Fetal growth restriction and consequences for the offspring in animal models

Journal of the Society for Gynecologic Investigation

Volumn 10, Issue 7, 2003, Pages 392-399

  Holemans, K ^a,b   Aerts, L ^a   Van Assche, F A ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; CORTICOSTERONE; DEXAMETHASONE; FRUCTOSE BISPHOSPHATASE; GLUCOCORTICOID; GLUCOSE; GLUCOSE 6 PHOSPHATASE; GLUCOSE TRANSPORTER 1; HYDROCORTISONE; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN; STREPTOZOCIN;

ADAPTATION; ANIMAL MODEL; ARTERY LIGATION; CARDIOVASCULAR DISEASE; DIABETES MELLITUS; DIET RESTRICTION; DIETARY INTAKE; DISEASE COURSE; DISEASE PREDISPOSITION; DOSE RESPONSE; FETUS CIRCULATION; FETUS DEVELOPMENT; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HYPERGLYCEMIA; HYPERTENSION; HYPOINSULINEMIA; HYPOTHESIS; INFORMATION PROCESSING; INSULIN RELEASE; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; LOW DRUG DOSE; MACROSOMIA; MALNUTRITION; MEDLINE; METABOLISM; MOLECULAR MECHANICS; MOTHER; NONHUMAN; OBESITY; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PERINATAL DEVELOPMENT; PERINATAL PERIOD; PHENOTYPE; PREGNANCY; PREGNANCY DIABETES MELLITUS; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; REVIEW; UTERINE ARTERY; UTERUS;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FETAL BLOOD; FETAL GROWTH RETARDATION; INSULIN; MALNUTRITION; MEDLINE; PREGNANCY; PREGNANCY IN DIABETICS; RATS;

EID: 0141453694     PISSN: 10715576     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1071-5576(03)00134-5     Document Type: Review

References (104)

1. Barker D.J. Fetal origins of coronary heart disease. BMJ. 31:1995;171-174.
2. Phillips D.I., Barker D.J., Hales C.N., Hirst S., Osmond C. Thinness at birth and insulin resistance in adult life. Diabetologia. 37:1994;150-154.
3. Barker D.J., Clark P.M. Fetal undernutrition and disease in later life. Rev Reprod. 2:1997;105-112.
4. Martin A.O., Simpson J.L., Ober C., Freinkel N. Frequency of diabetes mellitus in mothers of probands with gestational diabetes Possible maternal influence on the predisposition to gestational diabetes . Am J Obstet Gynecol. 151:1985;471-475.
5. Plagemann A., Harder T., Kohlhoff R., Rohde W., Dorner G. Overweight and obesity in infants of mothers with long-term insulin-dependent diabetes or gestational diabetes. Int J Obesity Related Metab Disord. 21:1997;451-456.
6. Pettitt D.J., Aleck K.A., Baird H.R., Carraher M.J., Bennett P.H., Knowler W.C. Congenital susceptibility to NIDDM. Role of intra-uterine environment. Diabetes. 37:1988;622-628.
7. Silverman B.L., Metzger B.E., Cho N.H., Loeb C.A. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care. 18:1995;611-617.
8. Young L.E., Fairburn H.R. Improving the safety of embryo technologies Possible role of genomic imprinting . Theriogenology. 53:2000;627-648.
9. Young L.E. Imprinting of genes and the Barker hypothesis. Twin Res. 4:2001;307-317.
10. Hattersley A.T., Beards F., Ballantyne E., Appleton M., Harvey R., Ellard S. Mutations in the glucokinase gene of the fetus result in reduced birth weight. Nat Genet. 19:1998;268-270.
11. Pettitt D.J., Baird H.R., Aleck K.A., Bennett P.H., Knowler W.C. Excessive obesity in offspring of Pima Indian women with diabetes during pregnancy. N Engl J Med. 308:1983;242-245.
12. Gerlini G., Arachi S., Gori M.G., et al. Developmental aspects of the offspring of diabetic mothers. Acta Endocrinol. 277:(Suppl):1986;150-155.
13. Silverman B.L., Rizzo T., Green O.C., et al. Long-term prospective evaluation of offspring of diabetic mothers. Diabetes. 40:(Suppl 2):1991;121-125.
