Home LiteratureArticle Details
PMID: 15459241 Published · ppublish English Journal Article Review

Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?

The Journal of physiology ·Vol. 561 ·No. Pt 2 ·2004-12-01 ·Pages 355-77

Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L

Abstract

The incidence of the metabolic syndrome, a cluster of abnormalities focusing on insulin resistance and associated with high risk for cardiovascular disease and diabetes, is reaching epidemic proportions. Prevalent in both developed and developing countries, the metabolic syndrome has largely been attributed to altered dietary and lifestyle factors that favour the development of central obesity. However, population-based studies have suggested that predisposition to the metabolic syndrome may be acquired very early in development through inappropriate fetal or neonatal nutrition. Further evidence for developmental programming of the metabolic syndrome has now been suggested by animal studies in which the fetal environment has been manipulated through altered maternal dietary intake or modification of uterine artery blood flow. This review examines these studies and assesses whether the metabolic syndrome can be reliably induced by the interventions made. The validity of the different species, diets, feeding regimes and end-point measures used is also discussed.

MeSH Terms
Animals Disease Models, Animal Female Fetal Development/physiology Humans Maternal Nutritional Physiological Phenomena/physiology Metabolic Syndrome/blood,embryology,physiopathology Pregnancy Prenatal Exposure Delayed Effects
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Armitage James A
Maternal and Fetal Research Unit, Department of Women's Health, Guy's, King's and St Thomas' School of Medicine, King's College London, UK. james.armitage@kcl.ac.uk
Khan Imran Y
Taylor Paul D
Nathanielsz Peter W
Poston Lucilla
References (172)
172 references, click to expand
  1. An inverse relation between blood pressure and birth weight among 5 year old children from Soweto, South Africa.
    J Epidemiol Community Health. 1999 May;53(5):264-8 PMID: 10396531
  2. A new dimension to the Barker hypothesis: low birthweight and susceptibility to renal disease.
    Kidney Int. 1999 Sep;56(3):1072-7 PMID: 10469376
  3. Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine.
    Clin Sci (Lond). 2002 Dec;103(6):633-9 PMID: 12444916
  4. Frequency of the WHO metabolic syndrome in European cohorts, and an alternative definition of an insulin resistance syndrome.
    Diabetes Metab. 2002 Nov;28(5):364-76 PMID: 12461473
  5. Maternal dietary NaCl intake influences weanling rats' salt preferences without affecting taste nerve responsiveness.
    Dev Psychobiol. 1987 Mar;20(2):111-30 PMID: 3582775
  6. Changes to metabolite concentration in fetal sheep subjected to prolonged hypobaric hypoxia.
    J Dev Physiol. 1988 Apr;10(2):113-21 PMID: 3397504
  7. Studies on the growth of the fetal sheep. Effects of surgical reduction in placental size, or experimental manipulation of uterine blood flow on plasma sulphation promoting activity and on the concentration of insulin-like growth factors I and II.
    J Dev Physiol. 1988 Apr;10(2):179-89 PMID: 3397509
  8. Weight in infancy and death from ischaemic heart disease.
    Lancet. 1989 Sep 9;2(8663):577-80 PMID: 2570282
  9. Perinatal salt intake alters blood pressure and salt balance in hypertensive rats.
    Hypertension. 1990 Feb;15(2):177-82 PMID: 2303281
  10. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas.
    Biol Neonate. 1990;57(2):107-18 PMID: 2178691
  11. Perinatal exposure to a high NaCl diet increases the NaCl intake of adult rats.
    Physiol Behav. 1990 Mar;47(3):507-12 PMID: 2359761
  12. Fetal and placental size and risk of hypertension in adult life.
    BMJ. 1990 Aug 4;301(6746):259-62 PMID: 2390618
  13. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid.
    Diabetes. 1991 Feb;40(2):280-9 PMID: 1991575
  14. Regional blood flow distribution in fetal sheep with intrauterine growth retardation produced by decreased umbilical placental perfusion.
    J Dev Physiol. 1990 Feb;13(2):81-5 PMID: 2283464
  15. Prenatal protein malnutrition and maternal behavior in Sprague-Dawley rats.
    J Nutr. 1991 May;121(5):762-9 PMID: 2019885
  16. Essentiality of omega 3 fatty acids in growth and development of infants.
    World Rev Nutr Diet. 1991;66:74-86 PMID: 2053367
  17. Islet function in offspring of mothers on low-protein diet during gestation.
    Diabetes. 1991 Dec;40 Suppl 2:115-20 PMID: 1748239
  18. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis.
