Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-20T00:21:56.314Z Has data issue: false hasContentIssue false

Prematurity and programming: contribution of neonatal Intensive Care Unit interventions

Published online by Cambridge University Press:  11 October 2012

S. C. Kalhan*
Affiliation:
Department of Molecular Medicine, Cleveland Clinic, Lerner College of Medicine of Case Western Reserve University, Cleveland, OH, USA Department of Pathobiology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA
D. Wilson-Costello
Affiliation:
Department of Neonatology, Rainbow Babies and Children's Hospital, Case Western Reserve University, Cleveland, OH, USA
*
*Address for correspondence: Dr S. C. Kalhan, Department of Pathobiology, Lerner Research Institute, Cleveland Clinic, NE-40, 9500 Euclid Avenue, Cleveland, OH 44195, USA. Email [email protected]

Abstract

Contemporary clinical practice for the care of the prematurely born babies has markedly improved their rates of survival so that most of these babies are expected to grow up to live a healthy functional life. Since the clinical follow-up is of short duration (years), only limited data are available to relate non-communicable diseases in adult life to events and interventions in the neonatal period. The major events that could have a programming effect include: (1) intrauterine growth restriction; (2) interruption of pregnancy with change in redox and reactive oxygen species (ROS) injury; (3) nutritional and pharmacological protocols for clinical care; and (4) nutritional care in the first 2 years resulting in accelerated weight gain. The available data are discussed in the context of perturbations in one carbon (methyl transfer) metabolism and its possible programming effects. Although direct evidence for genomic methylation is not available, clinical and experimental data on impact of redox and ROS, of low protein intake, excess methionine load and vitamin A, on methyl transfers are reviewed. The consequences of antenatal and postnatal administration of glucocorticoids are presented. Analysis of the correlates of insulin sensitivity at older age, suggests that premature birth is the major contributor, and is compounded by gain in weight during infancy. We speculate that premature interruption of pregnancy and neonatal interventions by affecting one carbon metabolism may cause programming effects on the immature baby. These can be additive to the effects of intrauterine environment (growth restriction) and are compounded by accelerated growth in early infancy.

Type
Review
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Eichenwald, EC, Stark, AR. Management and outcomes of very low birth weight. N Engl J Med. 2008; 358, 17001711.CrossRefGoogle ScholarPubMed
2.Fanaroff, AA, Hack, M, Walsh, MC. The NICHD neonatal research network: changes in practice and outcomes during the first 15 years. Semin Perinatol. 2003; 27, 281287.CrossRefGoogle Scholar
3.Hack, M. Adult outcomes of preterm children. J Dev Behav Pediatr. 2009; 30, 460470.Google Scholar
4.Wilson-Costello, D, Friedman, H, Minich, N, Fanaroff, AA, Hack, M. Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics. 2005; 115, 9971003.Google Scholar
5.Doyle, LW, Anderson, PJ. Adult outcome of extremely preterm infants. Pediatrics. 2010; 126, 342351.Google Scholar
6.Eriksson, J, Forsen, T, Tuomilehto, J, Osmond, C, Barker, D. Fetal and childhood growth and hypertension in adult life. Hypertension. 2000; 36, 790794.CrossRefGoogle ScholarPubMed
