Long-term metabolic consequences of being born small for gestational age

References

• Wollmann H. Intrauterine growth restriction: definition and etiology. Horm. Res.49, 1–6 (1998).
   Web of Science ®Google Scholar
• Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br. Med. J.298, 564–567 (1989).
   PubMed Web of Science ®Google Scholar
• Barker DJ. Fetal origins of coronary heart disease. Br. Med. J.311, 171–174 (1995).
   PubMed Web of Science ®Google Scholar
• Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet2, 577–580 (1989).
   PubMed Web of Science ®Google Scholar
• Hales CN, Barker DJ, Clark PM et al. Fetal and infant growth and impaired glucose tolerance at age 64. Br. Med. J.303, 1019–1022 (1991).
   PubMed Web of Science ®Google Scholar
• Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia36, 62–67 (1993).
   PubMed Web of Science ®Google Scholar
• Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. Br. Med. J.307, 1524–1527 (1993).
   PubMed Web of Science ®Google Scholar
• Fall CH, Barker DJ, Osmond C, Winter PD, Clark PM, Hales CN. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. Br. Med. J.304, 801–805 (1992).
   PubMed Web of Science ®Google Scholar
• Phipps K, Barker DJ, Hales CN, Fall CH, Osmond C, Clark PM. Fetal growth and impaired glucose tolerance in men and women. Diabetologia36, 225–228 (1993).
   PubMed Web of Science ®Google Scholar
• McCance DR, Pettitt DJ, Hanson RL, Jacobsson LT, Knowler WC, Bennett PH. Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype, or surviving small baby genotype? Br. Med. J.308, 942–945 (1994).
   PubMed Web of Science ®Google Scholar
• Valdez R, Athens MA, Thompson GH, Bradshaw BS, Stern MP. Birthweight and adult health outcomes in a biethnic population in the USA. Diabetologia37, 624–631 (1994).
   PubMed Web of Science ®Google Scholar
• Curhan GC, Chertow GM, Willett WC et al. Birth weight and adult hypertension and obesity in women. Circulation94, 1310–1315 (1996).
   PubMed Web of Science ®Google Scholar
• Leger J, Levy-Marchal C, Bloch J et al. Reduced final height and indications for insulin resistance in 20 year olds born small for gestational age: regional cohort study. Br. Med. J.315, 341–347 (1997).
   PubMed Web of Science ®Google Scholar
• Lithell HO, McKeigue PM, Berglund L, Mohsen R, Lithell UB, Leon DA. Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50–60 years. Br. Med. J.312, 406–410 (1996).
   Google Scholar
• Leibson CL, Burke JP, Ransom JE et al. Relative risk of mortality associated with diabetes as a function of birth weight. Diabetes Care.28, 2839–2843 (2005).
   PubMed Web of Science ®Google Scholar
• Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics115, E290–E296 (2005).
   PubMed Web of Science ®Google Scholar
• Garofano A, Czernichow P, Breant B. β-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat. Diabetologia41, 1114–1120 (1998).
   PubMed Web of Science ®Google Scholar
• Bertin E, Gangnerau MN, Bailbe D, Portha B. Glucose metabolism and β-cell mass in adult offspring of rats protein and/or energy restricted during the last week of pregnancy. Am. J. Physiol.277, E11–E17 (1999).
   PubMed Web of Science ®Google Scholar
• Jensen CB, Storgaard H, Dela F, Holst JJ, Madsbad S, Vaag AA. Early differential defects of insulin secretion and action in 19-year-old caucasian men who had low birth weight. Diabetes51, 1271–1280 (2002).
   PubMed Web of Science ®Google Scholar
• 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. Metabolism53, 904–911 (2004).
   PubMed Web of Science ®Google Scholar
• Phillips DI, Hirst S, Clark PM, Hales CN, Osmond C. Fetal growth and insulin secretion in adult life. Diabetologia37, 592–596 (1994).
   PubMed Web of Science ®Google Scholar
• Wills J, Watson JM, Hales CN, Phillips DI. The relation of fetal growth to insulin secretion in young men. Diabetes Med.13, 773–774 (1996).
   PubMed Web of Science ®Google Scholar
• Bavdekar A, Yajnik CS, Fall CH et al. Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8 years, or both? Diabetes48, 2422–2429 (1999).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Chevenne D, Czernichow P, Levy-Marchal C. No evidence for a major β-cell dysfunction in young adults born with intra-uterine growth retardation. Pediatr. Diabetes1, 181–185 (2000).