    Diabetologia. 1992 Jul;35(7):595-601 PMID: 1644236
  19. Sex difference in blood pressure of spontaneously hypertensive rats influenced by perinatal NaCl exposure.
    Physiol Behav. 1992 Mar;51(3):449-55 PMID: 1523220
  20. Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding.
    Exp Clin Endocrinol. 1992;99(3):154-8 PMID: 1526266
  21. High NaCl intake of rat dams alters maternal behavior and elevates blood pressure of adult offspring.
    Am J Physiol. 1993 Feb;264(2 Pt 2):R296-304 PMID: 8447485
  22. Fetal nutrition and cardiovascular disease in adult life.
    Lancet. 1993 Apr 10;341(8850):938-41 PMID: 8096277
  23. Growth in utero and serum cholesterol concentrations in adult life.
    BMJ. 1993 Dec 11;307(6918):1524-7 PMID: 8274921
  24. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets.
    Clin Sci (Lond). 1994 Feb;86(2):217-22; discussion 121 PMID: 8143432
  25. Regional brain blood flow and cerebral hemispheric oxygen consumption during acute hypoxaemia in the llama fetus.
    J Physiol. 2002 Feb 1;538(Pt 3):975-83 PMID: 11826180
  26. Severe nutritional restriction in pregnant rats aggravates hypertension, altered vascular reactivity, and renal development in spontaneously hypertensive rats offspring.
    J Cardiovasc Pharmacol. 2002 Mar;39(3):369-77 PMID: 11862116
  27. Estrogenic isoflavones in rodent diets.
    Toxicol Lett. 2002 Mar 10;128(1-3):145-57 PMID: 11869825
  28. Effects of prevailing hypoxaemia, acidaemia or hypoglycaemia upon the cardiovascular, endocrine and metabolic responses to acute hypoxaemia in the ovine fetus.
    J Physiol. 2002 Apr 1;540(Pt 1):351-66 PMID: 11927692
  29. Iron deficiency is prevalent in a sample of pregnant women at delivery in Germany.
    Eur J Obstet Gynecol Reprod Biol. 2002 May 10;102(2):155-60 PMID: 11950483
  30. Intrauterine growth restriction in rats is associated with hypertension and renal dysfunction in adulthood.
    Am J Physiol Endocrinol Metab. 2002 Jul;283(1):E124-31 PMID: 12067852
  31. Mitochondrial integrity and function in atherogenesis.
    Circulation. 2002 Jul 30;106(5):544-9 PMID: 12147534
  32. Long-term programming of blood pressure by maternal dietary iron restriction in the rat.
    Br J Nutr. 2002 Sep;88(3):283-90 PMID: 12207838
  33. Differential effects of the early and late intrauterine environment on corticotrophic cell development.
    J Clin Invest. 2002 Sep;110(6):783-91 PMID: 12235109
  34. Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring.
    Cardiovasc Res. 2002 Oct;56(1):145-53 PMID: 12237175
  35. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure?
    Lancet. 2002 Aug 31;360(9334):659-65 PMID: 12241871
  36. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero.
    J Cardiovasc Pharmacol. 2002 Oct;40(4):501-9 PMID: 12352311
  37. Effects of intrauterine growth restriction and intraamniotic insulin-like growth factor-I treatment on blood and amniotic fluid concentrations and on fetal gut uptake of amino acids in late-gestation ovine fetuses.
    J Pediatr Gastroenterol Nutr. 2002 Sep;35(3):287-97 PMID: 12352515
  38. Programmed hypertension: kidney, brain or both?
    Trends Endocrinol Metab. 2002 Nov;13(9):403-8 PMID: 12367823
  39. Diabetes in old male offspring of rat dams fed a reduced protein diet.
    Int J Exp Diabetes Res. 2001;2(2):139-43 PMID: 12369717
  40. Supplementation with conjugated linoleic acid causes isomer-dependent oxidative stress and elevated C-reactive protein: a potential link to fatty acid-induced insulin resistance.
    Circulation. 2002 Oct 8;106(15):1925-9 PMID: 12370214
  41. Dietary fatty acid composition during pregnancy and lactation in the rat programs growth and glucose metabolism in the offspring.