14. Harlan W.R. Epidemiology of childhood obesity. A national perspective. Ann N Y Acad Sci. 699:1993;1-5.
15. Berenson G.S., Dalferes E. Jr, Savage D., Webber L.S., Bao W. Ambulatory blood pressure measurements in children and young adults selected by high and low casual blood pressure levels and parental history of hypertension The Bogalusa Heart Study . Am J Med Sci. 305:1993;374-382.
16. Phipps K., Barker D.J., Hales C.N., Fall C.H., Osmond C., Clark P.M. Fetal growth and impaired glucose tolerance in men and women. Diabetologia. 36:1993;225-228.
17. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phipps K., Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X) Relation to reduced fetal growth . Diabetologia. 36:1993;62-67.
18. Eriksson U., Jansson L. Diabetes and pregnancy Decreased blood flow and disturbed fetal development in the rat . Pediatr Res. 18:1984;735-738.
19. Rosso P., Kava R. Effects of food restriction on cardiac output and blood flow to the uterus and placenta in the pregnant rat. J Nutr. 110:1980;2350-2354.
20. Ikawa H., Irahara M., Matsuzaki T., Saito S., Saito T., Aono T. Impaired induction of prolactin secretion from the anterior pituitary by suckling in streptozotocin-induced diabetic rats. Acta Endocrinol. 126:1992;167-172.
21. Rasmussen K.M., Warman N.L. Effect of maternal malnutrition during the reproductive cycle on growth and nutritional status of suckling rat pups. Am J Clin Nutr. 38:1983;77-83.
22. Aerts L., Van Assche F.A. Rat foetal endocrine pancreas in experimental diabetes. J Endocrinol. 73:1977;339-346.
23. Aerts L., Van Assche F.A. Is gestational diabetes an acquired condition? J Dev Biol. 1:1979;219-225.
24. Aerts L., Van Bree R., Feytons V., Rombauts W., Van Assche F.A. Plasma amino acids in diabetic pregnant rats and in their fetal and adult offspring. Biol Neonate. 56:1989;31-39.
25. Aerts L., Holemans K., Van Assche F.A. Maternal diabetes during pregnancy Consequences for the offspring . Diab Metab Rev. 6:1990;147-167.
26. Aerts L., Vercruysse L., Van Assche F.A. The endocrine pancreas in virgin and pregnant offspring of diabetic pregnant rats. Diab Res Clin Pract. 38:1997;9-19.
27. Holemans K., Aerts L., van Assche F.A. Evidence for an insulin resistance in the adult offspring of streptozotocin-diabetic pregnant rats. Diabetologia. 34:1991;81-85.
28. Holemans K., Aerts L., Van Assche F.A. Absence of pregnancy-induced alterations in tissue insulin sensitivity in the offspring of diabetic rats. J Endocrinol. 131:1991;387-393.
29. Holemans K., Van Bree R., Verhaeghe J., Aerts L., Van Assche F.A. In vivo glucose utilization by individual tissues in virgin and pregnant offspring of severely diabetic rats. Diabetes. 42:1993;530-556.
30. Holemans K., Gerber R.T., Meurrens K., De Clerck F., Poston L., Van Assche F.A. Streptozotocin diabetes in the pregnant rat induces cardiovascular dysfunction in adult offspring. Diabetologia. 42:1999;81-89.
31. Kervran A., Guillaume M., Jost A. The endocrine pancreas of the fetus from diabetic pregnant rat. Diabetologia. 15:1978;387-393.
32. Mulay S., Solomon S. Influence of streptozotocin-induced diabetes in pregnant rats on plasma corticosterone and progesterone levels and on cytoplasmic glucocorticoid receptors in fetal tissues. J Soc Gynecol Invest. 96:1983;335-345.
33. Oh W., Gelardi N.L., Cha C.J. Maternal hyperglycemia in pregnant rats Its effect on growth and carbohydrate metabolism in the offspring . Metabolism. 37:1988;1146-1151.
34. Ryan E.A., Liu D., Bell R.C., Finegood D.T., Crawford J. Long term consequences in offspring of diabetes in pregnancy Studies with syngeneic islet-transplanted streptozotocin-diabetic rats . Endocrinology. 136:1995;5587-5592.
35. Mulay S., Philip A., Solomon S. Influence of maternal diabetes on fetal rat development Alteration of insulin receptors in fetal liver and lung . J Endocrinol. 98:1983;401-410.
36. Canavan J.P., Goldspink D.F. Maternal diabetes in rats II. Effects on fetal growth and protein turnover. Diabetes. 37:1988;1671-1677.
