Skip to main content Accessibility help

Metabolic imprinting, programming and epigenetics – a review of present priorities and future opportunities

  • Bryan Hanley (a1), Jean Dijane (a2), Mary Fewtrell (a3), Alain Grynberg (a2), Sandra Hummel (a4), Claudine Junien (a5), Berthold Koletzko (a6), Sarah Lewis (a7), Harald Renz (a8), Michael Symonds (a9), Marjan Gros (a10), Lucien Harthoorn (a11), Katherine Mace (a12), Fiona Samuels (a13) and Eline M. van Der Beek (a14)...


Metabolic programming and metabolic imprinting describe early life events, which impact upon on later physiological outcomes. Despite the increasing numbers of papers and studies, the distinction between metabolic programming and metabolic imprinting remains confusing. The former can be defined as a dynamic process whose effects are dependent upon a critical window(s) while the latter can be more strictly associated with imprinting at the genomic level. The clinical end points associated with these phenomena can sometimes be mechanistically explicable in terms of gene expression mediated by epigenetics. The predictivity of outcomes depends on determining if there is causality or association in the context of both early dietary exposure and future health parameters. The use of biomarkers is a key aspect of determining the predictability of later outcome, and the strengths of particular types of biomarkers need to be determined. It has become clear that several important health endpoints are impacted upon by metabolic programming/imprinting. These include the link between perinatal nutrition, nutritional epigenetics and programming at an early developmental stage and its link to a range of future health risks such as CVD and diabetes. In some cases, the evidence base remains patchy and associative, while in others, a more direct causality between early nutrition and later health is clear. In addition, it is also essential to acknowledge the communication to consumers, industry, health care providers, policy-making bodies as well as to the scientific community. In this way, both programming and, eventually, reprogramming can become effective tools to improve health through dietary intervention at specific developmental points.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Metabolic imprinting, programming and epigenetics – a review of present priorities and future opportunities
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Metabolic imprinting, programming and epigenetics – a review of present priorities and future opportunities
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Metabolic imprinting, programming and epigenetics – a review of present priorities and future opportunities
      Available formats


Corresponding author

*Correspondence: ILSI Europe a.i.s.b.l. - Avenue E. Mounier 83, Box 6 - 1200 Brussels - Belgium, fax: +32 2 762 00 44, email:


Hide All
1Levin, BE (2006) Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond B Biol Sci 361, 11071121.
2Barker, DJ (1992) The effect of nutrition of the fetus and neonate on cardiovascular disease in adult life. Proc Nutr Soc 51, 135144.
3Barker, DJ (1995) The fetal and infant origins of disease. Eur J Clin Invest 25, 457463.
4Lucas, A (1991) Programming by early nutrition in man. Ciba Found Symp 156, 3850.
5Ness, AR (2004) The Avon Longitudinal Study of Parents and Children (ALSPAC) – a resource for the study of the environmental determinants of childhood obesity. Eur J Endocrinol 151, Suppl. 3, U141U149.
6Eriksson, JG, Forsén, T, Tuomilehto, J, et al. (2003) Early adiposity rebound in childhood and risk of Type 2 diabetes in adult life. Diabetologia 46, 190194.
7Campbell, DM, Hall, MH, Barker, DJ, et al. (1996) Diet in pregnancy and the offspring's blood pressure 40 years later. Br J Obstet Gynaecol 103, 273280.
8Godfrey, KM, Forrester, T, Barker, DJ, et al. (1994) Maternal nutritional status in pregnancy and blood pressure in childhood. Br J Obstet Gynaecol 101, 398403.
9Javaid, MK, Crozier, SR, Harvey, NC, et al. (2006) Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: a longitudinal study. Lancet 367, 3643.
10Waterland, RA & Garza, C (1999) Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr 69, 179197.
11Lucas, A (2000) Programming not metabolic imprinting. Am J Clin Nutr 71, 602.
12Branca, F, Hanley, AB, Pool-Zobel, B, et al. (2001) Biomarkers in disease and health. Br J Nutr 86, Suppl. 1, S55S92.
13Kim, Y-I (2005) Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr 135, 27032709.
14Barker, DJ, Bull, AR, Osmond, C, et al. (1990) Fetal and placental size and risk of hypertension in adult life. BMJ 301, 259262.
15Barker, DJ, Osmond, C, Forsen, TJ, et al. (2005) Trajectories of growth among children who have coronary events as adults. N Engl J Med 353, 18021809.
16Singhal, A (2005) Endothelial dysfunction: role in obesity-related disorders and the early origins of CVD. Proc Nutr Soc 64, 1522.
17Keith, SW, Redden, DT, Katzmarzyk, PT, et al. (2006) Putative contributors to the secular increase in obesity: exploring the roads less traveled. Int J Obes (Lond) 30, 15851594.
18Williams, P, Kurlak, LO, Perkins, A, et al. (2007) Impaired renal function and hypertension accompany juvenile obesity: effect of prenatal diet. Kidney Int 72, 279289.
19Symonds, ME, Stephenson, T, Gardner, DS, et al. (2007) Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reprod Fertil Dev 19, 5363.
20Reynolds, RM, Godfrey, KM, Barker, M, et al. (2007) Stress responsiveness in adult life: influence of mother's diet in late pregnancy. J Clin Endocrinol Metab 92, 22082210.
21Pepper, G & Roberts, S (2006) Rates of nausea and vomiting in pregnancy and dietary characteristics across populations. Proc Biol Sci 273, 26752679.
22Gardner, DS, Tingey, K, van Bon, BWM, et al. (2005) Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. Am J Physiol 289, R947R954.
