Prenatal origin of obesity and their complications: Gestational diabetes, maternal overweight and the paradoxical effects of fetal growth restriction and macrosomia

Reproductive Toxicology

Volumn 32, Issue 2, 2011, Pages 205-212

  Ornoy, Asher ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

Epigenetic changes; FGR; GDM; Hypothalamus; Insulin; Leptin; Macrosomia; Maternal overweight; Metabolic syndrome; PGDM

Indexed keywords

LEPTIN;

ARTICLE; BIRTH WEIGHT; BLOOD GLUCOSE MONITORING; CARDIOVASCULAR DISEASE; CONGENITAL MALFORMATION; DIET RESTRICTION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE COURSE; EPIGENETICS; FETUS DEATH; GENETIC ASSOCIATION; HUMAN; HYPERLEPTINEMIA; HYPERTENSION; HYPOTHALAMUS DISEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; MACROSOMIA; METABOLIC SYNDROME X; NEUROLOGIC DISEASE; NEWBORN DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PHYSICAL ACTIVITY; PREGNANCY DIABETES MELLITUS; PROTEIN FUNCTION; SPONTANEOUS ABORTION;

DIABETES, GESTATIONAL; EPIGENESIS, GENETIC; FEMALE; FETAL GROWTH RETARDATION; FETAL MACROSOMIA; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFANT, NEWBORN; INFANT, SMALL FOR GESTATIONAL AGE; METABOLIC SYNDROME X; OBESITY; OVERWEIGHT; PITUITARY-ADRENAL SYSTEM; PREGNANCY;

EID: 79960847990     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.05.002     Document Type: Article

References (73)