7.Hovi, P, Andersson, S, Raikkonen, K, et al. Ambulatory blood pressure in young adults with very low birth weight. J Pediatr. 2010; 156, 54,59.e1.Google Scholar
8.Whincup, PH, Kaye, SJ, Owen, CG, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300, 28862897.Google Scholar
9.Warner, MJ, Ozanne, SE. Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010; 427, 333347.Google Scholar
10.Simmons, R. Developmental origins of adult metabolic disease: concepts and controversies. Trends Endocrinol Metab. 2005; 16, 390394.Google Scholar
11.Ehrenkranz, RA, Younes, N, Lemons, JA, et al. Longitudinal growth of hospitalized very low birth weight infants. Pediatrics. 1999; 104, 280289.Google Scholar
12.Philippidis, H, Ballard, FJ. The development of gluconeogenesis in rat liver: experiments in vivo. Biochem J. 1969; 113, 651657.CrossRefGoogle ScholarPubMed
13.Filippi, L, Messeri, A, Dani, C, et al. Redox status in very-low birth-weight newborns. Biol Neonate. 2004; 85, 210216.Google Scholar
14.Avery, SV. Molecular targets of oxidative stress. Biochem J. 2011; 434, 201210.Google Scholar
15.Kalhan, SC, Marczewski, SE. Methionine, homocysteine, one carbon metabolism and fetal growth. Rev Endocr Metab Disord. 2012; 13, 109119.CrossRefGoogle ScholarPubMed
16.Prudova, A, Bauman, Z, Braun, A, et al. S-adenosylmethionine stabilizes cystathionine β synthase and modulates redox capacity. Proc Nat Acad Sci. 2006; 103, 64896494.Google Scholar
17.Vivitsky, V, Mosharov, E, Tritt, M, Ataullakhanov, F, Banerjee, R. Redox regulation of homocysteine-dependent glutathione synthesis. Redox Rep. 2003; 8, 5763.Google Scholar
18.Kabil, O, Banerjee, R. Redox biochemistry of hydrogen sulfide. J Biol Chem. 2010; 285, 2190321907.Google Scholar
19.Kalhan, S, Parimi, P. Gluconeogenesis in the fetus and neonate. Semin Perinatol. 2000; 24, 94106.CrossRefGoogle ScholarPubMed
20.Kalhan, SC, Bier, DM. Protein and amino acid metabolism in the human newborn. Annu Rev Nutr. 2008; 28, 389410.CrossRefGoogle ScholarPubMed
21.Srinivasan, M, Laychock, SG, Hill, DJ, Patel, MS. Neonatal nutrition: metabolic programming of pancreatic islets and obesity. Exp Biol Med (Maywood). 2003; 228, 1523.Google Scholar
22.Symonds, ME, Sebert, SP, Hyatt, MA, Budge, H. Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol. 2009; 5, 604610.CrossRefGoogle ScholarPubMed
23.Hay, WW, Thureen, P. Protein for preterm infants: how much is needed? How much is enough? How much is too much? Pediatr Neonatol. 2010; 51, 198207.Google Scholar
24.Olsen, IE, Richardson, DK, Schmid, CH, Ausman, LM, Dwyer, JT. Intersite differences in weight growth velocity of extremely premature infants. Pediatrics. 2002; 110, 11251132.CrossRefGoogle ScholarPubMed
25.Cooke, RJ, Ainsworth, SB, Fenton, AC. Postnatal growth retardation: a universal problem in preterm infants. Arch Dis Child Fetal Neonatal Ed. 2004; 89, F428F430.CrossRefGoogle ScholarPubMed
26.Hay, WW Jr, Thureen, PJ. Early postnatal administration of intravenous amino acids to preterm, extremely low birth weight infants. J Pediatr. 2006; 148, 291294.Google Scholar
27.Poindexter, BB, Langer, JC, Dusick, AM, Ehrenkranz, RA, National Institute of Child Health and Human Development Neonatal Research Network. Early provision of parenteral amino acids in extremely low birth weight infants: relation to growth and neurodevelopmental outcome. J Pediatr. 2006; 148, 300305.Google Scholar