23Symonds, ME (2007) Integration of physiological and molecular mechanisms of the developmental origins of adult disease: new concepts and insights. Proc Nutr Soc 66, 442450.
24Davey Smith, G, Steer, C, Leary, S, et al. (2007) Is there an intra-uterine influence on obesity? Evidence from parent–child associations in ALSPAC. Arch Dis Child 92, 876880.
25Toschke, AM, Martin, RM, von Kries, R, et al. (2007) Infant feeding method and obesity: body mass index and dual-energy X-ray absorptiometry measurements at 9–10 y of age from the Avon Longitudinal Study of Parents and Children (ALSPAC). Am J Clin Nutr 85, 15781585.
26Sievers, E, Oldigs, HD, Santer, R, et al. (2002) Feeding patterns in breast-fed and formula-fed infants. Ann Nutr Metab 46, 243248.
27Lee, K (2000) Crying and behavior pattern in breast- and formula-fed infants. Early Hum Dev 58, 133140.
28Heird, WC (2007) Progress in promoting breast-feeding, combating malnutrition, and composition and use of infant formula, 1981–2006. J Nutr 137, 499S502S.
29Bogen, DL, Hanusa, BH & Whitaker, RC (2004) The effect of breast-feeding with and without formula use on the risk of obesity at 4 years of age. Obes Res 12, 15271535.
30Symonds, ME, Stephenson, T, Gardner, DS, et al. (2009) Tissue specific adaptations to nutrient supply: more than just epigenetics? Adv Exp Med Biol 646, 113118.
31McMillen, IC & Robinson, JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Phys Rev 85, 571633.
32Prentice, AM & Prentice, A (1995) Evolutionary and environmental influences on lactation. Proc Nutr Soc 54, 391400.
33Taylor, PD, McConnell, J, Khan, IY, et al. (2005) Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol 288, R134R139.
34Widdowson, EM (1950) Chemical composition of newly born animals. Nature 116, 626628.
35Symonds, ME & Gardner, DS (2006) Experimental evidence for early nutritional programming of adult health in animals. Curr Opin Nutr Metab Care 9, 278283.
36Kwong, WY, Wild, AE, Roberts, P, et al. (2000) Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127, 41954202.
37D'Angelo, G, Elmarakby, AA, Pollock, DM, et al. (2005) Fructose feeding increases insulin resistance but not blood pressure in Sprague–Dawley rats. Hypertension 46, 806811.
38Bunag, RD (1973) Validation in awake rats of a tail-cuff method for measuring systolic pressure. J Appl Physiol 34, 279282.
39Fernandez-Twinn, DS, Ekizoglou, S, Wayman, A, et al. (2006) Maternal low-protein diet programs cardiac beta-adrenergic response and signaling in 3-mo-old male offspring. Am J Physiol 291, R429R436.
40Hoppe, CC, Evans, RG, Moritz, KM, et al. (2007) Combined prenatal and postnatal protein restriction influences adult kidney structure, function, and arterial pressure. Am J Physiol 292, R462R469.
41Brennan, KA, Olson, DM & Symonds, ME (2006) Maternal nutrient restriction alters renal development and blood pressure regulation of the offspring. Proc Nutr Soc 65, 116124.
42Dandrea, J, Wilson, V, Gopalakrishnan, G, et al. (2001) Maternal nutritional manipulation of placental growth and glucose transporter-1 abundance in sheep. Reproduction 122, 793800.
43Edwards, LJ, Symonds, ME, Warnes, K, et al. (2001) Responses of the fetal pituitary–adrenal axis to acute and chronic hypoglycaemia during late gestation in the sheep. Endocrinology 142, 17781785.
44Symonds, ME, Budge, H, Mostyn, A, et al. (2007) Maternal diet through pregnancy – the key to future good health of the next generation? In Nutrition Research Advances, pp. 223240 [Watkins, SV, editor]. New York: Nova Science Publishers, Inc.
45Gardner, DS, Pearce, S, Dandrea, J, et al. (2004) Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 43, 17.
46Valentine, CJ, Fernandez, S, Rogers, LK, et al. (2009) Early amino-acid administration improves preterm infant weight. J Perinatol 29, 428432.
47Groh-Wargo, S, Jacobs, J, Auestad, N, et al. (2005) Body composition in preterm infants who are fed long-chain polyunsaturated fatty acids: a prospective, randomized, controlled trial. Pediatr Res 57, (5 Pt 1), 712718.
48Innis, SM, Adamkin, DH, Hall, RT, et al. (2002) Docosahexaenoic acid and arachidonic acid enhance growth with no adverse effects in preterm infants fed formula. J Pediatr 140, 547554.
49Rankinen, T & Bouchard, C (2006) Genetics of food intake and eating behavior phenotypes in humans. Annu Rev Nutr 26, 413434.
50Rankinen, T, Zuberi, A, Chagnon, YC, et al. (2006) The human obesity gene map: the 2005 update. Obesity (Silver Spring) 14, 529644.
51Bouchard, C, Tremblay, A, Despres, JP, et al. (1990) The response to long-term overfeeding in identical twins. N Engl J Med 322, 14771482.
52Fraga, MF, Ballestar, E, Paz, MF, et al. (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102, 1060410609.
53Gallou-Kabani, C & Junien, C (2005) Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes 54, 18991906.
54Waddington, C (1942) Canalisation of development and inheritance of acquired characters. Nature 152, 563.
55Weaver, IC, Cervoni, N, Champagne, FA, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7, 847854.
56Champagne, FA, Weaver, IC, Diorio, J, et al. (2006) Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147, 29092915.
57Santoro, R (2005) The silence of the ribosomal RNA genes. Cell Mol Life Sci 62, 20672079.