1. Bouret S.G. Early life origins of obesity; role of hypothalamic programming. J Pediatric Gastro Nutr 2009, 48:S31-S38.
2. Ergaz Z., Avgil M., Ornoy A. Intrauterine growth restriction; etiology and consequences: what do we know about the human situation and experimental animal models. Reprod Toxicol 2005, 20:301-322.
3. World Health Organization. Obesity: preventing and managing a global epidemic. World Health Organization Tech. Report 2000;894:1-4.
4. Lazar M.A. How obesity causes diabetes: not a tall tale. Science 2005, 307:373-375.
5. Reaven G.M. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988, 37:1595-1607.
6. Hales C.N., Barker D.J. The thrifty phenotype hypothesis. Br Med Bull 2001, 60:5-20.
7. Barker D.J., Eriksson J.G., Forsen T., Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 2002, 31:1235-1239.
8. Beck B. Neuropeptides and obesity. Nutrition 2000, 16:916-923.
9. Karlberg J., Albertsson-Wikland K. Growth in full-term small-for-gestational age infants: from birth to final height. Pediatr Res 1995, 38:733-739.
10. Sas T., de Waal W., Mulder P., Houdijk M., Jansen M., Reeser M., et al. Growth hormone treatment in children with short stature born small for gestational age: 5-year results of a randomized, double-blind, dose-response trial. J Clin Endocrinol Metab 1999, 84:3064-3070.
11. Henriksen T. The macrosomic fetus: a challenge in current obstetrics. Acta Obstet Gynecol Scand 2008, 87:134-145.
12. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phillips K., Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993, 36:62-67.
13. Kanaka-Gantenbein C., Mastorakos G., Chrousos G.P. Endocrine-related causes and consequences of intrauterine growth retardation. Ann NY Acad Sci 2003, 997:150-157.
14. Newsome C.A., Shiell A.W., Fall Ch., Osmond Phillips D.I., Shier R., Law C.M. Is birth weight related to later glucose and insulin metabolism? A systematic review. Diabet Med 2003, 20:339-348.
15. Jornayvaz F.R., Selz R., Tappy L., Theinz G.E. Metabolism of oral glucose in children born small for gestational age: evidence for an impaired whole body glucose oxidation. Metabolism 2004, 53:847-851.
16. Eriksson J.G., Forsen T., Tuomilehto J., Osmond C., Barker D.J. Early adiposity rebound in childhood and risk of Type 2 diabetes in adult life. Diabetologia 2003, 46:190-194.
17. Osmond C., Barker D.J., Winter P.D., Fall C.H., Simmonds S.J. Early growth and death from cardiovascular disease in women. BMJ 1993, 307:1519-1524.
18. Stein C.E., Fall Ch., Kumaran K., Osmond C., Cox V., Barker D.J. Fetal growth and coronary heart disease in south India. Lancet 1996, 348:1269-1273.
19. Tenhola S., Martikainen A., Rahiala E., Herrgard E., Halonen P., Voutilainen R. Serum lipid concentrations and growth characteristics in 12-year-old children born small for gestational age. Pediatr Res 2000, 48:623-628.
20. Barker D.J., Martin C.N., Osmond C., Hales C.N., Fall C.H. Growth in utero and serum cholesterol concentrations in adult life. BMJ 1993, 307:1524-1527.
21. Crispi F., Bijnens B., Figuera F., Bartrons J., Eixsarch E., Le Noble F., et al. Fetal growth restriction results in remodeled and less eficient hearts in children. Circulation 2010, 121:2427-2436.
22. Clark P.M., Hindsmarch P.C., Shiel A.W., Law C.M., Honour J.W., Barker D.J. Size at birth and adrenocortical function in childhood. Clin Endocrinol (Oxf) 1996, 45:721-726.
23. Dahlgren J., Boguszewski M., Rosberg S., Albertson-wikland K. Adrenal steroid hormones in short children born small for gestational age. Clin Endocrinol (Oxf) 1998, 49:353-361.
24. Lienhardt A., Carel J.C., Preux P.M., Coutant R., Chaussain JLl. Amplitude of pubertal growth in short stature children with intrauterine growth retardation. Horm Res 2002, 57(Suppl. 2):88-94.
25. Ibanez L., Potau N., Enriquez G., Marcos M.V., de Zegher F. Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age. Hum Reprod 2003, 18:1565-1569.
26. Ibanez L., Potau N., Ferrer A., Rodriguez- Hierro F., Marcos M.V., de Zegher F. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocrinol Metab 2002, 87:3391-3393.
27. Goto M.P., Goldman A.S. Diabetic embryopathy. Curr Opin Pediatr 1994, 6:486-491.
28. Hod M., Diamant Y.Z. The offspring of a diabetic mother-short and long range implications. Isr J Med Sci 1992, 28:81-86.
29. Sheffield J.S., Butler-Koster E.L., Casey B.M., Mcintire D.D., Leveno K.J. Maternal diabetes mellitus and infant malformations. Obstet Gynecol 2002, 100:p925-930.
30. Eriksson U.J., Cederberg J., Wentzel P. Congenital malformations in offspring of diabetic mothers: animal and human studies. Rev Endocr Metab Disord 2003, 4:79-93.
31. Ornoy A., Ratzon N., Greenbaum C., Peretz E., Soriano D., Dulizky Ml. Neurobehavior of school age children born to diabetic mothers. Arch Dis Child 1998, 79:F94-F99.
32. Ornoy A., Wolf A., Ratzon N., Greenbaum C., Dulitzky M. Neurodevelopmental impact of diabetic alterations on early school-age children born to mothers with gestational diabetes. Arch Dis Child 1999, 81:F11-F16.
33. Yogev Y., Visser G.H.A. Obesity, gestational diabetes and pregnancy outcome. Semin Fetal Neonatal Med 2009, 14:77-84.
34. Gillman M.W., Rifas-Shiman S., Berkey C.S., Field A.E., Colditz G.A. Maternal gestational diabetes, birth weight and adolescent obesity. Pediatrics 2003, 111:e221-e226.
35. Silverman B.I., Cho N.H., Rizzo T.A., Metzger B.E. Long-term effects of the intrauterine environment. Diabetes Care 1998, 21:B142-B148.
36. Boney C.M., Verma A., Tucker R., Vohr B.R. Metabolic syndrome in childhood: association with birth weight, maternal obesity and gestational diabetes mellitus. Pediatrics 2005, 115:e290-e296.
37. Nohr E.A., Bech B.H., Davies M.J., Frydenberg M., Hemriksen T.B., Olsen J. Pre-pregnancy obesity and fetal death. A study within the Danish National Birth Cohort. Obst Gynecol 2005, 106:250-259.
38. Fall C.H., Stein C.E., Kumaran K., Osmond C., Barker D.J., Hales C.N. Size at birth, maternal weight, and type 2 diabetes in south India. Diabet Med 1998, 15:220-227.