   PubMedGoogle Scholar
• Flanagan DE, Moore VM, Godsland IF, Cockington RA, Robinson JS, Phillips DI. Fetal growth and the physiological control of glucose tolerance in adults: a minimal model analysis. Am. J. Physiol. Endocrinol. Metab.278, E700–E706 (2000).
   PubMed Web of Science ®Google Scholar
• Schou JH, Pilgaard K, Vilsboll T et al. Normal secretion and action of the gut incretin hormones glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide in young men with low birth weight. J. Clin. Endocrinol. Metab.90, 4912–4919 (2005).
   PubMed Web of Science ®Google Scholar
• Beringue F, Blondeau B, Castellotti MC, Breant B, Czernichow P, Polak M. Endocrine pancreas development in growth-retarded human fetuses. Diabetes51, 385–391 (2002).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J. Clin. Endocrinol. Metab.85, 1401–1406 (2000).
   PubMed Web of Science ®Google Scholar
• Phillips DI, Barker DJ, Hales CN, Hirst S, Osmond C. Thinness at birth and insulin resistance in adult life. Diabetologia37, 150–154 (1994).
   PubMed Web of Science ®Google Scholar
• Hofman PL, Cutfield WS, Robinson EM et al. Insulin resistance in short children with intrauterine growth retardation. J. Clin. Endocrinol. Metab.82, 402–406 (1997).
   PubMed Web of Science ®Google Scholar
• Veening MA, Van Weissenbruch MM, Delemarre-Van De Waal HA. Glucose tolerance, insulin sensitivity, and insulin secretion in children born small for gestational age. J. Clin. Endocrinol. Metab.87, 4657–4661 (2002).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Deghmoun S, Chevenne D, Collin D, Czernichow P, Levy-Marchal C. Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth. Diabetologia48, 849–855 (2005).
   PubMed Web of Science ®Google Scholar
• Yajnik CS, Fall CH, Vaidya U et al. Fetal growth and glucose and insulin metabolism in four-year-old Indian children. Diabetes Med.12, 330–336 (1995).
   PubMed Web of Science ®Google Scholar
• Law CM, Gordon GS, Shiell AW, Barker DJ, Hales CN. Thinness at birth and glucose tolerance in seven-year-old children. Diabetes Med.12, 24–29 (1995).
   PubMed Web of Science ®Google Scholar
• Arends NJ, Boonstra VH, Duivenvoorden HJ, Hofman PL, Cutfield WS, Hokken-Koelega AC. Reduced insulin sensitivity and the presence of cardiovascular risk factors in short prepubertal children born small for gestational age (SGA). Clin. Endocrinol. (Oxford)62, 44–50 (2005).
   PubMed Web of Science ®Google Scholar
• 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.88, 3645–3650 (2003).
   PubMed Web of Science ®Google Scholar
• Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am. J. Clin. Nutr.72, 1101–1106 (2000).
   PubMed Web of Science ®Google Scholar
• Li C, Johnson MS, Goran MI. Effects of low birth weight on insulin resistance syndrome in caucasian and African-American children. Diabetes Care.24, 2035–2042 (2001).
   PubMed Web of Science ®Google Scholar
• Okosun IS, Dever GE, Choi ST. Low birth weight is associated with elevated serum lipoprotein(a) in white and black American children ages 5–11 years. Public Health116, 33–38 (2002).
   Web of Science ®Google Scholar
• Ong KK, Petry CJ, Emmett PM et al. Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth, and plasma insulin-like growth factor-I levels. Diabetologia47, 1064–1070 (2004).
   PubMed Web of Science ®Google Scholar
• Colle E, Schiff D, Andrew G, Bauer CB, Fitzhardinge P. Insulin responses during catch-up growth of infants who were small for gestational age. Pediatrics57, 363–371 (1976).
   PubMed Web of Science ®Google Scholar
• Blondeau B, Avril I, Duchene B, Breant B. Endocrine pancreas development is altered in foetuses from rats previously showing intra-uterine growth retardation in response to malnutrition. Diabetologia45, 394–401 (2002).
   PubMed Web of Science ®Google Scholar
• Ezzahir N, Alberti C, Deghmoun S et al. Time course of catch-up in adiposity influences adult anthropometry in individuals who were born small for gestational age. Pediatr. Res.58, 243–247 (2005).