58Oakes, CC, Smiraglia, DJ, Plass, C, et al. (2003) Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc Natl Acad Sci U S A 100, 17751780.
59Pham, TD, MacLennan, NK, Chiu, CT, et al. (2003) Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol 285, R962R970.
60MacLennan, NK, James, SJ, Melnyk, S, et al. (2004) Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol Genomics 18, 4350.
61Pogribny, IP, Ross, SA, Wise, C, et al. (2006) Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat Res 593, 8087.
62Polo, SE, Roche, D & Almouzni, G (2006) New histone incorporation marks sites of UV repair in human cells. Cell 127, 481493.
63Nakatani, Y, Ray-Gallet, D, Quivy, JP, et al. (2004) Two distinct nucleosome assembly pathways: dependent or independent of DNA synthesis promoted by histone H3.1 and H3.3 complexes. Cold Spring Harb Symp Quant Biol 69, 273280.
64Yokomori, N, Tawata, M & Onaya, T (1999) DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. Diabetes 48, 685690.
65Yokomori, N, Tawata, M & Onaya, T (2002) DNA demethylation modulates mouse leptin promoter activity during the differentiation of 3T3-L1 cells. Diabetologia 45, 140148.
66Staels, B (2006) When the clock stops ticking, metabolic syndrome explodes. Nat Med 12, 5455.
67Fontaine, C & Staels, B (2007) The orphan nuclear receptor Rev-erbalpha: a transcriptional link between circadian rhythmicity and cardiometabolic disease. Curr Opin Lipidol 18, 141146.
68Issa, JP (2002) Epigenetic variation and human disease. J Nutr 132, Suppl. 8, 2388S2392S.
69Whitelaw, NC & Whitelaw, E (2006) How lifetimes shape epigenotype within and across generations. Hum Mol Genet 15, R131R137.
70Gluckman, PD, Hanson, MA & Beedle, AS (2007) Non-genomic transgenerational inheritance of disease risk. Bioessays 29, 145154.
71Yang, X, Schadt, EE, Wang, S, et al. (2006) Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16, 9951004.
72Junien, C & Nathanielsz, P (2006) Report on the IASO Stock Conference: early and lifelong environmental epigenomic programming of metabolic syndrome, obesity and type II diabetes. Obes Rev 8, 487502.
73Bjornsson, HT, Danielle Fallin, M & Feinberg, AP (2004) An integrated epigenetic and genetic approach to common human disease. Trends Genet 20, 350358.
74Abdolmaleky, HM, Smith, CL, Faraone, SV, et al. (2004) Methylomics in psychiatry: modulation of gene–environment interactions may be through DNA methylation. Am J Med Genet B Neuropsychiatr Genet 127B, 5159.
75Petronis, A (2006) Epigenetics and twins: three variations on the theme. Trends Genet 22, 347350.
76Egger, G, Liang, G, Aparicio, A, et al. (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457463.
77Ou, JN, Torrisani, J, Unterberger, A, et al. (2007) Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem Pharmacol 73, 12971307.
78Muhlhausler, BS, Adam, CL, Findlay, PA, et al. (2006) Increased maternal nutrition alters development of the appetite-regulating network in the brain. FASEB J 20, 12571259.
79Franco, MC, Akamine, EH, Di Marco, GS, et al. (2003) NADPH oxidase and enhanced superoxide generation in intrauterine undernourished rats: involvement of the rennin–angiotensin system. Cardiovasc Res 59, 767775.
80Singhal, A, Cole, TJ & Lucas, A (2001) Early nutrition in preterm infants and later blood pressure: two cohorts after randomised trials. Lancet 357, 413419.
81Huxley, RR & Neil, HA (2004) Does maternal nutrition in pregnancy and birth weight influence levels of CHD risk factors in adult life? Br J Nutr 91, 459468.
82Martin, RM, Ebrahim, S, Griffin, M, et al. (2005) Breastfeeding and atherosclerosis: intima-media thickness and plaques at 65-year follow-up of the Boyd Orr cohort. Arterioscler Thromb Vasc Biol 25, 14821488.
83Napoli, C, Glass, CK, Witztum, JL, et al. (1999) Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet 354, 12341241.
84Palinski, W, D'Armiento, FP, Witztum, JL, et al. (2001) Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res 89, 991996.
85Eriksson, JG, Forsen, T, Tuomilehto, J, et al. (2001) Early growth and coronary heart disease in later life: longitudinal study. BMJ 322, 949953.
86Rich-Edwards, JW, Stampfer, MJ, Manson, JE, et al. (2004) Breastfeeding during infancy and the risk of cardiovascular disease in adulthood. Epidemiology 15, 550556.
87Martin, RM, Ben-Shlomo, Y, Gunnell, D, et al. (2005) Breast feeding and cardiovascular disease risk factors, incidence, and mortality: the Caerphilly study. J Epidemiol Commun Health 59, 121129.
88Godfrey, KM & Barker, DJ (2000) Fetal nutrition and adult disease. Am J Clin Nutr 71, Suppl. 5, 1344S1352S.
89McLeod, CJ, Pagel, I & Sack, MN (2005) The mitochondrial biogenesis regulatory program in cardiac adaptation to ischemia – a putative target for therapeutic intervention. Trends Cardiovasc Med 15, 118123.
90Huss, JM & Kelly, DP (2004) Nuclear receptor signaling and cardiac energetics. Circ Res 95, 568578.
91Huss, JM & Kelly, DP (2005) Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 115, 547555.
92Grynberg, A (2005) Effectors of fatty acid oxidation reduction: promising new anti-ischaemic agents. Curr Pharm Des 11, 489509.
