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Perinatal Programming of Adult Metabolic Homeostasis

Lessons From Experimental Studies

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Early Life Origins of Health and Disease

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 573))

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Abstract

Poor fetal growth and associated neonatal catch-up growth are independent risk factors for metabolic disease in later life. Epidemiological studies in humans consistently show associations of small size at birth and later glucose intolerance and/or diabetes. A primary defect is thought to be insulin resistance, which is associated with both small size at birth and neonatal catch-up growth. The available evidence suggests that this resistance may result from a signalling defect downstream of the insulin receptor in peripheral tissues. Recent evidence also suggests that insulin secretion may be impaired in the individual who was small at birth. Most of the contemporary data in humans relates later outcomes to size at birth rather than to specific exposures. Experimental models that restrict fetal growth or produce variation in size at birth have therefore been used to explore these associations between small size at birth, neonatal catch-up growth and later metabolic disease. In this chapter we will review what has been learnt from human and experimental studies about the mechanistic basis for poor metabolic homeostasis following restricted fetal growth and neonatal catch-up growth, and comment on future directions in this area.

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References

  1. Fagot-Campagna A. Emergence of type 2 diabetes mellitus: Epidemiological evidence. J Pediatr Endocrinol Metab 2000; 13:1395–402.

    PubMed  Google Scholar 

  2. Aye T, Levitsky LL. Type 2 diabetes: An epidemic disease in childhood. Curr Opin Pediatrics 2003; 15:411–15.

    Google Scholar 

  3. Schulze MB, Hu FB. Primary prevention of diabetes: What can be done and how much can be prevented? Annu Rev Public Health 2005, (Review in advance: Doi: 10.1146/annurev.publhealth.26.021304.144532).

    Google Scholar 

  4. Parker L, Lamont DW, Unwin N et al. A lifecourse study of risk for hyperinsulinaemia, dyslipidaemia and obesity (the central metabolic syndrome) at age 49–51 years. Diabet Med 2003; 20:406–15.

    PubMed  CAS  Google Scholar 

  5. Newsome CA, Shiell AW, Fall CHD et al. Is birth weight related to later glucose and insulin metabolism?-a systemic review. Diabet Med 2003; 20:339–48.

    PubMed  CAS  Google Scholar 

  6. Rogers I, Group E-BS. The influence of birthweight and intrauterine environment on adiposity and fat distribution in later life. Int J Obes Relat Metab Disord 2003; 27:755–77.

    PubMed  CAS  Google Scholar 

  7. Pi-Sunyer FX. The epidemiology of central fat distribution in relation to disease. Nutr Rev 2004; 62:S120–S26.

    PubMed  Google Scholar 

  8. Robinson JS, Owens JA. Pathophysiology of intrauterine growth failure. In: Gluckman PD, Heymann MA, eds. Pediatrics and Perinatology. The Scientific Basis. 2nd ed. London: Arnold, 1996:290–97.

    Google Scholar 

  9. Fitzhardinge PM, Steven EM. The small-for-date infant I. Later growth patterns. Pediatrics 1972; 49:671–81.

    PubMed  CAS  Google Scholar 

  10. Tenovuo A, Kero P, Piekkala P et al. Growth of 519 small for gestational age infants during the first two years of life. Acta Paediatrica Scandinavica 1987; 76:636–46.

    PubMed  CAS  Google Scholar 

  11. Albertsson-Wikland K, Wennergren G, Wennergren M et al. Longitudinal follow-up of growth in children born small for gestational age. Acta Paediatrica 1993; 82:438–43.

    PubMed  CAS  Google Scholar 

  12. Hokken-Koelega ACS, De Ridder MAJ, Lemmen RJ et al. Children born small for gestational age: Do they catch up? Pediatric Res 1995; 38:267–71.

    CAS  Google Scholar 

  13. Crowther NJ, Cameron N, Trusler J et al. Association between poor glucose tolerance and rapid post natal weight gain in seven-year-old children. Diabetologia 1998; 41:1163–67.

    PubMed  CAS  Google Scholar 

  14. Forsén T, Eriksson J, Tuomilehto J et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med 2000; 133:176–82.

    PubMed  Google Scholar 

  15. Ong KKL, Ahmed ML, Emmett PM et al. Association between postnatal catch-up growth and obesity in childhood: Prospective cohort study. BMJ 2000; 320:967–71.