    Diabetologia. 2002 Oct;45(10):1397-403 PMID: 12378380
  42. Effect of maternal feed restriction on blood pressure in the adult guinea pig.
    Exp Physiol. 2002 Jul;87(4):469-77 PMID: 12392111
  43. Power spectral analysis of heart rate variability during acute hypoxia in fetal lambs.
    Acta Obstet Gynecol Scand. 2002 Nov;81(11):1001-5 PMID: 12421166
  44. Serum concentrations of homocysteine are elevated during early pregnancy in rodent models of fetal programming.
    Br J Nutr. 2002 Nov;88(5):471-7 PMID: 12425727
  45. Prenatal and early postnatal sodium chloride intake modifies the solution preferences of adult rats.
    J Nutr. 1983 May;113(5):1051-62 PMID: 6842300
  46. Effect of litter size on plasma cholesterol and insulin and some liver and adipose tissue enzymes in adult rodents.
    J Nutr. 1984 Jul;114(7):1231-4 PMID: 6376732
  47. Thinness at birth and insulin resistance in adult life.
    Diabetologia. 1994 Feb;37(2):150-4 PMID: 8163048
  48. Growth in utero, adult blood pressure, and arterial compliance.
    Br Heart J. 1995 Feb;73(2):116-21 PMID: 7696018
  49. Altered vascular function in fetal programming of hypertension.
    Stroke. 2002 Dec;33(12):2992-8 PMID: 12468802
  50. Altered glucose tolerance in rats exposed to maternal low protein diets in utero.
    Comp Biochem Physiol Physiol. 1994 Oct;109(2):223-9 PMID: 7956116
  51. Obesity at the age of 50 y in men and women exposed to famine prenatally.
    Am J Clin Nutr. 1999 Nov;70(5):811-6 PMID: 10539740
  52. Evidence that the mitochondrial genome is the thrifty genome.
    Diabetes Res Clin Pract. 1999 Sep;45(2-3):127-35 PMID: 10588365
  53. Effect of maternal nutrient restriction in early gestation on development of the hypothalamic-pituitary-adrenal axis in fetal sheep at 0.8-0.9 of gestation.
    J Endocrinol. 1999 Dec;163(3):553-61 PMID: 10588829
  54. Restricted fetal growth and the response to dietary cholesterol in the guinea pig.
    Am J Physiol. 1999 Dec;277(6 Pt 2):R1675-82 PMID: 10600913
  55. Antihypertensive treatment in early postnatal life modulates prenatal dietary influences upon blood pressure in the rat.
    Clin Sci (Lond). 2000 Mar;98(3):269-75 PMID: 10677384
  56. Blood pressure is related to placental volume and birth weight.
    Hypertension. 2000 Feb;35(2):662-7 PMID: 10679514
  57. Critical differences between two low protein diet protocols in the programming of hypertension in the rat.
    Int J Food Sci Nutr. 2000 Jan;51(1):11-7 PMID: 10746100
  58. Glucocorticoids, 11beta-hydroxysteroid dehydrogenase, and fetal programming.
    Kidney Int. 2000 Apr;57(4):1412-7 PMID: 10760076
  59. Phytoestrogens and cardiovascular health.
    J Am Coll Cardiol. 2000 May;35(6):1403-10 PMID: 10807439
  60. Low doses of dexamethasone suppress pituitary-adrenal function but augment the glycemic response to acute hypoxemia in fetal sheep during late gestation.
    Pediatr Res. 2000 May;47(5):684-91 PMID: 10813597
  61. Maternal protein deficiency causes hypermethylation of DNA in the livers of rat fetuses.
    J Nutr. 2000 Jul;130(7):1821-6 PMID: 10867057
  62. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition.
    Am J Physiol Endocrinol Metab. 2000 Jul;279(1):E83-7 PMID: 10893326
  63. Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes.
    Am J Physiol Regul Integr Comp Physiol. 2000 Jul;279(1):R340-8 PMID: 10896898
  64. Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult-onset disease.
    Proc Nutr Soc. 2000 May;59(2):257-65 PMID: 10946794
  65. Endocrine regulation and extended follow up of longitudinal growth in intrauterine growth-retarded rats.
    J Endocrinol. 2000 Sep;166(3):599-608 PMID: 10974654
  66. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine.
    Am J Clin Nutr. 2000 Nov;72(5):1101-6 PMID: 11063435
  67. Maternal hypercholesterolemia enhances atherogenesis in normocholesterolemic rabbits, which is inhibited by antioxidant or lipid-lowering intervention during pregnancy: an experimental model of atherogenic mechanisms in human fetuses.
