. Pepe GJ, Burch MG, Albrecht ED: Localization and developmental regulation of 11 beta-hydroxysteroid dehydrogenase-1 and -2 in the baboon syncytiotrophoblast. Endocrinology 2001, 142(1):68-80.

21. Steinhoff-Wagner J, Görs S, Junghans P, Bruckmaier RM, Kanitz E, Metges CC, Hammon HM: Maturation of endogenous glucose production in preterm and term calves. J Dairy Sci 2011, 94(10):5111-5123.

22. Plas C, Nunez J: Role of cortisol on the glycogenolytic effect of glucagon and on glycogenic response to insulin in fetal hepatocytes culture. J Biol Chem 1976, 251:1431-1437

23. Stojić V, Nikolić JA, Huszenicza Gy, Šamanc H, Gvozdić D, Kirovski D: Plasma levels of triiodothyronine, thyroxine and cortisol in newborn calves. Acta Veterinaria Beograd 2002, 52:5-6.

24. Grosvenor CE, Picciano MF, Baumrucker CR: Hormones and growth factors in milk. Endocr Rev 1993, 14(6):710-728.

25. Padbury JF, Ervin MG, Polk DH: Extrapulmonary effects of antenatally administered steroids. J Pediatr 1996, 128:167–172.

26. Sauter SN, Roffler B, Philipona C, Morel C, Romé V, Guilloteau P, Blum JW, Hammon HM: Intestinal development in neonatal calves: effects of glucocorticoids and dependence of colostrum feeding. Biol Neonate 2004, 85(2):94-104.

27. Franko KL, Giussani DA, Forhead AJ, Fowden AL, Effects of dexamethasone on the glucogenic capacity of fetal, pregnant, and non-pregnant adult sheep. J Endocrinol 2007, 192(1):67-73.

28. Girard JR, Caquet D, Guillet I: Control of rat liver phosphorylase, glucose-6-phosphatase and phosphophenolphyruvate carboxykinase activities by insulin and glucagon during the perinatal period. Enzyme 1973, 15:272-285.

29. Gluckman PD, Sizonenko SV, Bassett NS: The transition from fetus to neonate: an endocrine perspective. Acta Paediatr Suppl 1999, 428:7-11.

30. Godfrey RW, Smith SD, Guthrie MJ, Stanko RL, Neuendorff DA, Randel RD: Physiological responses of newborn Bos indicus and Bos indicus x Bos taurus calves after exposure to cold. J Anim Sci 1991, 69(1):258-63.

31. Newnham JP, Marshall CL, Padbury JF, Lam RV, Hobel CJ, Fisher DA: Fetal catecholamine release with preterm delivery. Am J Obstet Gynecol 1984, 149:888-893.

32. Cheung CY: Fetal adrenal medulla catecholamine response to hypoxia-direct and neural components. Am J Physiol 1990, 258:1340-1346.

33. Stein H, Oyama K, Martinez A, Chappel B, Padbury J: Plasma epinephrine appearance and clearance rates in fetal and newborn sheep. Am J Physiol 1993, 265:756-760.

34. Richet E, Davicco MJ, Barlet JP: Plasma catecholamine concentrations in lambs and calves during the perinatal period. Reprod Nutr Dev 1985, 25:1007-1016.

35. Sperling MA, Ganguli S, Leslie N, Landt K: Fetal-perinatal catecholamine secretion: role in perinatal glucose homeostasis. Am J Physiol 1984, 247:69-74.

36. Davidson D: Circulating vasoactive substances and hemodynamic adjustments at birth in lambs. J Appl Physiol 1987, 63:676-684.

37. Himms-Hagen J: Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB J 1990, 4(11):2890-2898.

38. Limesand SW, Rozance PJ, Smith D, Hay WW. Increased insulin sensitivity and maintenance of glucose utilizationm rates in fetal sheep with placental insufficiency and intra-uterine growth restriction. Am J Physiol Endocrinol Metab 2007, 293:1716-1725.

39. Gao F, Liu Y, Li L, Li M, Zhang C, Ao C, Hou X. Effects of maternal undernutrition during late pregnancy on the development and function of ovine fetal liver. Anim Reprod Sci 2014, 147(3-4):99-105.