28.te Braake, FW, van den Akker, CH, Wattimena, DJ, Huijmans, JG, van Goudoever, JB. Amino acid administration to premature infants directly after birth. J Pediatr. 2005; 147, 457461.Google Scholar
29.Jadhav, P, Parimi, PS, Kalhan, SC. Parenteral amino acid and metabolic acidosis in premature infants. J Parenter Enteral Nutr. 2007; 31, 278283.Google Scholar
30.Ibrahim, HM, Jeroudi, MA, Baier, RJ, Dhanireddy, R, Krouskop, RW. Aggressive early total parental nutrition in low-birth-weight infants. J Perinatol. 2004; 24, 482486.Google Scholar
31.Augustyniak, RA, Singh, K, Zeldes, D, Singh, M, Rossi, NF. Maternal protein restriction leads to hyperresponsiveness to stress and salt-sensitive hypertension in male offspring. Am J Physiol Regul Integr Comp Physiol. 2010; 298, R1375R1382.CrossRefGoogle ScholarPubMed
32.Kalhan, SC, Uppal, SO, Moorman, JL, et al. Metabolic and genomic response to dietary isocaloric protein restriction in the rat. J Biol Chem. 2011; 286, 52665277.Google Scholar
33.Ingenbleek, Y, Hardillier, E, Jung, L. Subclinical protein malnutrition is a determinant of hyperhomocysteinemia. Nutrition. 2002; 18, 4046.Google Scholar
34.Embleton, NE, Pang, N, Cooke, RJ. Postnatal malnutrition and growth retardation: an inevitable consequence of current recommendations in preterm infants? Pediatrics. 2001; 107, 270273.Google Scholar
35.Stephens, BE, Walden, RV, Gargus, RA, et al. First-week protein and energy intakes are associated with 18-month developmental outcomes in extremely low birth weight infants. Pediatrics. 2009; 123, 13371343.Google Scholar
36.Heird, WC, Hay, W, Helms, RA, et al. Pediatric parenteral amino acid mixture in low birth weight infants. Pediatrics. 1988; 81, 4150.Google Scholar
37.Blanco, CL, Gong, AK, Green, BK, et al. Early changes in plasma amino acid concentrations during aggressive nutrition therapy in extremely low birth weight infants. J Pediatr. 2011; 158, 543548.Google Scholar
38.Battista, MA, Price, PT, Kalhan, SC. Effect of parenteral amino acids on leucine and urea kinetics in preterm infants. J Pediatr. 1996; 128, 130140.Google Scholar
39.Thomas, B, Gruca, LL, Bennett, C, et al. Metabolism of methionine in the newborn infant: response to the parenteral and enteral administration of nutrients. Pediatr Res. 2008; 64, 381386. PMCID: 2651408.Google Scholar
40.Hollingsworth, JW, Maruoka, S, Boon, K, et al. In utero supplementation with methyl donors enhances allergic airway disease in mice. Journal of Clin Invest. 2008; 118, 34623469.Google ScholarPubMed
41.Haberg, SE, London, SJ, Stigum, H, Nafstad, P, Nystad, W. Folic acid supplements in pregnancy and early childhood respiratory health. Arch Dis Child. 2009; 94, 180184.Google Scholar
42.Whitrow, MJ, Moore, VM, Rumbold, AR, Davies, MJ. Effect of supplemental folic acid in pregnancy on childhood asthma: a prospective birth cohort study. Am J Epidemiol. 2009; 170, 14861493.Google Scholar
43.Wilson, DC, Cairns, P, Halliday, HL, et al. Randomised controlled trial of an aggressive nutritional regimen in sick very low birthweight infants. Arch Dis Child Fetal Neonatal Ed. 1997; 77, F4F11.CrossRefGoogle ScholarPubMed
44.Dinerstein, A, Nieto, RM, Solana, CL, et al. Early and aggressive nutritional strategy (parenteral and enteral) decreases postnatal growth failure in very low birth weight infants. J Perinatol. 2006; 26, 436442.Google Scholar