39. Sinha R., Fish G., Teague B., Tamborlane W.V., Banyas B., Allen K., et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N Engl J Med 2002, 315:802-810.
40. Pirkola J., Pouta A., Bloigu A., Hartikainen A.L., Laitinen J., Jarvelin M.R., et al. Risks of overweight and abdominal obesity at age 16 years associated with prenatal exposure to maternal pre-pregnancy overweight and gestational diabetes mellitus. Diabetes Care 2010, 33:1115-1121.
41. Iwashima S., Nakagawa Y., Ishikawa T., Satake S.S., Nagata E., Ohzeki T. Abdominal obesity is associated with cardiovascular risk in Japanese children and adolescents. J Pediatr Endocrinol Metab 2011, 24:51-54.
42. Hales C.N., Barker D.J. Type 2 (non-insulin-dependent) diabetes mellitus; the thrifty phenotype hypothesis. Diabetologia 1992, 35:595-601.
43. Eriksson J.G., Forsen T., Toumilheto J., Jaddoe V.W., Osmond C., Barker D.J. Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 2002, 45:342-348.
44. 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 1993, 36:62-67.
45. Jensen C.B., Storgaard H., Dela F., Holst H., Madsbad S., Vaag A.A. Early differential defects of insulin secretion and action in 19-year-old caucasian men who had low birth weight. Diabetes 2002, 51:1271-1280.
46. Ravelli A.C., va der Meulen J.H., Michels R.P., Osmond C., Barker D.J., Hales C.N., et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 1998, 351:173-177.
47. Yajnik C.S. Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J Nutr 2004, 134:205-210.
48. Bush N.C., Chandler-Laney P.C., Rouse D.J., Granger W.M., Oster R.A., Gower B.A. Higher. Maternal gestational glucose concentration is associated with lower offspring insulin sensitivity and altered {beta}-cell function. Clin Endocrinol Metab 2011, 96. E803-9.
49. Kanaka-Gantenbein C. Fetal origin of adult diabetes. Ann NY Acad Sci 2010, 1205:99-105.
50. Singh B.S., Westfall T.C., Devascar S.U. Maternal diabetes induced hyperglycemia and acute intracerebral hyperinsulinism supress fetal brain neuropeptide Y concentrations. Endocrinology 1997, 138:963-969.
51. Montague C.T., Farooqi I.S., Whitehead J.P., Soos M.A., Rau H., Wareham N.J., et al. Congenital leptin deficiency is associated with severe early-onset obesity in humans. Nature 1997, 387:903-908.
52. Clement K., Vaisse C., Lahlou N., Cabrol S., Pelloux V., Cassuto D., et al. A mutation in the human leptin receptor gene causes obesity and pituitary dysfunction. Nature 1998, 392:398-401.
53. Qswal A., Yeo G. Leptin and control of body weight: a review of its diverse central targets, signalling mechanism and role in the pathogenesis of obesity. Obesity 2010, 18:221-228.
54. Persson B., Westgren M., Celsi G., Nord E., Ortqvist E. Leptin concentrations in cord blood in normal newborn infants and offspring of diabetic mothers. Hoem Metab Res 1999, 31:467-471.
55. Myers M.G., Petti M.E., Leshan R.L. Hitting the target: leptin and perinatal nutrition in the predisposition to obesity. Endocrinology 2005, 246:4209-4210.
56. Tranchand-Bunel D., Delbende C., Guy J., Jegou S., Jenks B.L., Mocaer E., et al. Pro-opiomelanocortin neuronal system. Rev Neurol (Paris) 1987, 143:471-489.
57. Koutcherov Y. Organization of human hypothalamus in fetal development. J Comp Neurol 2002, 446:301-324.
58. Coupe B., Amarger V., Grit I., Benani A., Parnet P. Nutritional programming affects hypothalamic organization and early response to leptin. Endocrinology 2010, 151:702-713.
59. Szyf M. Epigenetics, DNA methylation, and chromatin modifying drugs. Annu Rev Pharmacol Toxicol 2009, 49:243-263.
60. Sinclair K.D., Lea R.G., Rees W.D., Young L.E. The developmental origins of health and disease: current theories and epigenetic mechanisms. Soc Reprod Fertil Suppl 2007, 64:425-443.
61. Simmons R.A. Developmental origins of diabetes: the role of epigenetic mechanisms. Curr Opin Endocrinol Diabetes Obes 2007, 14:13-16.
62. Park J.H., Stoffers D.A., Nicholls R.D., Simmons R.A. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest 2008, 118:2316-2324.
63. Williams K.T., Garrow T.A., Schalinske K.L. Type I diabetes leads to tissue-specific DNA hypomethylation in male rats. J Nutr 2008, 138:2064-2069.
64. Ling C., Del Guerra S., Lupi R., Ronn T., Granhall C., et al. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 2008, 51:615-622.
65. Ornoy A., Zivanit E., Guillemin C., Stodgell C., Miller R.K., Szyf M. Diabetic embryopathy: the roles of hyperglycemia, oxidative stress and copper deficiency in the induction of genetic and epigenetic changes. Reprod Toxicol 2011, 31:249-250. [abstract].
66. Gluckman P.D., Hanson M.A. Developmental and epigenetic pathways to obesity: an evolutionary-developmental perspective. Int J Obes 2008, 32:562-571.
67. Stevens A., Begun G., White A. Epigenetic changes in the hypothalamic pro-opiomelanocortin gene: a mechanism linking maternal undernutrition to obesity in the offspring. Eur J Pharmacol 2011, 660:194-201.
68. Coupé B, Delamaire E, Hoebler C, Grit I, Even P, Fromentin G, et al. Hypothalamus integrity and appetite regulation in low birth weight rats reared artificially on a high-protein milk formula. J Nutr Biochem; in press.
69. Stevens A., Begum G., Cook A., Connor K., Rumball C., Oliver M., et al. Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology 2010, 151:3652-3664.
70. Tamashiro K.L.K., Terrillion C.Y., Hyun J., Koenig J.I., Moran T.H. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 2009, 58:1116-1126.
71. Tamashiro K.L.K., Moran T.H. Perinatal environment and its influence on metabolic programming of offspring. Physiol Behav 2010, 100:560-566.
72. Heindel J.J., vom Saal F.S. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol Cell Endocrinol 2009, 3/4:90-96.
73. Manios Y., Moschonis G., Grammatikaki E., Anastasiadou A., Liarigkovinos T. Determinants of childhood obesity and association with maternal perceptions of their children's weight status: the "GENESIS" study. J Am Diet Assoc 2010, 110:1527-1531.