40. Gadhia MM, Maliszewski AM, O’Meara MC, Thorn SR, Lavezzi JR, Limesand SW, Hay WW Jr, Brown LD, Rozance PJ: Increased amino acid supply potentiates glucose-stimulated insulin secretion but does not increase β-cell mass in fetal sheep. Am J Physiol Endocrinol Metab 2013, 304(4):352-362.

41. Ford SP, Zhang L, Zhu M, Miller MM, Smith DT, Hess BW, Moss GE, Nathanielsz PW, Nijland MJ: Maternal obesity accelerates fetal pancreatic beta-cell but not alpha-cell development in sheep: prenatal consequences. Am J Physiol Regul Integr Comp Physiol 2009, 297(3):835-843.

42. Alexander DP, Assan R, Britton HG, Fenton E, Redstone D: Glucagon release in the sheep fetus. 1) Effect of hypo- and hyperglycaemia and arginine. Biol Neonate 1976, 30:1-10.

43. Kirovski D, Lazarević M, Baričević-Jones I, Nedić O, Masnikosa R, Nikolić JA: Effects of peroral insulin and glucose on circulating insulin-like growth factor-I, its binding proteins and thyroid hormones in neonatal calves. Can J Vet Res 2008, 72(3):253-258.

44. Kawai Y, Arinze IJ: Activation of Glycogenolysis in Neonatal Liver. J Biol Chem 1981, 256 (2):853-858.

45. Donkin SS, Bertics SJ, Armentano LE: Chronic and transitional regulation of gluconeogenesis and glyconeogenesis by insulin and glucagon in neonatal calf hepatocytes. J Anim Sci 1997, 75(11):3082-3087.

46. Charron MJ, Vuguin PM: Lack of glucagon receptor signaling and its implications beyond glucose homeostasis. J Endocrinol 2015, 224(3):123-130.

47. Philippidis H, Ballard FJ: The development of gluconeogenesis in rat liver. Effects of glucagon and ether. Biochem J 1970, 120(2):385-392.

48. Grütter R, Blum JW: Insulin and glucose in neonatal calves after peroral insulin and intravenous glucose administration. Reprod Nutr Dev 1991,31(4):389-397.

49. Prodanović R, Kirovski D, Vujanac I, Đurić M, Korićanac G, Vranješ-Đurić S, Ignjatović M, Šamanc H: Insulin responses to acute glucose infusions in Buša and Holstein-Friesian cattle breed during the peripartum period: comparative study. Acta Veterinaria Beograd 2013, 63 (2-3): 373-384.

50. Fisher DA: Thyroid system immaturities in very low birth weight premature infants. Semin Perinatol 2008, 32:387-397.

51. Breall JA, Rudolph AM, Heymann MA: Role of thyroid hormone in postnatal circulatory and metabolic adjustments. J Clin Invest 1984, 73:1418-1424.

52. Davicco MJ, Vigouroux E, Dardillat C, Barlet JP: Thyroxine, triiodothyronine and iodide in different breeds of newborn calves. Reprod Nutr Dev 1982, 22(2):355-362.

53. Grongnet JF, Grongnet-Pinchon E, Witowski A: Neonatal levels of plasma thyroxine in male and female calves fed a colostrum or immunoglobulin diet or fasted for the first 28 hours of life. Reprod Nutr Dev 1985, 25(3):537-543.

54. Annunziata M, Granata R, Ghigo E: The IGF system. Acta Diabetol 2011, 48(1):1-9.

55. Baxter RC: Insulin-like growth factor binding proteins in human circulation: a review. Horm Res 1994, 42:140-144.

56. Elhddad AS, Lashen H: Fetal growth in relation to maternal and fetal IGF-axes: a systematic review and meta-analysis. Acta Obstet Gynecol Scand 2013, 92(9):997-1006.

57. Mullis PE, Tonella P: Regulation of fetal growth: consequences and impact of being born small. Best Pract Res Clin Endocrinol Metab 2008, 22(1):173-190.

58. Soos MA, Navé BT, Siddle K: Immunological studies of type I IGF receptors and insulin receptors: characterisation of hybrid and atypical receptor subtypes. Adv Exp Med Biol 1993, 343:145-157.