37. Grill V., Johansson B., Jalkanen P., Eriksson U.J. Influence of severe diabetes mellitus early in pregnancy in the rat Effects on insulin sensitivity and insulin secretion in the offspring . Diabetologia. 34:1991;373-378.
38. Devaskar S., McMenamy K., Holtzclaw L., Sadiq F. Long-term maternal-fetal exposure to high-low insulin concentrations alter liver but not brain insulin receptors. Am J Obstet Gynecol. 163:1990;1350-1356.
39. Ktorza A, Gauguier D, Bihoreau MT, Berthault MF, Picon L. Adult offspring from mildly hyperglycemic rats show impairment of glucose regulation and insulin secretion which is transmissible to the next generation. In: Shafrir E, ed. Frontiers in diabetic research. Lessons from animal diabetes. London: Smith-Gordon and Company, Ltd. 1990:555-60.
40. Bihoreau M.T., Ktorza A., Kervran A., Picon L. Effect of gestational hyperglycemia on insulin secretion in vivo and in vitro by fetal rat pancreas. Am J Physiol. 251:1986;E86-91.
41. Bihoreau M.T., Ktorza A., Picon L. Gestational hyperglycemia and insulin release by the fetal rat pancreas in vitro Effect of amino-acids and glyceraldehydes . Diabetologia. 29:1986;434-439.
42. Schroeder R.E., Doria-Medina C.L., Das U.G., Sivitz W.I., Devaskar S.U. Effect of maternal diabetes upon fetal rat myocardial and skeletal muscle glucose transporters. Pediatr Res. 41:1997;11-19.
43. Copeland A.D., Hendrich C.E., Porterfield S.P. Distribution of free amino acids in streptozotocin-induced diabetic pregnant rats, their placentae and fetuses. Horm Metab Res. 22:1990;65-70.
44. Lane R.H., MacLennan N.K., Hsu J.L., Janke S.M., Pham T.D. Increased hepatic peroxisome proliferator-activated receptor-gamma coactivator-1 gene expression in a rat model of intrauterine growth restriction and subsequent insulin resistance. Endocrinology. 143:2002;2486-2490.
45. Johnstone M.T., Creager S.J., Scales K.M., Cusco J.A., Lee B.K., Creager M.A. Impaired endothelium-dependent vasodilatation in patients with insulin-dependent diabetes mellitus. Circulation. 88:1993;2510-2516.
46. Taylor P.D., McCarthy A.L., Thomas C.R., Poston L. Endothelium-dependent relaxation and noradrenaline sensitivity in mesenteric arteries of streptozotocin-induced diabetic rats. Br J Pharmacol. 107:1992;393-399.
47. Goode G.K., Heagerty A.M. In vitro responses of human peripheral small arteries in hypercholesterolemia and effects of therapy. Circulation. 91:1995;2898-2903.
48. Girerd X.J., Hirsch A.T., Cooke J.P., Dzau V.J., Creager M.A. L-arginine augments endothelium-dependent vasodilation in cholesterol-fed rabbits. Circ Res. 67:1990;1301-1308.
49. Aerts L., Van Assche F.A. Ultrastructural evaluation of B-cell recruitment in virgin and pregnant offspring of diabetic mothers. Diab Res Clin Pract. 41:1998;9-14.
50. Holemans K., Gerber R.T., O'Brian-Coker I., Mallet A., Van Assche F.A., Poston L. Raised saturated fat intake worsens vascular function in virgin and pregnant offspring of streptozotocin-diabetic rats. Br J Nutr. 84:2000;285-296.
51. Hunt J.V., Dean R.T., Wolff S.P. Hydroxyl radical production and autoxidative glycosylation Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus and ageing . Biochem J. 256:1988;205-212.
52. Holemans K., Verhaeghe J., Dequeker J., Van Assche F.A. Insulin sensitivity in adult female offspring of rats subjected to malnutrition during the perinatal period. J Soc Gynecol Invest. 3:1996;71-77.
53. Holemans K., Van Bree R., Verhaeghe J., Van Assche F.A. Maternal undernutrition and streptozotocin-diabetes in the rat have different effects on in vivo glucose uptake by peripheral tissues in their female adult offspring. J Nutr. 127:1997;1371-1376.
54. Holemans K., Gerber R.T., Meurrens K., De Clerck F., Poston L., Van Assche F.A. Maternal food restriction in the second half of pregnancy affects vascular function but not blood pressure of rat female offspring. Br J Nutr. 81:1999;73-79.