45.Cooke, RJ, Griffin, I. Altered body composition in preterm infants at hospital discharge. Acta Paediatr. 2009; 98, 12691273.Google Scholar
46.Yajnik, CS, Fall, CH, Coyaji, KJ, et al. Neonatal anthropometry: the thin–fat Indian baby. The Pune Maternal Nutrition Study. Int J Obes Relat Metab Disord. 2003; 27, 173180.Google Scholar
47.Ehrenkranz, RA, Dusick, AM, Vohr, BR, et al. Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics. 2006; 117, 12531261.Google Scholar
48.Peeples, JM, Carlson, SE, Werkman, SH, Cooke, RJ. Vitamin A status of preterm infants during infancy. Am J Clin Nutr. 1991; 53, 14551459.Google Scholar
49.Greene, HL, Phillips, BL, Franck, L, et al. Persistently low blood retinol levels during and after parenteral feeding of very low birth weight infants: examination of losses into intravenous administration sets and a method of prevention by addition to a lipid emulsion. Pediatrics. 1987; 79, 894900.CrossRefGoogle Scholar
50.Shenai, JP, Chytil, F, Stahlman, MT. Liver vitamin A reserves of very low birth weight neonates. Pediatr Res. 1985; 19, 892893.Google Scholar
51.Shenai, JP, Chytil, F, Stahlman, MT. Vitamin A status of neonates with bronchopulmonary dysplasia. Pediatr Res. 1958; 19, 185188.Google Scholar
52.Spears, K, Cheney, C, Zerzan, J. Low plasma retinol concentrations increase the risk of developing bronchopulmonary dysplasia and long-term respiratory disability in very low birth weight infants. Am J Clin Nutr. 2004; 80, 15891594.Google Scholar
53.Shenai, JP, Kennedy, KA, Chytil, F, Stahlman, MT. Clinical trial of vitamin A supplementation in infants susceptible to bronchopulmonary dysplasia. J Pediatr. 1987; 111, 269277.Google Scholar
54.Pearson, E, Bose, C, Snidow, T, et al. Trial of vitamin A supplementation in very low birth weight infants at risk for bronchopulmonary dysplasia. J Pediatr. 1992; 121, 420427.Google Scholar
55.Wardle, SP, Hughes, A, Chen, S, Shaw, NJ. Randomised controlled trial of oral vitamin A supplementation in preterm infants to prevent chronic lung disease. Arch Dis Child Fetal Neonatal Ed. 2001; 84, F9F13.Google Scholar
56.Tyson, JE, Wright, LL, Oh, W, et al. Vitamin A supplementation for extremely low birth weight infants. N Engl J Med. 1999; 340, 19621968.CrossRefGoogle ScholarPubMed
57.Darlow, BA, Graham, PJ. Vitamin A supplementation to prevent mortality and short and long term morbidity in very low birth weight infants. Cochrane Database Syst Rev. 2011; 10, Art. No.: CD000501. doi:10.1002/14651858.CD000501.pub3.Google Scholar
58.Barros, FC, Bhutta, ZA, Batra, M, et al. Global report on preterm birth and stillbirth (3 of 7): evidence for effectiveness of interventions. BMC Pregnancy Childbirth. 2010; 10(Suppl. 1), S3.CrossRefGoogle ScholarPubMed
59.Ambalavanan, N, Tyson, JE, Kennedy, KA, et al. Vitamin A supplementation for extremely low birth weight infants: outcome at 18 to 22 months. Pediatrics. 2005; 115, e249e254.Google Scholar
60.Rowling, MJ, McMullen, MH, Schalinske, KL. Vitamin A and its derivatives induce hepatic glycine N-methyltransferase and hypomethylation of DNA in rats. J Nutr. 2002; 132, 365369.CrossRefGoogle ScholarPubMed
61.Rowling, MJ, Schalinske, KL. Retinoid compounds activate and induce hepatic glycine N-methyltransferase in rats. J Nutr. 2001; 131, 19141917.CrossRefGoogle ScholarPubMed