59. Owens JA: Endocrine and substrate control of fetal growth: placental and maternal influences and insulin-like growth factors. Reprod Fertil Dev 1991, 3(5):501-517.

60. Bang P, Westgren M, Schwander J, Blum WF, Rosenfeld RG, Stangenberg M: Ontogeny of insulin-like growth factor-binding protein-1, -2, and -3: quantitative measurements by radioimmunoassay in human fetal serum. Pediatr Res 1994, 36(4):528-536.

61. Holt RI: Fetal programming of the growth hormone-insulin-like growth factor axis. Trends Endocrinol Metab 2002, 13(9):392-397.

62. Hyatt MA, Walker DA, Stephenson T, Symonds ME: Ontogeny and nutritional manipulation of the hepatic prolactin-growth hormone-insulin-like growth factor axis in the ovine fetus and in neonate and juvenile sheep. Proc Nutr Soc 2004, 63(1):127-135.

63. Rajaram S, Baylink DJ, Mohan S: Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr Rev 1997, 18(6):801-831.

64. Cordano P, Hammon HM, Morel C, Zurbriggen A, Blum JW: mRNA of insulin-like growth factor (IGF) quantification and presence of IGF binding proteins, and receptors for growth hormone, IGF-I and insulin, determined by reverse transcribed polymerase chain reaction, in the liver of growing and mature male cattle. Domest Anim Endocrinol 2000, 19(3):191-208.

65. Sauter SN, Ontsouka E, Roffler B, Zbinden Y, Philipona C, Pfaffl M, Breier BH, Blum JW, Hammon HM: Effects of dexamethasone and colostrum intake on the somatotropic axis in neonatal calves. Am J Physiol Endocrinol Metab 2003, 285(2):252-261.

66. Brameld JM, Gilmour RS, Buttery PJ: Glucose and amino acids interact with hormones to control expression of insulin-like growth factor-I and growth hormone receptor mRNA in cultured pig hepatocytes. J Nutr 1999,129:1298–1306.

67. McGuire MA, Dwyer DA, Harrell RJ, Bauman DE: Insulin regulates circulating insulin-like growth factors and some of their binding proteins in lactating cows. Am J Physiol 1995, 269:723–730.

68. Kirovski D, Lazarević M, Stojić V, Šamanc H, Vujanac I, Nedić O, Masnikosa R: Hormonal status and regulation of glycemia in neonatal calves dutring the first hours of postnatal life. Acta Veterinaria Beograd 2011, 61(4): 349-361.

69. Morovat A, Dauncey MJ: Effects of thyroid status on insulin-like growth factor-I, growth hormone and insulin are modified by food intake. Eur J Endocrinol 1998, 138(1):95-103.

70. Owens PC, Conlon MA, Campbell RG, Johnson RJ, King R, Ballard FJ: Developmental changes in growth hormone, insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in plasma of young growing pigs. J Endocrinol 1991, 128(3):439-447.

71. Baxter RC, Martin JL: Binding proteins for insulin-like growth factors in adult rat serum. Comparison with other human and rat binding proteins. Biochem Biophys Res Commun 1987, 147(1):408-415.

72. Binoux M: The IGF system in metabolism regulation. Diabete Metab 1995, 21(5):330-337.

73. Murphy LJ: The role of the insulin-like growth factors and their binding proteins in glucose homeostasis. Exp Diabesity Res 2003, 4(4):213-224.

74. Collett-Solberg PF, Cohen P: The role of the insulin-like growth factor binding proteins and the IGFBP proteases in modulating IGF action: Endocrinol Metab Clin North Am 1996, 25(3):591-614.

75. Bae JH, Song DK, Im SS: Regulation of IGFBP-1 in Metabolic Diseases. J Lifestyle Med 2013, 3(2):73-79.

76. Skaar TC, Baumrucker CR, Deaver DR, Blum JW: Diet effects and ontogeny of alterations of circulating insulin-like growth factor binding proteins in newborn dairy calves. J Anim Sci 1994, 72(2):421-427.

77. Underwood LE, Thissen JP, Lemozy S, Ketelslegers JM, Clemmons DR: Hormonal and nutritional regulation of IGF-I and its binding proteins. Horm Res 1994, 42(4-5):145-151.