55. Garofano A., Czernichow P., Bréant B. In utero undernutrition impairs rat beta-cell development. Diabetologia. 40:1997;1231-1234.
56. Garofano A., Czernichow P., Bréant B. Beta cell mass and proliferation following late fetal and early postnatal malnutrition in the rat. Diabetologia. 41:1998;1114-1120.
57. Garofano A., Czernichow P., Bréant B. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia. 42:1999;711-718.
58. Woodall S.M., Johnston B.M., Breier B.H., Gluckman P.D. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res. 40:1996;438-443.
59. Olausson H., Uvnas-Moberg K., Sohlstrom A. Postnatal oxytocin alleviates adverse effects in adult rat offspring caused by maternal malnutrition. Am J Physiol Endocrinol Metab. 284:2003;E475-480.
60. Langley S.C., Jackson A.A. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci. 86:1994;217-222.
61. Langley-Evans S.C., Nwagwu M. Impaired growth and increased glucocorticoid sensitive enzyme activities in tissues of rat fetuses exposed to maternal low protein diets. Life Sci. 63:1998;605-615.
62. Dahri S., Snoeck A., Reusens-Billen B., Remacle C., Hoet J.J. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes. 40:1991;115-120.
63. Dahri S., Reusens B., Remacle C., Hoet J.J. Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proc Nutr Soc. 54:1995;345-356.
64. Swenne I., Crace C.J., Milner R.D. Persistent impairment of insulin secretory response to glucose in adult rats after limited period of protein-calorie malnutrition early in life. Diabetes. 36:1987;454-458.
65. Snoeck A., Remacle C., Reusens B., Hoet J.J. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate. 57:1990;107-118.
66. Lewis R.M., Petry C.J., Ozanne S.E., Hales C.N. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring. Metabolism. 50:2001;562-567.
67. De Prins F.A., Van Assche F.A. Intra-uterine growth restriction and development of endocrine pancreas in the experimental rat. Biol Neonate. 41:1982;16-21.
68. De Prins F.A., Van Assche F.A. Insulin levels in amniotic fluid and fetal growth. Padiatr Padol. 17:1982;223-229.
69. De Prins F.A., Van Assche F.A., Milner R.D.G. C-peptide levels in amniotic fluid in experimental fetal growth restriction. Biol Neonate. 43:1983;181-185.
70. Jansson T., Lambert G.W. Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous system activity in the rat at 3-4 months of age. J Hypertens. 17:1999;1239-1248.
71. Ogata E.S., Bussey M.E., Finley S. Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism. 35:1986;970-977.
72. Leturque A., Hauguel S., Revelli J.P. Fetal glucose utilization in response to maternal starvation and acute hyperketonemia. Am J Physiol. 256:1989;E699-E703.
73. Simmons R.A., Gounis A.S., Bangalore S.A., Ogata E.S. Intrauterine growth retardation Fetal glucose transport is diminished in lung but spared in the brain . Pediatr Res. 31:1992;59-63.
74. Liechty E.A., Lemons J.A. Changes in ovine fetal hindlimb amino acid metabolism during maternal fasting. Am J Physiol. 246:1984;E430-435.
75. Girard J., Ferre P., Gilbert M., Kervran A., Assan R., Marliss E.B. Fetal metabolic response to maternal fasting in the rat. Am J Phisiol. 232:1977;E456-463.
76. Fowden A.L., Mijovic J., Silver M. The effects of cortisol on hepatic and renal gluconeogenic enzyme activities in the sheep fetus during late gestation. J Endocrinol. 137:1993;213-222.
77. Houdijk E.C., Engelbregt M.J., Popp-Snijders C., Delemarre-van de Waal H.A. Endocrine regulation and extended follow up of longitudinal growth in intrauterine growth-retarded rats. J Endocrinol. 166:2000;599-608.
78. Simmons R.A., Templeton L.J., Gertz S.J. Intrauterine growth restriction leads to the development of type 2 diabetes in the rat. Diabetes. 50:2001;2279-2286.
79. Engelbregt M.J., Houdijk M.E., Popp-Snijders C., Delemarre van de Waal H.A. The effects of intra-uterine growth restriction and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res. 48:2000;803-807.
80. Blondeau B., Garofano A., Czernichow P., Bréant B. Age-dependent inability of the endocrine pancreas to adapt to pregnancy A long-term consequence of perinatal malnutrition in the rat . Endocrinology. 140:1999;4208-4213.