62.McMullen, MH, Rowling, MJ, Ozias, MK, Schalinske, KL. Activation and induction of glycine N-methyltransferase by retinoids are tissue and gender specific. Arch Biochem Biophys. 2002; 401, 7380.CrossRefGoogle ScholarPubMed
63.Rowling, MJ, Schalinske, KL. Retinoic acid and glucocorticoid treatment induce hepatic glycine N-methyltransferase and lower plasma homocysteine concentrations in rats and rat hepatoma cells. J Nutr. 2003; 133, 33923398.Google Scholar
64.Kihara, T, Matsuo, T, Sakamoto, M, Yasuda, Y, Tanimura, T. Effects of the neonatal vitamin A exposure on behaviors of adult rats. J Toxicol Sci. 1995; 20, 93101.Google Scholar
65.Csaba, G, Kovacs, P, Pallinger, E. Transgenerational effect of neonatal vitamin A or D treatment (hormonal imprinting) on the hormone content of rat immune cells. Horm Metab Res. 2007; 39, 197201.Google Scholar
66.Coluccia, A, Borracci, P, Belfiore, D, Renna, G, Carratu, MR. Late embryonic exposure to all trans retinoic acid induces a pattern of motor deficits unrelated to the developmental stage. Neurotoxicology. 2009; 30, 11201126.Google Scholar
67.Harris, A, Seckl, J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011; 59, 279289.CrossRefGoogle ScholarPubMed
68.Drake, AJ, Tang, JI, Nyirenda, MJ. Mechanisms underlying the role of glucocorticoids in the early life programming of adult disease. Clin Sci (Lond). 2007; 113, 219232.Google Scholar
69.Doyle, LW, Ford, GW, Davis, NM, Callanan, C. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin Sci (Lond). 2000; 98, 137142.CrossRefGoogle ScholarPubMed
70.Dessens, AB, Haas, HS, Koppe, JG. Twenty-year follow up of antenatal corticosteroid treatment. Pediatrics. 2000; 105, E77.Google Scholar
71.Finken, MJ, Keijzer-Veen, MG, Dekker, FW, et al. Antenatal glucocorticoid treatment is not associated with long term metabolic risks in individuals born before 32 weeks of gestation. Arch Dis Child Fetal Neonatal Ed. 2008; 93, F442F447.Google Scholar
72.Dalziel, SR, Walker, NK, Parag, V, et al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30 year follow up of a randomised controlled trial. Lancet. 2005; 365, 18561862.CrossRefGoogle ScholarPubMed
73.Dalziel, SR, Rea, HH, Walker, NK, et al. Long term effects of antenatal betamethasone on lung function: 30 year follow up of a randomised controlled trial. Thorax. 2006; 61, 678683.Google Scholar
74.Dalziel, SR, Lim, VK, Lambert, A, et al. Antenatal exposure to betamethasone: psychological functioning and health related quality of life 31 years after inclusion in randomised controlled trial. BMJ. 2005; 331, 665.CrossRefGoogle ScholarPubMed
75.Wapner, RJ, Sorokin, Y, Mele, L, et al. Long term outcomes after repeat doses of antenatal corticosteroids. N Engl J Med. 2007; 357, 11901198.CrossRefGoogle ScholarPubMed
76.Peltoniemi, OM, Kari, MA, Lano, A, et al. Two year follow up of a randomised trial with repeated antenatal betamethasone. Arch Dis Child Fetal Neonatal Ed. 2009; 94, F402F406.CrossRefGoogle ScholarPubMed
77.Yates, H, Newell, S. Postnatal intravenous steroids and long term neurological outcome: recommendations from meta analyses. Arch Dis Child Fetal Neonatal Ed. 2011; 97, F299F303.Google Scholar
78.Wilson-Costello, D, Walsh, MC, Langer, JC, et al. Impact of postnatal corticosteroid use on neurodevelopment at 18 to 22 months’ adjusted age: effects of dose, timing, and risk of bronchopulmonary dysplasia in extremely low birth weight infants. Pediatrics. 2009; 123, e430e437.Google Scholar