    PubMed  CAS  Google Scholar 

  16. Parsons TJ, Power C, Manor O. Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: Longitudinal study. BMJ 2001; 323:1331–35.

    PubMed  CAS  Google Scholar 

  17. Eriksson JG, Forsen T, Tuomilehto J et al. Catch-up growth in childhood and death from coronary heart diesase: Longitudinal study. BMJ 1999; 318:427–31.

    PubMed  CAS  Google Scholar 

  18. Forsén T, Eriksson JG, Tuomilehto J et al. Growth in utero and during childhood among women who develop coronary heart disease: Longitudinal study. BMJ 1999; 319:1403–07.

    PubMed  Google Scholar 

  19. Barker DJP. Mothers, babies and health in later life. 2nd ed. Edinburgh: Churchill Livingstone, 1998.

    Google Scholar 

  20. Lucas A. Programming by early nutrition in man. In: Bock GR, Whelan J, eds. The Childhood Environment and Adult Disease. Chicester: Wiley, 1991:38–55.

    Google Scholar 

  21. Barker DJP, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986; 1(8489):1077–81.

    PubMed  CAS  Google Scholar 

  22. Rich-Edwards JW, Stampfer MJ, Manson JE et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 1997; 315:396–400.

    PubMed  CAS  Google Scholar 

  23. Rich-Edwards JW, Colditz GA, Stampfer MJ et al. Birthweight and the risk for type 2 diabetes mellitus in adult women. Ann Intern Med 1999; 130:322–24.

    Google Scholar 

  24. Ravelli G-P, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Eng J Med 1976; 295:349–53.

    CAS  Google Scholar 

  25. Ravelli ACJ, ven der Meulen JHP, Osmond C et al. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 1999; 70:811–16.

    PubMed  CAS  Google Scholar 

  26. Ravelli ACJ, van der Meulen JHP, Michels RPJ et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 1998; 351:173–77.

    PubMed  CAS  Google Scholar 

  27. Flanagan DE, Vaile JC, Petley GW et al. The autonomic control of heart rate and insulin resistance in young adults. J Clin Endocrinol Metab 1999; 84:1263–67.

    PubMed  CAS  Google Scholar 

  28. Fowden AL, Hill DJ. Intra-uterine programming of the endocrine pancreas. British Medical Bulletin 2001; 60:123–42.

    PubMed  CAS  Google Scholar 

  29. Ozanne SE, Nave BT, Wang CL et al. Poor fetal nutrition causes long-term changes in expression of insulin-signaling components in adipocytes. Am J Physiol 1997; 273:E46–E51.

    PubMed  CAS  Google Scholar 

  30. Fowden AL, Forhead AJ. Endocrine mechanisms of intrauterine programming. Reproduction 2004; 127:515–26.

    PubMed  CAS  Google Scholar 

  31. Gluckman PD, Hanson MA. Living with the past: Evolution, development, and patterns of disease. Science 2004; 305:1733–36.

    PubMed  CAS  Google Scholar 

  32. Bergman RN, Ader M, Huecking K et al. Accurate assessment of β-cell function. The hyperbolic correction. Diabetes 2002; 51(Suppl 1):S212–S20.

    PubMed  CAS  Google Scholar 

  33. Veening MA, van Weissenbruch MM, Heine RJ et al. β-cell capacity and insulin sensitivity in prepubertal children born small for gestational age. Influence of body size during childhood. Diabetes 2003; 52:1756–60.

    PubMed  CAS  Google Scholar 

  34. Whincup PH, Cook DG, Adshead F et al. Childhood size is more closely related than size at birth to glucose and insulin levels in 10–11-year-old children. Diabetologia 1997; 40:319–26.

    PubMed  CAS  Google Scholar 

  35. Soto N, Bazaes RA, Pena V et al. Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: Results from a prospective cohort. J Clin Endocrinol Metab 2003; 88:3645–50.

    PubMed  CAS  Google Scholar 

  36. Phillips DIW. Relation of fetal growth to adult muscle mass and glucose tolerance. Diabet Med 1995; 12:686–90.

    PubMed  CAS  Google Scholar 

  37. Moore VM, Davies MJ, Willson KJ et al. Dietary composition of pregnant women is related to size of the baby at birth. J Nutrition 2004; 134:1820–26.