    Circ Res. 2000 Nov 10;87(10):946-52 PMID: 11073892
  68. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45.
    Heart. 2000 Dec;84(6):595-8 PMID: 11083734
  69. Effects of undernutrition in early pregnancy on systemic small artery function in late-gestation fetal sheep.
    Am J Obstet Gynecol. 2000 Nov;183(5):1301-7 PMID: 11084581
  70. Neuropeptide Y in the sheep fetus: effects of acute hypoxemia and dexamethasone during late gestation.
    Endocrinology. 2000 Nov;141(11):3976-82 PMID: 11089527
  71. Prenatal programming of adult hypertension in the rat.
    Kidney Int. 2001 Jan;59(1):238-45 PMID: 11135076
  72. High dietary NaCl early in development enhances mean arterial pressure of adult rats.
    Physiol Behav. 2000 Oct 1-15;71(1-2):173-81 PMID: 11134699
  73. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring.
    J Physiol. 2001 Jan 1;530(Pt 1):141-52 PMID: 11136866
  74. Plasma adrenocorticotropin and cortisol concentrations during acute hypoxemia after a reversible period of adverse intrauterine conditions in the ovine fetus during late gestation.
    Endocrinology. 2001 Feb;142(2):589-98 PMID: 11159829
  75. Prenatal exposure to a maternal low protein diet shortens life span in rats.
    Gerontology. 2001 Jan-Feb;47(1):9-14 PMID: 11244286
  76. Perinatal omega-3 fatty acid deficiency affects blood pressure later in life.
    Nat Med. 2001 Mar;7(3):258-9 PMID: 11231597
  77. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats.
    Pediatr Res. 2001 Apr;49(4):460-7 PMID: 11264427
  78. Effects of altitude versus economic status on birth weight and body shape at birth.
    Pediatr Res. 2001 Apr;49(4):490-4 PMID: 11264431
  79. Dietary modulation of endothelial function: implications for cardiovascular disease.
    Am J Clin Nutr. 2001 Apr;73(4):673-86 PMID: 11273841
  80. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring.
    Metabolism. 2001 May;50(5):562-7 PMID: 11319718
  81. Peripheral blood mitochondrial DNA content is related to insulin sensitivity in offspring of type 2 diabetic patients.
    Diabetes Care. 2001 May;24(5):865-9 PMID: 11347745
  82. Abnormal aortic fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy.
    J Physiol. 2001 Jun 15;533(Pt 3):815-22 PMID: 11410637
  83. Dysregulation of the adipoinsular axis -- a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming.
    J Endocrinol. 2001 Aug;170(2):323-32 PMID: 11479129
  84. Adult survival after prenatal exposure to the Dutch famine 1944--45.
    Paediatr Perinat Epidemiol. 2001 Jul;15(3):220-5 PMID: 11489148
  85. IGF-I treatment reduces hyperphagia, obesity, and hypertension in metabolic disorders induced by fetal programming.
    Endocrinology. 2001 Sep;142(9):3964-73 PMID: 11517175
  86. Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits.
    Circ Res. 2001 Nov 23;89(11):991-6 PMID: 11717155
  87. Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease.
    Circulation. 2001 Nov 27;104(22):2673-8 PMID: 11723017
  88. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview.
    Mol Cell Endocrinol. 2001 Dec 20;185(1-2):93-8 PMID: 11738798
  89. The thrifty phenotype hypothesis.
    Br Med Bull. 2001;60:5-20 PMID: 11809615
  90. Long-term consequences for offspring of diabetes during pregnancy.
    Br Med Bull. 2001;60:173-82 PMID: 11809625
  91. Postnatal somatic growth and insulin contents in moderate or severe intrauterine growth retardation in the rat.
    Biol Neonate. 1998;73(2):89-98 PMID: 9483301
  92. The influence of restraint on blood pressure in the rat.
    J Pharmacol Toxicol Methods. 1997 Nov;38(3):157-62 PMID: 9523769
  93. Size at birth, maternal weight, and type 2 diabetes in South India.
    Diabet Med. 1998 Mar;15(3):220-7 PMID: 9545123
  94. Aging, changes in the cardiovascular system, and responses to stress.
    Am J Hypertens. 1998 Mar;11(3 Pt 2):41S-45S PMID: 9546036
  95. Prenatal malnutrition-induced changes in blood pressure: dissociation of stress and nonstress responses using radiotelemetry.