   PubMed Web of Science ®Google Scholar
• Singhal A, Lucas A. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet363, 1642–1645 (2004).
   PubMed Web of Science ®Google Scholar
• Singhal A, Cole TJ, Fewtrell M, Lucas A. Breastmilk feeding and lipoprotein profile in adolescents born preterm: follow-up of a prospective randomised study. Lancet363, 1571–1578 (2004).
   PubMed Web of Science ®Google Scholar
• Owen CG, Whincup PH, Odoki K, Gilg JA, Cook DG. Infant feeding and blood cholesterol: a study in adolescents and a systematic review. Pediatrics110, 597–608 (2002).
   PubMed Web of Science ®Google Scholar
• Singhal A, Fewtrell M, Cole TJ, Lucas A. Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet361, 1089–1097 (2003).
   PubMed Web of Science ®Google Scholar
• Eriksson JG, Forsen T, Tuomilehto J, Osmond C, Barker DJ. Early growth and coronary heart disease in later life: longitudinal study. Br. Med. J.322, 949–953 (2001).
   PubMed Web of Science ®Google Scholar
• Forsen TJ, Eriksson JG, Osmond C, Barker DJ. The infant growth of boys who later develop coronary heart disease. Ann. Med.36, 389–392 (2004).
   PubMed Web of Science ®Google Scholar
• Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. Trajectories of growth among children who have coronary events as adults. N. Engl. J. Med.353, 1802–1809 (2005).
   PubMed Web of Science ®Google Scholar
• Gillman MW. Developmental origins of health and disease. N. Engl. J. Med.353, 1848–1850 (2005).
   PubMed Web of Science ®Google Scholar
• Engstrom E, Niklasson A, Wikland KA, Ewald U, Hellstrom A. The role of maternal factors, postnatal nutrition, weight gain, and gender in regulation of serum IGF-I among preterm infants. Pediatr. Res.57, 605–610 (2005).
   PubMed Web of Science ®Google Scholar
• Reilly JJ, Methven E, McDowell ZC et al. Health consequences of obesity. Arch. Dis. Child.88, 748–752 (2003).
   PubMed Web of Science ®Google Scholar
• Lapillonne A, Braillon P, Claris O, Chatelain PG, Delmas PD, Salle BL. Body composition in appropriate and in small for gestational age infants. Acta Paediatr.86, 196–200 (1997).
   PubMed Web of Science ®Google Scholar
• Enzi G, Zanardo V, Caretta F, Inelmen EM, Rubaltelli F. Intrauterine growth and adipose tissue development. Am. J. Clin. Nutr.34, 1785–1790 (1981).
   PubMed Web of Science ®Google Scholar
• Petersen S, Gotfredsen A, Knudsen FU. Lean body mass in small for gestational age and appropriate for gestational age infants. J. Pediatr.113, 886–889 (1988).
   PubMed Web of Science ®Google Scholar
• Hediger ML, Overpeck MD, Kuczmarski RJ, McGlynn A, Maurer KR, Davis WW. Muscularity and fatness of infants and young children born small- or large-for-gestational-age. Pediatrics102, E60 (1998).
   Web of Science ®Google Scholar
• Eriksson J, Forsen T, Tuomilehto J, Osmond C, Barker D. Size at birth, fat-free mass and resting metabolic rate in adult life. Horm. Metab. Res.34, 72–76 (2002).
   PubMed Web of Science ®Google Scholar
• Taylor DJ, Thompson CH, Kemp GJ et al. A relationship between impaired fetal growth and reduced muscle glycolysis revealed by 31P magnetic resonance spectroscopy. Diabetologia38, 1205–1212 (1995).
   PubMed Web of Science ®Google Scholar
• Dulloo AG. A role for suppressed skeletal muscle thermogenesis in pathways from weight fluctuations to the insulin resistance syndrome. Acta Physiol. Scand.184, 295–307 (2005).
   PubMedGoogle Scholar
• Barker M, Robinson S, Osmond C, Barker DJ. Birth weight and body fat distribution in adolescent girls. Arch. Dis. Child.77, 381–383 (1997).
   PubMed Web of Science ®Google Scholar
• Rasmussen EL, Malis C, Jensen CB et al. Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care.28, 151–153 (2005).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Leger J, Tabone MD, Czernichow P, Levy-Marchal C. High serum leptin concentrations during catch-up growth of children born with intrauterine growth retardation. J. Clin. Endocrinol. Metab.84, 1949–1953 (1999).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Relatively low serum leptin levels in adults born with intra-uterine growth retardation. Int. J. Obes. Relat. Metab. Disord.25, 491–495 (2001).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Deghmoun S, Chevenne D, Czernichow P, Levy-Marchal C. Low serum adiponectin levels in subjects born small for gestational age: impact on insulin sensitivity. Int. J. Obes. (Lond.)30(1), 83–87(2005).