79.Stark, AR, Carlo, WA, Tyson, JE, et al. Adverse effects of early dexamethasone in extremely low birth weight infants. N Engl J Med. 2001; 344, 95101.Google Scholar
80.le Cras, TD, Markhan, NE, Morris, KG, et al. Neonatal dexamethasone treatment increases the risk for pulmonary hypertension in adult rats. Am J Physiol Lung Cell Mol Physiol. 2000; 278, L822L829.Google Scholar
81.Flier, NN, Barrington, KJ. Nitric oxide for respiratory failure in infants born at or near term. Cochrane Database Syst Rev. 2006, CD000399.Google Scholar
82.Subhedar, N, Dewhurst, C. Is nitric oxide effective in preterm infants? Arch Dis Child Fetal and Neonatal Ed. 2007; 92, 337341.Google Scholar
83.Donohue, PKGilmore, MM, Cristofalo, E, et al. Inhaled nitric oxide in preterm infants: a systematic review. Pediatrics. 2011; 127, e414e422.CrossRefGoogle ScholarPubMed
84.Cole, FS, Alleyene, C, Barks, JD, et al. NIH consensus development conference statement: inhaled nitric oxide therapy for premature infants. Pediatrics. 2011; 127, 363369.Google Scholar
85.Weinberger, B, Laskin, DL, Heck, DE, Laskin, JD. The toxicology of inhaled nitric oxide. Toxicol Sci. 2001; 59, 516.Google Scholar
86.Illi, B, Colussi, C, Grasselli, A, et al. NO sparks off chromatin: tales of a multifaceted epigenetic regulator. Pharmacol Ther. 2009; 123, 344352.Google Scholar
87.Nott, A, Riccio, A. Nitric oxide-mediated epigenetic mechanisms in developing neurons. Cell Cycle. 2009; 8, 725730.Google Scholar
88.Keanney, JF Jr, Simon, DI, Stamler, JS, et al. NO forms an adduct with serum albumin that has endothelium-derived relaxing factor-like properties. J Clin Invest. 1993; 91, 15821589.Google Scholar
89.Lin, YS, Nguyen, C, Mendoza, JL, et al. Preclinical pharmacokinetics, interspecies scaling and tissue distribution of a humanized monoclonal antibody against vascular endothelial growth factor. J Pharmacol Exp Ther. 1999; 288, 371378.Google Scholar
90.Ferrara, N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004; 25, 581611.Google Scholar
91.Mintz-Hittner, HA, Kennedy, KA, Chuang, AZ. Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. N Engl J Med. 2011; 364, 603615.Google Scholar
92.Wang, Y, Fei, D, Venderlaan, M, Song, A. Biological activity of bevacizumab, a humanized anti-VEGF antibody in vitro. Angiogenesis. 2004; 7, 335345.Google Scholar
93.Gerber, HP, Hillan, KJ, Ryan, AM, et al. VEGF is required for growth and survival in neonatal mice. Development. 1999; 126, 11491159.Google Scholar
94.Gerber, HP, Vu, TH, Ryan, AM, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999; 5, 623628.Google Scholar
95.Wu, WC, Lai, CC, Chen, KJ, et al. Long-term tolerability and serum concentration of bevacizumab (avastin) when injected in newborn rabbit eyes. Invest Ophthalmol Vis Sci. 2010; 51, 37013708.Google Scholar
96.Maffini, MV, Rubin, BS, Sonnenschein, C, Sotoi, AM. Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol Cell Endocr. 2006; 254–255, 179186.Google Scholar
97.Calafat, AM, Weuve, J, Ye, X, et al. Exposure to bisphenol A and other phenols in Neonatal Intensive Care Unit premature infants. Environ Health Perspect. 2009; 117, 639644.Google Scholar
98.Dolibnoy, DC, Huang, D, Jirtle, RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Nat Acad Sci. 2007; 104, 1305613061.Google Scholar
99.Jasarevic, E, Sieli, PT, Twellman, EE, et al. Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc Nat Acad Sci. 2011; 108, 1171511720.Google Scholar