    Hypertension. 1998 Jul;32(1):108-14 PMID: 9674646
  96. Fetal brain injury following prolonged hypoxemia and placental insufficiency: a review.
    Comp Biochem Physiol A Mol Integr Physiol. 1998 Mar;119(3):653-60 PMID: 9683403
  97. Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat.
    Diabetologia. 1998 Sep;41(9):1114-20 PMID: 9754832
  98. Offspring of normal and diabetic rats fed saturated fat in pregnancy demonstrate vascular dysfunction.
    Circulation. 1998 Dec 22-29;98(25):2899-904 PMID: 9860793
  99. Leptin resistance in obese humans: does it exist and what does it mean?
    Int J Obes Relat Metab Disord. 1998 Dec;22(12):1159-63 PMID: 9877250
  100. Antecedent protein restriction exacerbates development of impaired insulin action after high-fat feeding.
    Am J Physiol. 1999 Jan;276(1 Pt 1):E85-93 PMID: 9886954
  101. Maternal undernutrition increases arterial blood pressure in the sheep fetus during late gestation.
    J Physiol. 2001 Jun 1;533(Pt 2):561-70 PMID: 11389212
  102. Decreased mitochondrial DNA content in peripheral blood precedes the development of non-insulin-dependent diabetes mellitus.
    Diabetes Res Clin Pract. 1998 Dec;42(3):161-7 PMID: 9925346
  103. Catch-up growth in childhood and death from coronary heart disease: longitudinal study.
    BMJ. 1999 Feb 13;318(7181):427-31 PMID: 9974455
  104. Induction of intrauterine growth restriction with a low-sodium diet fed to pregnant rats.
    Am J Obstet Gynecol. 1999 Mar;180(3 Pt 1):608-13 PMID: 10076136
  105. Blood pressure in adults after prenatal exposure to famine.
    J Hypertens. 1999 Mar;17(3):325-30 PMID: 10100069
  106. Cholesterol-independent endothelial dysfunction in virgin and pregnant rats fed a diet high in saturated fat.
    J Physiol. 1999 Jun 1;517 ( Pt 2):607-16 PMID: 10332106
  107. Maternal food restriction in the second half of pregnancy affects vascular function but not blood pressure of rat female offspring.
    Br J Nutr. 1999 Jan;81(1):73-9 PMID: 10341679
  108. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period.
    Diabetologia. 1999 Jun;42(6):711-8 PMID: 10382591
  109. Captopril normalises systolic blood pressure in rats with hypertension induced by fetal exposure to maternal low protein diets.
    Comp Biochem Physiol A Physiol. 1995 Mar;110(3):223-8 PMID: 7712066
  110. High-fat feeding during pregnancy and lactation affects offspring metabolism in rats.
    Physiol Behav. 1995 Apr;57(4):681-6 PMID: 7777603
  111. Fetal origins of coronary heart disease.
    BMJ. 1995 Jul 15;311(6998):171-4 PMID: 7613432
  112. Rats with hypertension induced by in utero exposure to maternal low-protein diets fail to increase blood pressure in response to a high salt intake.
    Ann Nutr Metab. 1996;40(1):1-9 PMID: 8722301
  113. Intrauterine programming of hypertension in the rat: nutrient interactions.
    Comp Biochem Physiol A Physiol. 1996 Aug;114(4):327-33 PMID: 8759281
  114. 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 Aug;150(2):231-42 PMID: 8869590
  115. Influence of dietary fats upon systolic blood pressure in the rat.
    Int J Food Sci Nutr. 1996 Sep;47(5):417-25 PMID: 8889627
  116. Nutrient metabolism in pancreatic islets from protein malnourished rats.
    Biochem Mol Med. 1996 Oct;59(1):62-7 PMID: 8902196
  117. Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring.
    Br J Nutr. 1996 Oct;76(4):605-12 PMID: 8942366
  118. Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension.
    Clin Sci (Lond). 1996 Nov;91(5):607-15 PMID: 8942400
  119. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats.
    Am J Physiol. 1996 Dec;271(6 Pt 1):E1128-34 PMID: 8997235
  120. Evaluation of the IITC tail cuff blood pressure recorder in the rat against intraarterial pressure according to criteria for human devices.