78. Godden S: Colostrum management for dairy calves. Vet Clin North Am Food Anim Pract 2008, 24(1):19-39.

79. Stelwagen K, Carpenter E, Haigh B, Hodgkinson A, Wheeler TT: Immune components of bovine colostrums and milk. J Anim Sci 2009, 87 (13): 3-9.

80. Šamanc H, Sladojević Ž, Vujanac I, Prodanović R, Kirovski M, Dodovski P, Kirovski D: Relationship between growth of nursing pigs and composition of sow colostrum and milk from anterioar and posterior mammary glands. Acta veterinaria Beograd 2013, 63(5-6):537-548.

81. Trajčev M, Nakov D, Hristov S, Andonov S, Joksimović-Todorović M: Clinical mastitis in Macedonian dairy herds. Acta veterinaria Beograd 2013, 63(1):63-76.

82. Maletić M, Vakanjac S, Djelić N, Lakić N, Pavlović M, Nedić S, Stanimirović Z: Analysis of lactoferrin gene polymophism and its association to milk quality and mammary gland health in holstein-friesian cows. Acta veterinaria Beograd 2013, 63(5-6):487-498.

83. Kirovski D, Nikolić JA, Stojić V: Serum levels of inuslin-like growth factor I and total protein in newborn calves offered different amounts of colostrum. Acta Veterinaria Beograd 2002, 52(5-6): 285-298.

84. Hammon H, Blum JW: The somatotropic axis in neonatal calves can be modulated by nutrition, growth hormone, and Long-R3-IGF-I. Am J Physiol 1997, 273:130-138.

85. Vacher PY, Bestetti G, Blum JW: Insulin-like growth factor I absorption in the jejunum of neonatal calves. Biol Neonate 1995, 68(5):354-367.

86. Guilloteau P, Zabielski R, Blum JW: Gastrointestinal tract and digestion in the young ruminant: ontogenesis, adaptations, consequences and manipulations. J Physiol Pharmacol 2009, 60 (3):37-46.

87. Heinrichs C, Yanovski JA, Roth AH, Yu YM, Domené HM, Yano K, Cutler B Jr, Baron J: Dexamethasone increases growth hormone receptor messenger ribonucleic acid levels in liver and growth plate. Endocrinology 1994,135: 1113-1118.

88. Baumrucker CR, Hadsell DL, Blum JW: Effects of dietary insulin-like growth factor I on growth and insulin-like growth factor receptors in neonatal calf intestine. J Anim Sci 1994, 72(2):428-433.

89. Egli CP, Blum JW: Clinical, haematological, metabolic and endocrine traits during the first three months of life of suckling simmentaler calves held in a cow-calf operation. Zentralbl Veterinarmed A 1998, 45(2):99-118.

90. Livingstone C, Borai A: Insulin-like growth factor-II: its role in metabolic and endocrine disease. Clin Endocrinol (Oxf) 2014, 80(6):773-781.

91. McGowen JE, Aldoreta PW, Hay WW Jr: Contribution of fructose and lactate produced in placenta to circulation of fetal glucose oxidation rate. Am J Physiol 1995, 269 (5 Pt 1): E834-839.

92. Hillman NH, Kallapur SG, Jobe AH: Physiology of transition from intrauterine to extrauterine life. Clin Perinatol 2012, 39(4):769-783.

93. Comline RS, Silver M: Some aspects of foetal and uteroplacental metabolism in cows with indwelling umbilical and uterine vascular catheters. Physiol 1976, 260(3):571-586.

94. Gu W, Jones CT, Harding JE: Metabolism of glucose by fetus and placenta of sheep. The effects of normal fluctuations in uterine blood flow. J Dev Physiol 1987, 9(4):369-389.

95. Fowden AL, Mapstone J, Forhead AJ: Regulation of glucogenesis by thyroid hormones in fetal sheep during late gestation. J Endocrinol 2001, 170(2):461-469.

96. Liang L, Guo WH, Esquiliano DR, Asai M, Rodriguez S, Giraud J, Kushner JA, White MF, Lopez MF: Insulin-like growth factor 2 and the insulin receptor, but not insulin, regulate fetal hepatic glycogensynthesis. Endocrinology 2010, 151(2):741-747.