93Paradies, G, Petrosillo, G, Pistolese, M, et al. (2004) Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res 94, 5359.
94Berger, A, Gershwin, ME & German, JB (1992) Effects of various dietary fats on cardiolipin acyl composition during ontogeny of mice. Lipids 27, 605612.
95Dong, F, Ford, SP, Fang, CX, et al. (2005) Maternal nutrient restriction during early to mid gestation up-regulates cardiac insulin-like growth factor (IGF) receptors associated with enlarged ventricular size in fetal sheep. Growth Horm IGF Res 15, 291299.
96Han, HC, Austin, KJ, Nathanielsz, PW, et al. (2004) Maternal nutrient restriction alters gene expression in the ovine fetal heart. J Physiol 558, (Pt 1), 111121.
97Khan, IY, Taylor, PD, Dekou, V, et al. (2003) Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41, 168175.
98Ghosh, P, Bitsanis, D, Ghebremeskel, K, et al. (2001) Abnormal aortic fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy. J Physiol 533, 815822.
99Forsyth, JS, Willatts, P, Agostoni, C, et al. (2003) Long chain polyunsaturated fatty acid supplementation in infant formula and blood pressure in later childhood: follow up of a randomised controlled trial. BMJ 326, 953.
100Rodgers, A, Vaughan, P, Prentice, T, et al. (2002) The World Health Report: Reducing Risks, Promoting Healthy Life. Geneva: World Health Organisation.
101Cottrell, EC & Ozanne, SE (2007) Developmental programming of energy balance and the metabolic syndrome. Proc Nutr Soc 66, 198206.
102Laivuori, H, Gallaher, MJ, Collura, L, et al. (2006) Relationships between maternal plasma leptin, placental leptin mRNA and protein in normal pregnancy, pre-eclampsia and intrauterine growth restriction without pre-eclampsia. Mol Hum Reprod 12, 551556.
103Smith-Kirwin, SM, O'Connor, DM, De Johnston, J, et al. (1998) Leptin expression in human mammary epithelial cells and breast milk. J Clin Endocrinol Metab 83, 18101813.
104Uysal, FK, Onal, EE, Aral, YZ, et al. (2002) Breast milk leptin: its relationship to maternal and infant adiposity. Clin Nutr 21, 157160.
105Friedman, JM & Halaas, JL (1998) Leptin and the regulation of body weight in mammals. Nature 395, 763770.
106Bouret, SG, Draper, SJ & Simerly, RB (2004) Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304, 108110.
107Bouret, SG & Simerly, RB (2006) Developmental programming of hypothalamic feeding circuits. Clin Genet 70, 295301. Review.
108Bouret, SG, Gorski, JN, Patterson, CM, et al. (2008) Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab 7, 179185.
109Vickers, MH, Gluckman, PD, Coveny, AH, et al. (2005) Neonatal leptin treatment reverses developmental programming. Endocrinology 146, 42114216.
110Solomon, G, Niv-Spector, L, Gonen-Berger, D, et al. (2006) Preparation of leptin antagonists by site-directed mutagenesis of human, ovine, rat, and mouse leptin's site III: implications on blocking undesired leptin action in vivo. Ann N Y Acad Sci 1091, 531539.
111Attig, L, Solomon, G & Taouis, M, et al. (2007) Early postnatal leptin blockage induces a long term leptin resistance in rats Pre-congress satellite meeting on ‘Early Nutrition Programming and health outcomes in later life’, European Congress on Obesity, Budapest.
112Jaquet, D, Leger, J, Levy-Marchal, C, et al. (1998) Ontogeny of leptin in human fetuses and newborns: effect of intrauterine growth retardation on serum leptin concentrations. J Clin Endocrinol Metab 83, 12431246.
113Grayson, BE, Allen, SE, Billes, SK, et al. (2006) Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 143, 975986.
114Savino, F, Nanni, GE, Maccario, S, et al. (2004) Breast-fed infants have higher leptin values than formula-fed infants in the first four months of life. J Pediatr Endocrinol Metab 17, 15271532.
115von Kries, R, Koletzko, B, Sauerwald, T, et al. (1999) Breast feeding and obesity: cross-sectional study. BMJ 17, 147150.
116Pico, C, Oliver, P, Sanchez, J, et al. (2007) The intake of physiological doses of leptin during lactation in rats prevents obesity in later life. Int J Obes (Lond) 31, 11991209.
117Green, A & Patterson, CC (2001) Trends in the incidence of childhood-onset diabetes in Europe 1989–1998. Diabetologia 44 Suppl. 3, B3B8.
118Onkamo, P, Vaananen, S, Karvonen, M, et al. (1999) Worldwide increase in incidence of Type I diabetes – the analysis of the data on published incidence trends. Diabetologia 42, 13951403.
119Eisenbarth, GS (1986) Type I diabetes mellitus. A chronic autoimmune disease. N Engl J Med 314, 13601368.
120Atkinson, MA & Eisenbarth, GS (2001) Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 358, 221229.
121Ziegler, AG, Hillebrand, B, Rabl, W, et al. (1993) On the appearance of islet associated autoimmunity in offspring of diabetic mothers: a prospective study from birth. Diabetologia 36, 402408.
122Kupila, A, Muona, P, Simell, T, et al. (2001) Feasibility of genetic and immunological prediction of type I diabetes in a population-based birth cohort. Diabetologia 44, 290297.
123Rewers, M, Bugawan, TL, Norris, JM, et al. (1996) Newborn screening for HLA markers associated with IDDM: diabetes autoimmunity study in the young (DAISY). Diabetologia 39, 807812.