100.Hack, M, Merkatz, IR, McGrath, SK, Jones, PK, Fanaroff, AA. Catch-up growth in very low birth weight infants. Am J Dis Child. 1984; 138, 370375.Google Scholar
101.Brandt, I, Sticker, EJ, Gausche, R, Lentze, MJ. Catch-up growth of supine length/height of very low birth weight, small for gestational age preterm infants to adulthood. J Pediatr. 2005; 147, 662668.Google Scholar
102.Itabashi, K, Mishina, J, Tada, H, et al. Longitudinal follow up of height up to five years of age in infants born preterm small for gestational age; comparison to full term small for gestational age infants. Early Hum Dev. 2007; 83, 327333.Google Scholar
103.Uthaya, S, Thomas, EL, Hamilton, G, et al. Altered adiposity after extremely preterm birth. Pediatr Res. 2005; 57, 211215.Google Scholar
104.Cooke, RJ, Griffin, IJ, McCormick, K. Adiposity is not altered in preterm infants fed with a nutrient enriched formula after hospital discharge. Pediatr Res. 2010; 67, 660664.Google Scholar
105.Yeung, MY. Postnatal growth, neurodevelopment and altered adiposity after preterm birth – from a clinical nutrition perspective. Acta Paediatr. 2006; 95, 909917.Google Scholar
106.Ong, KK, Loos, RJ. Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr. 2006; 95, 904908.Google Scholar
107.Monteiro, PO, Victora, CG. Rapid growth in infancy and childhood and obesity in later life – a systematic review. Obes Rev. 2005; 6, 143154.Google Scholar
108.Wehkalampi, K, Hovi, P, Dunkel, L, et al. Advanced pubertal growth spurt in subjects born preterm: the Helsinki study of very low birth weight adults. J Clin Endocrinol Metab. 2011; 96, 525533.Google Scholar
109.Bazaes, RA, Alegría, A, Pittaluga, E, et al. Determinants of insulin sensitivity and secretion in very low birth weight children. J Clin Endocrinol Metab. 2004; 89, 12671272.Google Scholar
110.Stettler, N, Iotova, V. Early growth patterns and long term obesity risk. Curr Opin Clin Nutr Metab Care. 2010; 13, 294299.Google Scholar
111.Hofman, PL, Regan, F, Jackson, WE, et al. Premature birth and later insulin resistance. N Engl J Med. 2004; 351, 21792186. Erratum in: N Engl J Med. 2004; 351, 2888.Google Scholar
112.Fewtrell, MS, Doherty, C, Cole, TJ, et al. Effects of size at birth, gestational age and early growth in preterm infants on glucose and insulin concentrations at 9–12 years. Diabetologia. 2000; 43, 714717.Google Scholar
113.Hovi, P, Andersson, S, Eriksson, JG, et al. Glucose regulation in young adults with very low birth weight. N Engl J Med. 2007; 356, 20532063. PubMed PMID: 17507704.Google Scholar
114.Finken, MJ, Keijzer-Veen, MG, Dekker, FW, et al, Dutch POPS-19 Collaborative Study Group. Preterm birth and later insulin resistance: effects of birth weight and postnatal growth in a population based longitudinal study from birth into adult life. Diabetologia. 2006; 49, 478485.Google Scholar
115.Rotteveel, J, van Weissenbruch, MM, Twisk, JW, Delemarre-Van de Waal, HA. Infant and childhood growth patterns, insulin sensitivity, and blood pressure in prematurely born young adults. Pediatrics. 2008; 122, 313321.Google Scholar
116.Pilgaard, K, Færch, K, Carstensen, B, et al. Low birthweight and premature birth are both associated with type 2 diabetes in a random sample of middle-aged Danes. Diabetologia. 2010; 53, 25262530.Google Scholar
117.Kaijser, M, Bonamy, AK, Akre, O, et al. Perinatal risk factors for diabetes in later life. Diabetes. 2009; 58, 523526.Google Scholar