    CAS  Google Scholar 

  38. Clapp JFR. Maternal carbohydrate intake and pregnancy outcome. Proc Nutr Soc 2002; 61:45–50.

    PubMed  Google Scholar 

  39. Battaglia FC. Fetal liver and the placenta: An interactive system. In: Battaglia FC, ed. Placental Function and Fetal Nutrition. Philadelphia: Lippincott-Raven Publishers, 1997:47–57.

    Google Scholar 

  40. Meschia G. Placental delivery of amino acids. Utilization and production vs. transport. In: Battaglia FC, ed. Placental Function and Fetal Nutrition. Philadelphia: Lippincott-Raven Publishers, 1997:21–30.

    Google Scholar 

  41. Helmerhorst FM, Perquin DA, Donker D et al. Perinatal outcome of singletons and twins after assisted conception: A systematic review of controlled studies. BMJ 2004; 328:261.

    PubMed  Google Scholar 

  42. Jackson RA, Gibson KA, Wu YW et al. Perinatal outcomes in singletons following in vitro fertilization: A meta-analysis. Obstet Gynecol 2004; 103:551–63.

    PubMed  Google Scholar 

  43. Ghazi HA, CS, Kallen B. Delivery outcome after infertility — a registry study. Fertil Steril 1991; 55(4):726–32.

    PubMed  CAS  Google Scholar 

  44. Holemans K, Verhaeghe J, Dequeker J et al. Insulin sensitivity in adult female rats subjected to malnutrition during the perinatal period. J Soc Gynecol Investig 1996; 3:71–77.

    PubMed  CAS  Google Scholar 

  45. Woodall SM, Breier BH, Johnston BM et al. A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: Effects on the somatotrophic axis and postnatal growth. J Endocrinol 1996; 150:231–42.

    PubMed  CAS  Google Scholar 

  46. Woodall SM, Johnston BM, Breier BH et al. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res 1996; 40:438–43.

    PubMed  CAS  Google Scholar 

  47. Vickers MH, Breier BH, Cutfield WS et al. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol 2000; 279(1):E83–E87.

    CAS  Google Scholar 

  48. Kind KL, Clifton PM, Katsman AI et al. Restricted fetal growth and the response to dietary cholesterol in the guinea pig. Am J Physiol 1999; 277:R1675–R82.

    PubMed  CAS  Google Scholar 

  49. Kind KL, Clifton PM, Grant PA et al. Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am J Physiol 2003; 284:R140–R52.

    CAS  Google Scholar 

  50. Jones AP, Friedman MI. Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science 1982; 215:1518–19.

    PubMed  CAS  Google Scholar 

  51. Jones AP, Simson EL, Friedman MI. Gestational undernutrition and the development of obesity in rats. J Nutrition 1984; 114:1484–92.

    CAS  Google Scholar 

  52. Portha B, Kergoat M, Blondel O et al. Underfeeding of rat mothers during the first two trimesters of gestation does not alter insulin action and insulin secretion in the progeny. Eur J Endocrinol 1995; 133:475–82.

    PubMed  CAS  Google Scholar 

  53. Szitanyi P, Hanzlova J, Poledne R. Influence of intrauterine undernutrition on the development of hypercholesterolemia in an animal model. Physiological Res 2000; 49(6):721–24.

    CAS  Google Scholar 

  54. Garofano A, Czernichow P, Bréant B. In utero undernutrition impairs rat beta-cell development. Diabetologia 1997; 40:1231–34.

    PubMed  CAS  Google Scholar 

  55. Garofano A, Czernichow P, Bréant B. Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat. Diabetologia 1998; 41:1114–20.

    PubMed  CAS  Google Scholar 

  56. Bertin E, Gangnerau MN, Bailb D et al. Glucose metabolism and beta-cell mass in adult offspring of rats protein and/or energy restricted during the last week of pregnancy. Am J Physiol 1999; 277:E11–E17.

    PubMed  CAS  Google Scholar 

  57. Ashwell M, Purkins L, Cowen T et al. Pre and postnatal development of adipose tissue at four sites in the guinea pig: Effect of maternal diet restriction during the second half of pregnancy. Ann Nutr Metab 1987; 31:197–210.

    PubMed  CAS  Google Scholar 

  58. Oliver MH, Breier BH, Gluckman PD et al. Birth weight rather than maternal nutrition influences glucose tolerance, blood pressure, and IGF-I levels in sheep. Pediatr Res 2002; 52(4):516–24.