124Honeyman, MC, Coulson, BS, Stone, NL, et al. (2000) Association between rotavirus infection and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes 49, 13191324.
125Risch, N (1989) Genetics of IDDM: evidence for complex inheritance with HLA. Genet Epidemiol 6, 143148.
126Davies, JL, Kawaguchi, Y, Bennett, ST, et al. (1994) A genome-wide search for human type 1 diabetes susceptibility genes. Nature 371, 130136.
127Cox, NJ, Wapelhorst, B, Morrison, VA, et al. (2001) Seven regions of the genome show evidence of linkage to type 1 diabetes in a consensus analysis of 767 multiplex families. Am J Hum Genet 69, 820830.
128Kyvik, KO, Green, A & Beck-Nielsen, H (1995) Concordance rates of insulin dependent diabetes mellitus: a population based study of young Danish twins. BMJ 311, 913917.
129Hummel, M, Bonifacio, E, Schmid, S, et al. (2004) Brief communication: early appearance of islet autoantibodies predicts childhood type 1 diabetes in offspring of diabetic parents. Ann Intern Med 140, 882886.
130Kimpimaki, T, Kulmala, P, Savola, K, et al. (2002) Natural history of beta-cell autoimmunity in young children with increased genetic susceptibility to type 1 diabetes recruited from the general population. J Clin Endocrinol Metab 87, 45724579.
131Couper, JJ, Beresford, S, Hirte, C, et al. (2009) Weight gain in early life predicts risk of islet autoimmunity in children with first degree relative with type 1 diabetes. Diabetes Care 32, 9499.
132Sadauskaite-Kuehne, V, Ludvigsson, J, Padaiga, Z, et al. (2004) Longer breastfeeding is an independent protective factor against development of type 1 diabetes mellitus in childhood. Diabetes Metab Res Rev 20, 150157.
133Vaarala, O, Knip, M, Paronen, J, et al. (1999) Cow's milk formula feeding induces primary immunization to insulin in infants at genetic risk for type 1 diabetes. Diabetes 48, 13891394.
134Couper, JJ, Steele, C, Beresford, S, et al. (1999) Lack of association between duration of breast-feeding or introduction of cow's milk and development of islet autoimmunity. Diabetes 48, 21452149.
135Norris, JM, Beaty, B, Klingensmith, G, et al. (1996) Lack of association between early exposures to cow's milk protein and beta-cell autoimmunity. Diabetes Autoimmunity Study in the Young (DAISY). JAMA 276, 609614.
136Hummel, M, Fuchtenbusch, M, Schenker, M, et al. (2000) No major association of breast-feeding, vaccinations, and childhood viral diseases with early islet autoimmunity in the German BABYDIAB Study. Diabetes Care 23, 969974.
137Virtanen, SM, Kenward, MG, Erkkola, M, et al. (2006) Age at introduction of new foods and advanced beta cell autoimmunity in young children with HLA-conferred susceptibility to type 1 diabetes. Diabetologia 49, 15121521.
138Lupopajarvi, K, Savilahti, E, Virtanen, SM, et al. (2008) Enhanced levels of cow's milk antibodies in infancy in children who develop type 1 diabetes later in childhood. Pediatr Diabetes 9, 434—441.
139Ziegler, AG, Schmid, S, Huber, D, et al. (2003) Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies. JAMA 290, 17211728.
140Norris, JM, Barriga, K, Klingensmith, G, et al. (2003) Timing of initial cereal exposure in infancy and risk of islet autoimmunity. JAMA 290, 17131720.
141Fronczak, CM, Barón, AE, Chase, HP, et al. (2003) In utero dietary exposures and risk of islet autoimmunity in children. Diabetes Care 26, 32373242.
142Zipitis, CS & Akobeng, AK (2008) Supplementation in early childhood and risk of type 1 diabetes: a systematic review and meta-analysis. Arch Dis Child 93, 512517.
143Sadeharju, K, Hamalainen, AM, Knip, M, et al. (2003) Enterovirus infections as a risk factor for type I diabetes: virus analyses in a dietary intervention trial. Clin Exp Immunol 132, 271277.
144Schmid, S, Buuck, D, Knopff, A, et al. (2004) BABYDIET, a feasibility study to prevent the appearance of islet autoantibodies in relatives of patients with Type 1 diabetes by delaying exposure to gluten. Diabetologia 47, 11301131.
145Greeley, SA, Katsumata, M, Yu, L, et al. (2002) Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nat Med 8, 399402.
146Koczwara, K, Ziegler, AG & Bonifacio, E (2004) Maternal immunity to insulin does not affect diabetes risk in progeny of non obese diabetic mice. Clin Exp Immunol 136, 5659.
147Melanitou, E, Devendra, D, Liu, E, et al. (2004) Early and quantal (by litter) expression of insulin autoantibodies in the nonobese diabetic mice predict early diabetes onset. J Immunol 173, 66036610.
148Koczwara, K, Bonifacio, E & Ziegler, AG (2004) Transmission of maternal islet antibodies and risk of autoimmune diabetes in offspring of mothers with type 1 diabetes. Diabetes 53, 14.
149Warram, JH, Krolewski, AS, Gottlieb, MS, et al. (1984) Differences in risk of insulin-dependent diabetes in offspring of diabetic mothers and diabetic fathers. N Engl J Med 311, 149152.
150Pociot, F, Norgaard, K, Hobolth, N, et al. (1993) A nationwide population-based study of the familial aggregation of type 1 (insulin-dependent) diabetes mellitus in Denmark. Danish Study Group of Diabetes in Childhood. Diabetologia 36, 870875.