    Am J Hypertens. 1997 Feb;10(2):209-16 PMID: 9037330
  121. The beneficial effects of omega-3 fatty acids: cardiovascular disease and neurodevelopment.
    Curr Opin Lipidol. 1997 Feb;8(1):1-3 PMID: 9127702
  122. Fetal nutrition and cardiovascular disease in later life.
    Br Med Bull. 1997 Jan;53(1):96-108 PMID: 9158287
  123. Maternal birthweight and diet in pregnancy in relation to the infant's thinness at birth.
    Br J Obstet Gynaecol. 1997 Jun;104(6):663-7 PMID: 9197868
  124. Altered adipocyte properties in the offspring of protein malnourished rats.
    Br J Nutr. 1997 Jul;78(1):121-9 PMID: 9292765
  125. Early protein restriction and obesity independently induce hypertension in 1-year-old rats.
    Clin Sci (Lond). 1997 Aug;93(2):147-52 PMID: 9301429
  126. In utero undernutrition impairs rat beta-cell development.
    Diabetologia. 1997 Oct;40(10):1231-4 PMID: 9349607
  127. Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet.
    Am J Physiol. 1997 Oct;273(4 Pt 1):G899-904 PMID: 9357833
  128. Cerebral circulatory responses of near-term ovine fetuses during sustained fetal placental embolization.
    Am J Physiol. 1997 Oct;273(4 Pt 2):H2001-8 PMID: 9362272
  129. Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study.
    BMJ. 1997 Nov 22;315(7119):1342-8 PMID: 9402775
  130. Glucose tolerance in adults after prenatal exposure to famine.
    Lancet. 1998 Jan 17;351(9097):173-7 PMID: 9449872
  131. A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II.
    Endocrinology. 1999 Oct;140(10):4861-73 PMID: 10499546
  132. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy.
    Am J Physiol Regul Integr Comp Physiol. 2005 Jan;288(1):R134-9 PMID: 15388492
  133. Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig.
    Am J Physiol Regul Integr Comp Physiol. 2003 Jan;284(1):R140-52 PMID: 12388450
  134. Gender-linked hypertension in offspring of lard-fed pregnant rats.
    Hypertension. 2003 Jan;41(1):168-75 PMID: 12511548
  135. Maternal protein restriction in the rat impairs resistance artery but not conduit artery function in pregnant offspring.
    J Physiol. 2003 Feb 15;547(Pt 1):77-84 PMID: 12562942
  136. Hindlimb glucose and lactate metabolism during umbilical cord compression and acute hypoxemia in the late-gestation ovine fetus.
    Am J Physiol Regul Integr Comp Physiol. 2003 Apr;284(4):R954-64 PMID: 12666662
  137. Postnatal development of arterial pressure: influence of the intrauterine environment.
    Arch Physiol Biochem. 2003 Feb;111(1):53-60 PMID: 12715275
  138. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle.
    J Endocrinol. 2003 May;177(2):235-41 PMID: 12740011
  139. Effects of aging on cardiovascular responses to parasympathetic withdrawal.
    J Am Coll Cardiol. 2003 Jun 4;41(11):2077-83 PMID: 12798585
  140. Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in the fetal sheep.
    Biol Reprod. 2003 Jul;69(1):133-40 PMID: 12606329
  141. Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring.
    Pediatr Res. 2003 Jul;54(1):83-90 PMID: 12646717
  142. Effect of maternal iron restriction during pregnancy on renal morphology in the adult rat offspring.
    Br J Nutr. 2003 Jul;90(1):33-9 PMID: 12844373
  143. Increased blood pressure later in life may be associated with perinatal n-3 fatty acid deficiency.
    Lipids. 2003 Apr;38(4):459-64 PMID: 12848294
  144. Effects of chronic hypoxia on maternal vasodilation and vascular reactivity in guinea pig and ovine pregnancy.
    High Alt Med Biol. 2003 Summer;4(2):157-69 PMID: 12855049
  145. Effect of reduced maternal protein intake in pregnancy in the rat on the fatty acid composition of brain, liver, plasma, heart and lung phospholipids of the offspring after weaning.
    Br J Nutr. 2003 Aug;90(2):345-52 PMID: 12908895
  146. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction.
    Br J Nutr. 2003 Oct;90(4):815-22 PMID: 13129451
  147. NADPH oxidase and enhanced superoxide generation in intrauterine undernourished rats: involvement of the renin-angiotensin system.