    PubMed  CAS  Google Scholar 

  59. McLeod KI, Goldrick RB, Whyte HM. The effect of maternal malnutrition on the progeny of the rat. Aust J Exp Biol Med Sci 1972; 50:435–46.

    PubMed  CAS  Google Scholar 

  60. Dahri S, Snoeck A, Reusens-Billen B et al. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 1991; 40(suppl 2):115–20.

    PubMed  CAS  Google Scholar 

  61. Langley SC, Browne RF, Jackson AA. Altered glucose tolerance in rats exposed to maternal low protein diets in utero. Comp Biochem Physiol 1994; 109A:223–29.

    CAS  Google Scholar 

  62. Lucas A, Baker BA, Desai M et al. Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutrition 1996; 76:605–12.

    CAS  Google Scholar 

  63. Muaku SM, Beauloye V, Thissen J-P et al. Long-term effects of gestational protein malnutrition on postnatal growth, insulin-like growth factor (IGF)-I, and IGF-binding proteins in rat progeny. Pediatr Res 1996; 39:649–55.

    PubMed  CAS  Google Scholar 

  64. Hales CN, Desai BM, Ozanne SE et al. Fishing in the stream of diabetes: From measuring insulin to the control of fetal organogenesis. Biochem Soc Trans 1996; 24:341–50.

    PubMed  CAS  Google Scholar 

  65. Ozanne SE, Smith GD, Tikerpae J et al. Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am J Physiol 1996; 2701:E559–E64.

    Google Scholar 

  66. Ozanne SE, Wang CL, Coleman N et al. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol 1996; 271:E1128–E34.

    PubMed  CAS  Google Scholar 

  67. Sugden MC, Holness MJ. Gender-specific programming of insulin secretion and action. J Endocrinol 2002; 175:757–67.

    PubMed  CAS  Google Scholar 

  68. Horton DM, Kind KL, Thavaneswaran P et al. Large size at birth and neonatal catch-up growth independently predict increased adiposity and reduced muscle mass in the guinea pig. Paper presented at: Perinatal Society of Australia and New Zealand 6th Annual Congress. New Zealand: Christchurch, 2002.

    Google Scholar 

  69. Horton DM, Kind KL, Walker MR et al. Fetal growth restriction and accelerated postnatal growth independently predict insulin resistance in the adult guinea pig. Am J Physiol 2005; in press.

    Google Scholar 

  70. Poore K, Fowden AL. The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 2002; 45:1247–54.

    PubMed  CAS  Google Scholar 

  71. Poore K, Fowden AL. Insulin sensitivity in juvenile and adult Large White pigs of low and high birthweight. Diabetologia 2004; 47:340–48.

    PubMed  CAS  Google Scholar 

  72. Greenwood PL, Hunt AS, Hermanson JW et al. Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. J Anim Sci 1998; 76:2354–67.

    PubMed  CAS  Google Scholar 

  73. Greenwood PL, Hunt AS, Slepetis RM et al. Effects of birth weight and postnatal nutrition on neonatal sheep: III. Regulation of energy metabolism. J Anim Sci 2002; 80:2850–61.

    CAS  Google Scholar 

  74. Gatford KL, Clarke IJ, De Blasio MJ et al. Perinatal growth and plasma GH profiles in adolescent and adult sheep. J Endocrinol 2002; 173:151–59.

    PubMed  CAS  Google Scholar 

  75. De Blasio MJ, Gatford KL, Fielke SL et al. Placental restriction of fetal growth reduces size at birth and increases postnatal growth and adiposity in the young lamb. Am J Physiol 2005; in press.

    Google Scholar 

  76. Gatford KL, De Blasio MJ, Walker M et al. Restriction of placental and fetal growth impairs insulin secretory capacity in the sheep postnatally. Paper presented at: 12th International Congress of Endocrinology. Portugal: Lisbon, 2004.

    Google Scholar 

  77. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 2001; 50:2279–86.

    PubMed  CAS  Google Scholar 

  78. Gelardi NL, Cha C-JM, Oh W. Glucose metabolism in adipocytes of obese offspring of mild hyperglycemic rats. Pediatr Res 1990; 28:641–45.

    PubMed  CAS  Google Scholar 

  79. Holemans K, van Bree R, Verhaeghe J et al. Maternal semistarvation and streptozotocin-diabetes in rats have different effects on the in vivo glucose uptake by peripheral tissues in their female adult offspring. J Nutr 1997; 127:1371–76.