151TEDDY investigators (USA – Denver Augusta/Gainesville, Seattle, Tampa; Germany – Munich; Finland – Turku, Tampere, Oulu; Sweden – Malmö) (2004) The environmental determinants of diabetes in the young study (Abstract). In Programme and Abstracts. Cambridge: Immunology of Diabetes Society Conference, p. 160.
152Bornstein, MH, Hahn, CS, Bell, C, et al. (2006) Stability in cognition across childhood: a developmental cascade. Psychol Sci 17, 151158.
153Batty, GD, Deary, IJ & Gottfredson, LS (2007) Pre-morbid (early life) IQ and later mortality risk: systematic review. Ann Epidemiol 17, 278288.
154Zammit, S, Allebeck, P, David, AS, et al. (2004) Longitudinal study of premorbid IQ Score and risk of developing schizophrenia, bipolar disorder, severe depression, and other nonaffective psychoses. Arch Gen Psychiatry 61, 354360.
155Gunnell, D, Harrison, G, Whitley, E, et al. (2005) The association of fetal and childhood growth with risk of schizophrenia. Cohort study of 720,000 Swedish men and women. Schizophr Res 79, 315322.
156Osler, M, Lawlor, DA & Nordentoft, M (2007) Cognitive function in childhood and early adulthood and hospital admission for schizophrenia in Danish men born in 1953. Schizophr Res 92, 132141.
157Mittendorfer-Rutz, E, Rasmussen, F & Wasserman, D (2004) Restricted fetal growth and adverse maternal psychosocial and socioeconomic conditions as risk factors for suicidal behaviour of offspring: a cohort study. Lancet 364, 11351140.
158Batty, GD & Deary, IJ (2004) Early life intelligence and adult health. BMJ 329, 585586.
159Hart, CL, Taylor, MD, Smith, GD, et al. (2005) Childhood IQ and all-cause mortality before and after age 65: prospective observational study linking the Scottish Mental Survey 1932 and the Midspan studies. Br J Health Psychol 10, 153165.
160Shenkin, SD, Starr, JM, Pattie, A, et al. (2001) Birth weight and cognitive function at age 11 years: the Scottish Mental Survey 1932. Arch Dis Child 85, 189197.
161Richards, M, Hardy, R, Kuh, D, et al. (2001) Birth weight and cognitive function in the British 1946 birth cohort: longitudinal population-based study. BMJ 322, 199203.
162Wiles, NJ, Peters, TJ, Heron, J, et al. (1996) Fetal growth and behavioural problems: results from the ALSPAC cohort. Am J Epidemiol 163, 829837.
163Isaacs, EB, Gadian, DG, Sabatini, S, et al. (2008) The effect of early human diet on caudate volumes and IQ. Pediatr Res 63, 308—314.
164Hibbeln, JR, Davis, JM, Steer, C, et al. (2007) Maternal seafood consumption in pregnancy and neurodevelopment outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 369, 578585.
165Rogers, I, Emmett, P, Baker, D, et al. (1998) Financial difficulties, smoking habits, composition of the diet and birthweight in a population of pregnant women in the South West of England. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Eur J Clin Nutr 52, 251260.
166Williams, C, Birch, EE, Emmett, PM, et al. (2001) Avon Longitudinal Study of Pregnancy and Childhood Study Team. Stereoacuity at age 3·5 y in children born full-term is associated with prenatal and postnatal dietary factors: a report from a population-based cohort study. Am J Clin Nutr 73, 316322.
167Black, RE (2001) Micronutrients in pregnancy. Br J Nutr 85, S193S197.
168Santiago-Fernandez, P, Torres-Barahona, R, Muela-Martinez, JA, et al. (2004) Intelligence quotient and iodine intake: a cross-sectional study in children. J Clin Endocrinol Metab 89, 38513857.
169Kibirige, MS, Hutchison, S, Owen, CJ, et al. (2004) Prevalence of maternal dietary iodine insufficiency in the north east of England: implications for the fetus. Arch Dis Child Fetal Neonatal Ed 89, F436F439.
170Beard, J (2007) Recent evidence from human and animal studies regarding iron status and infant development. J Nutr 137, 524S530S.
171Blaise, SA, Nedelec, E, Schroeder, H, et al. (2007) Gestational vitamin B deficiency leads to homocysteine-associated brain apoptosis and alters neurobehavioral development in rats. Am J Pathol 170, 667679.
172Zeisel, SH (2006) The fetal origins of memory: the role of dietary choline in optimal brain development. J Pediatr 149, S131S136.
173Bhatnagar, S & Taneja, S (2001) Zinc and cognitive development. Br J Nutr 85, S139S145.
174McGrath, JJ, Feron, FP, Burne, TH, et al. (2004) Vitamin D3-implications for brain development. J Steroid Biochem Mol Biol 89–90, 557560.
175Herz, J & Chen, Y (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7, 850859.
176Perry, I (1997) Fetal growth and development: the role of nutrition and other factors. In A lifecourse approach to chronic disease epidemiology, pp. 145168 [Kuh, D and Ben Shlomo, Y, editors]. Oxford: OUP.
177Lucas, A (1998) Programming by early nutrition: an experimental approach. J Nutr 128, 401S406S.
178Morgane, PJ, Austin-LaFrance, R, Bronzino, J, et al. (1993) Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev 17, 91128.
179Susser, E, Hoek, HW & Brown, A (1998) Neurodevelopmental disorders after prenatal famine: the story of the Dutch Famine Study. Am J Epidemiol 147, 213216.
180McClellan, JM, Susser, E & King, MC (2006) Maternal famine, de novo mutations, and schizophrenia. JAMA 296, 582584.