97. Fowden AL, Forhead AJ: Adrenal glands are essential for activation of glucogenesis during undernutrition in fetal sheep near term. Am J Physiol Endocrinol Metab 2011, 300(1):94-102.

98. Stratford LL, Hooper SB: Effect of hypoxemia on tissue glycogen content and glycolytic enzyme activities in fetal sheep. Am J Physiol 1997, 272:103-110.

99. Fowden AL, Mijovic J, Ousey JC, McGladdery A, Silver M: The development of gluconeogenic enzymes in the liver and kidney of fetal and newborn foals. J Dev Physiol 1992, 18(3):137-142.

100. Houin SS, Rozance PJ, Brown LD, Hay WW Jr, Wilkening RB, Thorn SR: Coordinated changes in hepatic amino acid metabolism and endocrine signals support hepatic glucose production during fetal hypoglycemia. Am J Physiol Endocrinol Metab 2015, 308(4):306-314.

101. Scheuer BH, Zbinden Y, Schneiter P, Tappy L, Blum JW, Hammon HM: Effects of colostrum feeding and glucocorticoid administration on insulin-dependent glucose metabolism in neonatal calves. Domest Anim Endocrinol 2006, 31(3):227-245.

102. Edwards AV, Silver M: The glycogenolytic response to stimulation of the splanchnic nerves in adrenalectomized calves. J Physiol 1970, 211(1):109-124.

103. Power GG, Yoneyama Y, Asakura H, Sawa R: Disappearance of palmitic acid from plasma of fetal and newborn sheep. J Appl Physiol 1993, 74(1):62-67.

104. Hammon HM, Steinhoff-Wagner J, Flor J, Schönhusen U, Metges CC: Lactation Biology Symposium: role of colostrum and colostrum components on glucose metabolism in neonatal calves. J Anim Sci 2013, 91(2):685-695.

105. Hammon HM, Philipona C, Zbinden Y, Blum JW, Donkin SS: Effects of dexamethasone and growth hormone treatment on hepatic gluconeogenic enzymes in calves. J Dairy Sci 2005, 88(6):2107-2116.

106. Keller HL, Gherman LI, Kosa RE, Borger DC, Weiss WP, Willett LB: Kinetics of plasma fructose and glucose when lactose and fructose are used as energy supplements for neonatal calves. J Anim Sci 1998, 76(8):2197-204.

107. Steinhoff-Wagner J, Görs S, Junghans P, Bruckmaier RM, Kanitz E, Metges CC, Hammon HM: Intestinal glucose absorption but not endogenous glucose production differs between colostrum- and formula-fed neonatal calves. J Nutr 2011, 141(1):48-55.

108. Hammon HM, Sauter SN, Reist M, Zbinden Y, Philipona C, Morel C, Blum JW: Dexamethasone and colostrum feeding affect hepatic gluconeogenic enzymes differently in neonatal calves. J Anim Sci 2003, 81(12):3095-3106.

109. Lepine AJ, Boyd RD, Whiteheat DM: Effect of colostrum intake on hepatic gluconeogenesis and fatty acid oxidation in neonatal pig. J Anim Sci 1991, 69 (5): 1966-1974.

110. Rauprich AB, Hammon HM, Blum JW: Effects of feeding colostrum and a formula with nutrient contents as colostrum on metabolic and endocrine traits in neonatal calves. Biol Neonate 2000, 78(1):53-64.

111. Schäff CT, Rohrbeck D, Steinhoff-Wagner J, Kanitz E, Sauerwein H, Bruckmaier RM, Hammon HM: Effects of colostrum versus formula feeding on hepatic glucocorticoid and α1- and β2-adrenergic receptors inneonatal calves and their effect on glucose and lipid metabolism. J Dairy Sci 2014, 97(10):6344-6357.

112. Hocquette JF, Bauchart D: Intestinal absorption, blood transport and hepatic and muscle metabolism of fatty acids in preruminant and ruminant animals. Reprod Nutr Dev 1999, 39(1):27-48.