    Cardiovasc Res. 2003 Sep 1;59(3):767-75 PMID: 14499878
  148. The metabolic syndrome: practical guide to origins and treatment: Part I.
    Circulation. 2003 Sep 23;108(12):1422-4 PMID: 14504251
  149. Metabolic syndrome: epidemiology and more extensive phenotypic description. Cross-sectional data from the Bruneck Study.
    Int J Obes Relat Metab Disord. 2003 Oct;27(10):1283-9 PMID: 14513078
  150. The metabolic syndrome: more than the sum of its parts?
    Circulation. 2003 Sep 30;108(13):1546-51 PMID: 14517150
  151. Fetal and early postnatal protein malnutrition cause long-term changes in rat liver and muscle mitochondria.
    J Nutr. 2003 Oct;133(10):3085-90 PMID: 14519789
  152. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney.
    Am J Physiol Regul Integr Comp Physiol. 2003 Nov;285(5):R962-70 PMID: 12869365
  153. Iron deficiency during pregnancy affects postnatal blood pressure in the rat.
    J Physiol. 2003 Oct 15;552(Pt 2):603-10 PMID: 14561840
  154. Intrauterine programming of fetal islet gene expression in rats--effects of maternal protein restriction during gestation revealed by proteome analysis.
    Diabetologia. 2003 Nov;46(11):1497-511 PMID: 13680128
  155. Endothelial dysfunction in obesity and insulin resistance: a road to diabetes and heart disease.
    Obes Res. 2003 Nov;11(11):1278-89 PMID: 14627747
  156. Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet.
    Clin Sci (Lond). 2004 Feb;106(2):141-5 PMID: 14507258
  157. Glycine rectifies vascular dysfunction induced by dietary protein imbalance during pregnancy.
    J Physiol. 2004 Jan 15;554(Pt 2):497-504 PMID: 14578485
  158. Lifespan: catch-up growth and obesity in male mice.
    Nature. 2004 Jan 29;427(6973):411-2 PMID: 14749819
  159. Evaluation of estrogenic activity in diets for experimental animals using in vitro assay.
    J Agric Food Chem. 2004 Mar 10;52(5):1410-4 PMID: 14995154
  160. Prenatal stress changes rat arterial adrenergic reactivity in a regionally selective manner.
    Eur J Pharmacol. 2004 Mar 19;488(1-3):147-55 PMID: 15044046
  161. Interrelations between ceruloplasmin and Fe status during human pregnancy.
    Biol Trace Elem Res. 2004 Apr;98(1):1-12 PMID: 15051895
  162. The developmental origins of the metabolic syndrome.
    Trends Endocrinol Metab. 2004 May-Jun;15(4):183-7 PMID: 15109618
  163. Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus.
    JAMA. 2004 Apr 28;291(16):1978-86 PMID: 15113816
  164. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep.
    Hypertension. 2004 Jun;43(6):1290-6 PMID: 15078864
  165. Reduced uteroplacental blood flow alters renal arterial reactivity and glomerular properties in the rat offspring.
    Hypertension. 2004 Jun;43(6):1283-9 PMID: 15117909
  166. Programming of adult cardiovascular function after early maternal undernutrition in sheep.
    Am J Physiol Regul Integr Comp Physiol. 2004 Jul;287(1):R12-20 PMID: 14975924
  167. Epigenetic programming by maternal behavior.
    Nat Neurosci. 2004 Aug;7(8):847-54 PMID: 15220929
  168. Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines.
    Diabetologia. 2004 Apr;47(4):669-75 PMID: 15298344
  169. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring.
    Circulation. 2004 Aug 31;110(9):1097-102 PMID: 15326063
  170. Obesity in young men after famine exposure in utero and early infancy.
    N Engl J Med. 1976 Aug 12;295(7):349-53 PMID: 934222
  171. Cerebral oxidative metabolism during intrauterine growth retardation.
    Biol Neonate. 1978;34(3-4):170-3 PMID: 737237
  172. Age-related alterations in the cardiovascular response to adrenergic mediated stress.
    Fed Proc. 1980 Dec;39(14):3173-7 PMID: 6108242
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
DOI
10.1113/jphysiol.2004.072009
Email
james.armitage@kcl.ac.uk
Published
2004-12-01
Epub
2004-00-30
Pages
355-77
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1665360
Subset
IM
Grants
NICHD NIH HHS · P01 HD021350 · United States
External Links
PubMed source DOI: 10.1113/jphysiol.2004.072009 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2