   Web of Science ®Google Scholar
• Cianfarani S, Martinez C, Maiorana A, Scire G, Spadoni GL, Boemi S. Adiponectin levels are reduced in children born small for gestational age and are inversely related to postnatal catch-up growth. J. Clin. Endocrinol. Metab.89, 1346–1351 (2004).
   PubMed Web of Science ®Google Scholar
• Iniguez G, Soto N, Avila A et al. Adiponectin levels in the first two years of life in a prospective cohort: relations with weight gain, leptin levels and insulin sensitivity. J. Clin. Endocrinol. Metab.89, 5500–5503 (2004).
   PubMed Web of Science ®Google Scholar
• Boiko J, Jaquet D, Chevenne D, Rigal O, Czernichow P, Levy-Marchal C. In situ lipolytic regulation in subjects born small for gestational age. Int. J. Obes. (Lond.)29, 565–570 (2005).
   PubMed Web of Science ®Google Scholar
• Jaquet D, Tregouet DA, Godefroy T et al. Combined effects of genetic and environmental factors on insulin resistance associated with reduced fetal growth. Diabetes51, 3473–3478 (2002).
   PubMed Web of Science ®Google Scholar
• Eriksson JG, Lindi V, Uusitupa M et al. The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-γ2 gene on insulin sensitivity and insulin metabolism interact with size at birth. Diabetes51, 2321–2324 (2002).
   PubMed Web of Science ®Google Scholar
• Neel JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am. J. Hum. Genet.14, 353–362 (1962).
   PubMed Web of Science ®Google Scholar
• Hattersley AT, Tooke JE. The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet353, 1789–1792 (1999).
   PubMed Web of Science ®Google Scholar
• Hattersley AT, Beards F, Ballantyne E, Appleton M, Harvey R, Ellard S. Mutations in the glucokinase gene of the fetus result in reduced birth weight. Nature Genet.19, 268–270 (1998).
   PubMed Web of Science ®Google Scholar
• Dunger DB, Ong KK, Huxtable SJ et al. Association of the INS VNTR with size at birth. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Nature Genet.19, 98–100 (1998).
   PubMed Web of Science ®Google Scholar
• Bennett ST, Todd JA. Human type 1 diabetes and the insulin gene: principles of mapping polygenes. Ann Rev. Genet.30, 343–370 (1996).
   PubMed Web of Science ®Google Scholar
• Lindsay RS, Hanson RL, Wiedrich C, Knowler WC, Bennett PH, Baier LJ. The insulin gene variable number tandem repeat class I/III polymorphism is in linkage disequilibrium with birth weight but not Type 2 diabetes in the Pima population. Diabetes52, 187–193 (2003).
   PubMed Web of Science ®Google Scholar
• Bennett AJ, Sovio U, Ruokonen A et al. Variation at the insulin gene VNTR (variable number tandem repeat) polymorphism and early growth: studies in a large Finnish birth cohort. Diabetes53, 2126–2131 (2004).
   PubMed Web of Science ®Google Scholar
• Bennett A, Sovio U, Ruokonen A et al. No association between insulin gene variation and adult metabolic phenotypes in a large Finnish birth cohort. Diabetologia48, 886–891 (2005).
   PubMed Web of Science ®Google Scholar
• Lucas A. Programming by early nutrition in man. Ciba. Found. Symp.156, 38–50 (1991).
   PubMedGoogle Scholar
• Poulsen P, Vaag A, Kyvik K, Beck-Nielsen H. Genetic versus environmental aetiology of the metabolic syndrome among male and female twins. Diabetologia44, 537–543 (2001).
   PubMed Web of Science ®Google Scholar
• Poulsen P, Levin K, Petersen I, Christensen K, Beck-Nielsen H, Vaag A. Heritability of insulin secretion, peripheral and hepatic insulin action, and intracellular glucose partitioning in young and old Danish twins. Diabetes54, 275–283 (2005).
   PubMed Web of Science ®Google Scholar
• Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science305, 1733–1736 (2004).
   PubMed Web of Science ®Google Scholar