113. Smith SB, Crouse JD: Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J Nutr 1984, 114(4):792-800.

114. Lammoglia MA, Bellows RA, Short RE, Bellows SE, Bighorn EG, Stevenson JS, Randel RD: Body temperature and endocrine interactions before and after calving in beef cows. J Anim Sci 1997, 75(9):2526-2534.

115. Carstens GE: Cold thermoregulation in the newborn calf. Vet Clin North Am Food Anim Pract 1994, 10(1):69-106.

116. Robinson JB, Young BA: Metabolic heat production of neonatal calves during hypothermia and recovery. J Anim Sci 1988, 66(10):2538-44.

117. Labussière E, van Milgen J, de Lange CF, Noblet J: Maintenance energy requirements of growing pigs and calves are influenced by feeding level. J Nutr 2011, 141(10):1855-1861.

118. Zanker IA, Hammon HM, Blum JW: Delayed feeding of first colostrum: are there prolonged effects on haematological, metabolic and endocrine parameters and on growth performance in calves?. J Anim Physiol Anim Nutr (Berl) 2001, 85(3-4):53-66.

119. Koldovský O, Dobiásová M, Drahota Z, Hahn P: Developmental aspects of lipid metabolism. Physiol Res 1995, 44(6):353-356.

120. Smith SB, Carstens GE, Randel RD, Mersmann HJ, Lunt DK: Brown adipose tissue development and metabolism in ruminants. J Anim Sci 2004, 82(3):942-954.

121. Casteilla L, Forest C, Robelin J, Ricquier D, Lombet A, Ailhaud G: Characterization of mitochondrial-uncoupling protein in bovine fetus and newborn calf. Am J Physiol 1987, 252:627-636.

122. Himms-Hagen J, Cui J, Lynn Sigurdson S: Sympathetic and sensory nerves in control of growth of brown adipose tissue: Effects of denervation and of capsaicin. Neurochem Int 1990,17(2):271-279.

123. Giralt M, Casteilla L, Viñas O, Mampel T, Iglesias R, Robelin J, Villarroya F: Iodothyronine 5′-deiodinase activity as an early event of prenatal brown-fat differentiation in bovine development. Biochem J 1989, 259(2):555-559.

124. Khedoe PP, Hoeke G, Kooijman S, Dijk W, Buijs JT, Kersten S, Havekes LM, Hiemstra PS, Berbée JF, Boon MR, Rensen PC: Brown adipose tissue takes up plasma triglycerides mostly after lipolysis. J Lipid Res 2015, 56(1):51-59.

125. Alexander G: Quantitive development of adipose tissue in fetal sheep. Aust J Biol Sci 1978, 31: 489-503.

126. Alexander G: Body temperature control in mammalian young. Br Med Bull 1975, 31(1):62-8.

127. Trayhurn P, Thomas ME, Keith JS: Postnatal development of uncoupling protein, uncoupling protein mRNA, and GLUT4 in adipose tissues of goats. Am J Physiol 1993, 265:676-682.

128. Trayhurn P, Thomas ME, Duncan JS, Nicol F, Arthur JR: Presence of the brown fat-specific mitochondrial uncoupling protein and iodothyronine 5′-deiodinase activity in subcutaneous adipose tissue of neonatal lambs. FEBS Lett 1993, 322(1):76-78.

129. Holloway BR, Davidson RG, Freeman S, Wheeler H, Stribling D: Post-natal development of interscapular (brown) adipose tissue in the guinea pig: effect of environmental temperature. Int J Obes 1984, 8(4):295-303.

130. Restelli L, Lecchi C, Invernizzi G, Avallone G, Savoini G, Ceciliani F: UCP1 and UCP2 expression in different subcutaneous and visceral adipose tissue deposits in 30 days old goat kids and effect of fatty acid enriched diets. Res Vet Sci 2015, 100:131-137.

131. Vermorel M, Dardillat C, Vernet J, Saido, Demigne C: Energy metabolism and thermoregulation in the newborn calf. Ann Rech Vet 1983,14(4):382-389.

132. Herpin P, Le Dividich J, Van Os M: Contribution of colostral fat to thermogenesis and glucose homeostasis in the newborn pig. J Dev Physiol 1992, 17(3):133-141.

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