181Lawlor, DA, Ronalds, G, Clarke, H, et al. (2006) Season of birth and childhood intelligence: findings from the Aberdeen Children of the 1950s cohort study. Br J Educ Psychol 76, 481499.
182Jacobson, JL, Jacobson, SW, Muckle, G, et al. (2008) Beneficial effects of a polyunsaturated fatty acid on infant development: evidence from the Inuit of Arctic Quebec. J Pediatr 152, 356364.
183Fleith, M & Clandinin, MT (2005) Dietary PUFA for preterm and term infants: review of clinical studies. Crit Rev Food Sci Nutr 45, 205229. Review.
184Eilander, A, Hundscheid, DC, Osendarp, SJ, et al. (2007) Effects of n-3 long chain polyunsaturated fatty acid supplementation on visual and cognitive development throughout childhood: a review of human studies. Prostaglandins Leukot Essent Fatty Acids 76, 189203. Review.
185McCann, JC & Ames, BN (2005) Is docosahexaenoic acid, an n-3 long-chain polyunsaturated fatty acid, required for development of normal brain function? An overview of evidence from cognitive and behavioral tests in humans and animals. Am J Clin Nutr 82, 281295.
186Helland, IB, Smith, L, Saarem, K, et al. (2003) Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age. Pediatrics 111, e39e44.
187Zhou, SJ, Gibson, RA, Crowther, CA, et al. (2006) Effect of iron supplementation during pregnancy on the intelligence quotient and behavior of children at 4 y of age: long-term follow-up of a randomized controlled trial. Am J Clin Nutr 83, 11121117.
188Davey Smith, G & Ebrahim, S (2005) What can mendelian randomisation tell us about modifiable behavioural and environmental exposures? BMJ 330, 10761079.
189Davey Smith, G & Ebrahim, S (2004) Mendelian randomization: prospects, potentials, and limitations. Int J Epidemiol 33, 3042.
190Bouwstra, H, Dijck-Brouwer, DA, Wildeman, JA, et al. (2003) Long-chain polyunsaturated fatty acids have a positive effect on the quality of general movements of healthy term infants. Am J Clin Nutr 78, 313318.
191Smithers, LG, Gibson, RA, McPhee, A, et al. (2008) Effect of long-chain polyunsaturated fatty acid supplementation of preterm infants on disease risk and neurodevelopment: a systematic review of randomized controlled trials. Am J Clin Nutr 87, 912920. Review.
192Davey Smith, G & Ebrahim, S (2003) ‘Mendelian randomization’: can genetic epidemiology contribute to understanding environmental determinants of disease? Int J Epidemiol 32, 122.
193Botto, LD & Yang, Q (2000) 5, 10-Methylenetetrahydrofolate reductase gene variants and congenital anomalies: a HuGE review. Am J Epidemiol 151, 862877.
194Spittle, AJ, Orton, J, Doyle, LW, et al. (2007) Early developmental intervention programs post hospital discharge to prevent motor and cognitive impairments in preterm infants. The Cochrane Database System Reviews, 18(2), CD005495.
195Garn, H & Renz, H (2007) Epidemiological and immunological evidence for the hygiene hypothesis. Immunobiology 212, 441452.
196Kabesch, M & Lauener, RP (2004) Why Old McDonald had a farm but no allergies: genes, environments, and the hygiene hypothesis. J Leukoc Biol 75, 383387.
197Renz, H & Herz, U (2002) The bidirectional capacity of bacterial antigens to modulate allergy and asthma. Eur Respir J 19, 158171.
198von Mutius, E (2007) Allergies, infections and the hygiene hypothesis – the epidemiological evidence. Immunobiology 212, 433439.
199von Mutius, E & Schmid, S (2006) The PASTURE project: EU support for the improvement of knowledge about risk factors and preventive factors for atopy in Europe. Allergy 61, 407413.
200Prescott, SL, Macaubas, C, Smallacombe, T, et al. (1999) Development of allergen-specific T-cell memory in atopic and normal children. Lancet 353, 196200.
201Szepfalusi, Z, Nentwich, I, Gerstmayr, M, et al. (1997) Prenatal allergen contact with milk proteins. Clin Exp Allergy 27, 2835.
202Uthoff, H, Spenner, A, Reckelkamm, W, et al. (2003) Critical role of preconceptional immunization for protective and nonpathological specific immunity in murine neonates. J Immunol 171, 34853492.
203Antohe, F, Radulescu, L, Gafencu, A, et al. (2000) Expression of functionally active FcRn and the differentiated bidirectional transport of IgG in human placental endothelial cells. Hum Immunol 62, 93105.
204Gutierrez, G, Gentile, T, Miranda, S, et al. (2005) Asymmetric antibodies: a protective arm in pregnancy. In Immunology of Pregnancy. [Markert UR, editor] Karger, Chem Immunol Allergy 89, 158–168.
205Szepfalusi, Z, Loibichler, C, Pichler, J, et al. (2000) Direct evidence for transplacental allergen transfer. Pediatr Res 48, 404.
206Breuer, K, Wittmann, M, Bosche, B, et al. (2000) Severe atopic dermatitis is associated with sensitization to staphylococcal enterotoxin B (SEB). Allergy 55, 551555.
207Bunikowski, R, Mielke, M, Skarabis, H, et al. (1999) Prevalence and role of serum IgE antibodies to the Staphylococcus aureus-derived superantigens SEA and SEB in children with atopic dermatitis. J Allergy Clin Immunol 103, (1 Pt 1), 119124.
208Waser, M, Michels, KB, Bieli, C, et al. (2006) Inverse association of farm milk consumption with asthma and allergy in rural and suburban populations across Europe. Clin Exp Allergy 37, 661670.