    PubMed  CAS  Google Scholar 

  80. Weintrob N, Karp M, Hod M. Short-and long-range complications in offspring of diabetic mothers. Journal of Diabetes and its Complications 1996; 10(5):294–301.

    PubMed  CAS  Google Scholar 

  81. Moss TJM, Sloboda DM, Gurrin LC et al. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol 2001; 281:R960–R70.

    CAS  Google Scholar 

  82. Crowther C, Harding J. Repeat doses of prenatal corticosteroids for women at risk of preterm birth for preventing neonatal respiratory disease. The Cochrane Database of Systematic Reviews 2003, (Issue 2(2):Art. No.: CD003935. DOI: 10.1002/14651858.CD003935).

    Google Scholar 

  83. Nyirenda MJ, Lindsay RS, Kenyon CJ et al. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. Journal of Clinical Investigation 1998; 101:2174–81.

    PubMed  CAS  Google Scholar 

  84. Dahlgren J, Nilsson C, Jennische E et al. Prenatal cytokine exposure results in obesity and gender-specific programming. Am J Physiol 2001; 281(2):E326–E34.

    CAS  Google Scholar 

  85. De Blasio MJ, Gatford KL, Fielke SL et al. Fetal growth restriction increases growth rate and insulin sensitivity in the postnatal lamb. Paper presented at: 11th International Congress of Endocrinology. Australia: Sydney, 2000.

    Google Scholar 

  86. De Blasio MJ, Bradbury MR, Adams DH et al. Placental restriction increases postnatal growth rate and sensitivity to IGF-I in the neonatal lamb. Paper presented at: Endocrine Society of Australia Annual Scientific Meeting. Australia: Gold Coast, 2001.

    Google Scholar 

  87. Lloyd NK, Thavaneswaran P, Grover S et al. IGF-1 sensitivity and catch-up growth following intrauterine growth restriction in the weanling guinea pig. Paper presented at: Second World Congress on Fetal Origins of Adult Disease. United Kingdom: Brighton, 2003.

    Google Scholar 

  88. Horton DM. Prenatal growth and postnatal insulin sensitivity in the guinea pig. Paper presented at: Perinatal Origins of Adult Disease Workshop. Australia: Melbourne, 1999.

    Google Scholar 

  89. Gatford KL, De Blasio MJ, McMillen IC et al. Placental restriction and ontogeny of insulin-regulated glucose homeostasis in sheep. Paper presented at: Endocrine Society of Australia Annual Scientific Meeting. Australia: Adelaide, 2002.

    Google Scholar 

  90. Bazaes RA, Salazar TE, Pittaluga E et al. Glucose and lipid metabolism in small for gestational age infants at 48 hours of age. Pediatrics 2003; 111:804–09.

    PubMed  Google Scholar 

  91. Wang X, Cui Y, Tong X et al. Effects of the Trp64Arg polymorphism in the b3-adrenergic receptor gene on insulin sensitivity in small for gestational age neonates. J Clin Endocrinol Metab 2004; 89:4981–85.

    PubMed  CAS  Google Scholar 

  92. Li C, Johnson MS, Goran MI. Effects of low birth weight on insulin resistance syndrome in Caucasian and African-American children. Diabetes Care 2001; 24:2035–42.

    PubMed  CAS  Google Scholar 

  93. Jensen CB, Storgaard H, Dela F et al. Early differential defects of insulin secretion and action in 19-year-old Caucasian men who had low birth weight. Diabetes 2002; 51:1271–80.

    PubMed  CAS  Google Scholar 

  94. Jaquet D, Gaboriau A, Czernichow P et al. Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J Clin Endocrinol Metab 2000; 85:1401–06.

    PubMed  CAS  Google Scholar 

  95. Hermann TS, Rask-Madsen C, Ihlemann N et al. Normal insulin-stimulated endothelial function and impaired insulin-stimulated muscle glucose uptake in young adults with low birth weight. J Clin Endocrinol Metab 2003; 88:1252–57.

    PubMed  CAS  Google Scholar 

  96. Jaquet D, Vidal H, Hankard R et al. Impaired regulation of glucose transporter 4 gene expression in insulin resistance associated with in utero undernutrition. J Clin Endocrinol Metab 2001; 86:3266–71.