81. Hales C.N., Desai M., Ozanne S.E., Crowther N.J. Fishing in the stream of diabetes From measuring insulin to the control of fetal organogenesis . Biochem Soc Trans. 24:1996;341-350.
82. Holness M.J. Impact of early growth retardation on glucoregulatory control and insulin action in mature rats. Am J Physiol. 270:1996;E946-954.
83. Petry C.J., Ozanne S.E., Wang C.L., Hales C.N. Effects of early protein restriction and adult obesity on rat pancreatic hormone content and glucose tolerance. Horm Metab Res. 32:2000;233-239.
84. Wilson M.R., Hughes S.J. The effect of maternal protein deficiency during pregnancy and lactation on glucose tolerance and pancreatic islet function in adult rat offspring. J Endocrinol. 154:1997;177-185.
85. Desai M., Byrne C.D., Zhang J., Petry C.J., Lucas A., Hales C.N. Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. Am J Physiol. 272:1997;G1083-1090.
86. Ozanne S.E., Smith G.D., Tikerpae J., Hales C.N. Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am J Physiol. 270:1996;E559-564.
87. Langley-Evans S.C. Critical difference between two low protein diet protocols in the programming of hypertension in the rat. Int J Food Sci Nutr. 51:2000;11-17.
88. Avril I., Blondeau B., Duchene B., Czernikow P., Bréant B. Decreased β-cell proliferation impairs the adaptation to pregnancy in rats malnourished during perinatal life. J Endocrinol. 174:2002;215-223.
89. Holness M.J., Sugden M.C. Suboptimal protein nutrition in early life later influences insulin action in pregnant rats. Diabetologia. 39:1996;12-21.
90. Hales C.N., Barker D.J. Type 2 (non-insulin-dependent) diabetes mellitus The thrifty phenotype hypothesis . Diabetologia. 35:1992;595-601.
91. Neel J.V. Diabetes mellitus A thrifty genotype rendered detrimental by "progress"? Am J Hum Genet. 14:1962;353-362.
92. Edwards C.R.W., Benediktsson R., Lindsay R., Seckl J.R. Dysfunction of the placental glucocorticoid barrier A link between fetal environment and adult hypertension . Lancet. 341:1993;355-357.
93. Lindsay R.S., Lindsay R.M., Waddell B.J., Seckl J.R. Prenatal glucocorticoid exposure leads to hyperglycemia in the rat Studies with 11β-hydroxysteroid dehydrogenase inhibitor carbenoxolone . Diabetologia. 39:1996;1299-1305.
94. Reinisch J.M., Simon N.G., Karow W.G., Gandleman R. Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science. 202:1978;436-438.
95. Ward R.M. Pharmacologic enhancement of fetal lung maturation. Clin Perinatol. 21:1994;523-542.
96. Cole T.J., Blendy J.A., Monaghan A.P., Schmid W., Aguzzi A., Schutz G. Molecular genetic analysis of glucocorticoid signaling during mouse development. Steroids. 60:1995;93-96.
97. Moss T.J., Sloboda D.M., Gurrin L.C., Harding R., Challis J.R., Newnham J.P. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol. 281:2001;R960-970.
98. Celsi G., Kistner A., Aizman R., et al. Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr Res. 44:1998;317-322.
99. Seckl J.R., Cleasby M., Nyirenda M.J. Glucocorticoids, 11β-hydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 57:2000;1412-1417.
100. Benediktsson R., Calder A.A., Edwards C.R., Seckl J.R. Placental 11 beta-hydroxysteroid dehydrogenase A key regulator of fetal glucocorticoid exposure . Clin Endocrinol. 46:1997;161-166.
101. Brown R.W., Diaz R., Robson A.C., et al. The ontogeny of 11 beta-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development. Endocrinology. 137:1996;794-797.
102. Lesage J., Blondeau B., Grino M., Breant B., Dupouy J.P. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth restriction, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology. 142:2001;1692-1702.
103. Bertram C., Trowern A.R., Copin N., Jackson A.A., Whorwood C.B. The maternal diet during pregnancy programs altered expression on the glucocorticoid receptor and type 2 11beta-hydroxysteroid dehydrogenase Potential molecular mechanisms underlying the programming of hypertension in utero . Endocrinology. 142:2001;2841-2853.
104. Nyirenda M.J., Lindsay R.S., Kenyon C.J., Burchell A., Seckl J.R. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Investig. 101:1998;2174-2181.