    PubMed  CAS  Google Scholar 

  97. Phillips DIW, Borthwick AC, Stein C et al. Fetal growth and insulin resistance in adult life: Relationship between glycogen synthase activity in adult skeletal muscle and birthweight. Diabet Med 1996; 13:325–29.

    PubMed  CAS  Google Scholar 

  98. Thompson CH, Sanderson AL, Sandeman D et al. Fetal growth and insulin resistance in adult life: Role of skeletal muscle morphology. Clin Sci 1997; 92:291–96.

    PubMed  CAS  Google Scholar 

  99. Arrowsmith F, Ward J, Ling A et al. Fetal nutrition and muscle oxygen supply in childhood. Metabolism 2002; 51:1569–72.

    PubMed  CAS  Google Scholar 

  100. IJzerman RG, van Weissenbruch MM, Voordouw JJ et al. The association between birth weight and capillary recruitment is independent of blood pressure and insulin sensitivity: A study in prepubertal children. J Hypertens 2002; 20:1957–63.

    PubMed  CAS  Google Scholar 

  101. Stefan N, Weyer C, Levy-Marchal C et al. Endogenous glucose production, insulin sensitivity, and insulin secretion in normal glucose-tolerant Pima Indians with low birth weight. Metabolism 2004; 53(7):904–11.

    PubMed  CAS  Google Scholar 

  102. Van Assche FA, De Prins F, Aerts L et al. The endocrine pancreas in small-for-dates infants. Br J Obstetr Gynaecol 1977; 84:751–53.

    Google Scholar 

  103. Béringue F, Blondeau B, Castellotti MC et al. Endocrine pancreas development in growth-retarded human fetuses. Diabetes 2002; 51:385–91.

    PubMed  Google Scholar 

  104. Robinson JS, Moore VM, Owens JA et al. Origins of fetal growth restriction. Eur J Obstetr Gynecol Reprod Biol 2000; 92:13–19.

    CAS  Google Scholar 

  105. Dwyer CM, Madgwick AJA, Ward SS et al. Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod Fertil Dev 1995; 7:1285–92.

    PubMed  CAS  Google Scholar 

  106. Bedi KS, Birzgalis AR, Mahon M et al. Early life undernutrition in rats 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. Br J Nutr 1982; 47:417–31.

    PubMed  CAS  Google Scholar 

  107. Garofano A, Czernichow P, Bréant B. Effect of aging on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia 1999; 42:711–18.

    PubMed  CAS  Google Scholar 

  108. Schoknecht PA, Pond WG, Mersmann HJ et al. Protein restriction during pregnancy affects postnatal growth in swine progeny. J Nutr 1993; 123:1818–25.

    PubMed  CAS  Google Scholar 

  109. Bihoreau M-T, Ktorza A, Kinebanyan MF et al. Impaired glucose homeostasis in adult rats from hyperglycemic mothers. Diabetes 1986; 35:979–84.

    PubMed  CAS  Google Scholar 

  110. Gauguier D, Bihoreau M-T, Ktorza A et al. Inheritance of diabetes mellitus as consequence of gestational hyperglycemia in rats. Diabetes 1990; 39:734–39.

    PubMed  CAS  Google Scholar 

  111. Dodic M, May CN, Wintour EM et al. An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin Sci 1998; 94:149–55.

    PubMed  CAS  Google Scholar 

  112. Gatford KL, Wintour EM, De Blasio MJ et al. Differential timing for programming of glucose homeostasis, metabolic sensitivity to insulin and blood pressure by in utero exposure to dexamethasone in sheep. Clin Sci 2000; 98:553–60.

    PubMed  CAS  Google Scholar 

  113. Banjanin S, Kapoor A, Matthews SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J Physiol 2004; 558:305–18.

    PubMed  CAS  Google Scholar 

  114. Phillips DIW, Barker DJP, Hales CN et al. Thinness at birth and insulin resistance in adult life. Diabetologia 1994; 37:150–54.

    PubMed  CAS  Google Scholar 

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Gatford, K.L., De Blasio, M.J., Dodic, M., Horton, D.M., Kind, K.L. (2006). Perinatal Programming of Adult Metabolic Homeostasis. In: Wintour, E.M., Owens, J.A. (eds) Early Life Origins of Health and Disease. Advances in Experimental Medicine and Biology, vol 573. Springer, Boston, MA. https://doi.org/10.1007/0-387-32632-4_13

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