209Batra, A, Pietsch, J, Fedke, I, et al. (2007) Leptin-dependent toll-like receptor expression and responsiveness in preadipocytes and adipocytes. Am J Pathol 170, 19311941.
210Fantuzzi, G, Sennello, JA, Batra, A, et al. (2005) Defining the role of T cell-derived leptin in the modulation of hepatic or intestinal inflammation in mice. Clin Exp Immunol 142, 3138.
211Froicu, M & Cantorna, MT (2007) Vitamin D and the vitamin D receptor are critical for control of the innate immune response to colonic injury. BMC Immunol 8, 1–11.
212Reichrath, J, Lehmann, B, Carlberg, C, et al. (2006) Vitamins as hormones. Horm Metab Res 39, 71–84.
213Blümer, N, Sel, S, Virna, S, et al. (2007) Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin Exp Allergy 37, 348357.
214Kalliomaki, M, Salminen, S, Poussa, T, et al. (2003) Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361, 18691871.
215Boehm, G, Jelinek, J, Knol, J, et al. (2004) Prebiotics and immune responses. J Pediatr Gastroenterol Nutr 39, Suppl. 3, S772S773. Review.
216Wegmann, M, Fehrenbach, H, Fehrenbach, A, et al. (2005) Involvement of distal airways in a chronic model of experimental asthma. Clin Exp Allergy 35, 12631271.
217Torgerson, C (2001) The effective management of osteoporosis. In The Economics of Fracture Prevention, pp. 111121 [Barlow, DH, Francis, RM and Miles, A, editors].
218UK coronary Heart Disease Statistics (2009-2010). British Heart Foundation. Resource Code: G30U/0210. Date Published: 15/02/2010. = 1001141.
219Winsloe, C, Earl, S, Dennison, EM, et al. (2009) Early life factors in the pathogenesis of osteoporosis. Curr Osteroporosis Rep 7, 140144.
220Tobias, JH, Steer, CD, Emmett, PM, et al. (2005) Bone mass in childhood is related to maternal diet in pregnancy. Osteoporos Int 16, 17311741.
221Nguyen, TV, Center, JR & Eisman, JA (2004) Bone mineral density-independent association of quantitative ultrasound measurements and fracture risk in women. Osteoporos Int 15, 942947.
222Rauchenzauner, M, Schmid, A, Heinz-Erian, P, et al. (2007) Sex- and age-specific reference curves for serum markers of bone turnover in healthy children from 2 months to 18 years. J Clin Endocrinol Metab 92, 443449.
223Clark, EM, Ness, AR, Bishop, NJ, et al. (2006) Association between bone mass and fractures in children: a prospective cohort study. J Bone Miner Res 21, 14891495.
224Goulding, A, Jones, IE, Taylor, RW, et al. (2000) More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res 15, 20112018.
225Hernandez, CJ, Beaupré, GS & Carter, DR (2003) A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporosis Int 14, 843847.
226Godfrey, K, Walker-Bone, K, Robinson, S, et al. (2001) Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res 16, 16941703.
227Javaid, MK, Godfrey, KM, Taylor, P, et al. (2005) Umbilical cord leptin predicts neonatal bone mass. Calcif Tissue Int 76, 341347.
228Javaid, MK, Godfrey, KM, Taylor, P, et al. (2004) Umbilical venous IGF-1 concentration, neonatal bone mass, and body composition. J Bone Miner Res 19, 5663.
229Cooper, C, Fall, C, Egger, P, et al. (1997) Growth in infancy and bone mass in later life. Ann Rheum Dis 56, 1721.
230Cooper, C, Cawley, M, Bhalla, A, et al. (1995) Childhood growth, physical activity, and peak bone mass in women. J Bone Miner Res 10, 940947.
231Jones, G & Dwyer, T (2000) Birth weight, birth length, and bone density in prepubertal children: evidence for an association that may be mediated by genetic factors. Calcif Tissue Int 67, 304308.
232Fewtrell, M, Prentice, A, Cole, TJ, et al. (2000) Effects of growth during infancy and childhood on bone mineralization and turnover in preterm children aged 8–12 years. Acta Paediatr 89, 148153.
233Fall, C, Hindmarsh, P, Dennison, E, et al. (1998) Programming of growth hormone secretion and bone mineral density in elderly men: a hypothesis. J Clin Endocrinol Metab 83, 135139.
234Weiler, HA, Yuen, CK & Seshia, MM (2002) Growth and bone mineralization of young adults weighing less than 1500 g at birth. Early Hum Dev 67, 101112.
235Javaid, MK, Lekamwasam, S, Clark, J, et al. (2006) Infant growth influences proximal femoral geometry in adulthood. J Bone Miner Res 21, 508512.
236Cooper, C, Eriksson, JG, Forsen, T, et al. (2001) Maternal height, childhood growth and risk of hip fracture in later life: a longitudinal study. Osteoporos Int 12, 623629.
237Fewtrell, MS, Prentice, A, Jones, SC, et al. (1999) Bone mineralization and turnover in preterm infants at 8–12 years of age: the effect of early diet. J Bone Miner Res 14, 810820.
238Fewtrell, M, Cole, TJ, Bishop, NJ, et al. (2000) Neonatal factors predicting childhood height in preterm infants: evidence for a persisting effect of early metabolic bone disease? J Pediatrics 137, 668673.
239Winzenberg, TM, Shaw, K, Fryer, J, et al. (2006) Calcium supplementation for improving bone mineral density in children. The Cochrane Database System Reviews issue 2, CD005119.
240Fuchs, RK & Snow, CM (2002) Gains in hip bone mass from high-impact training are maintained: a randomized controlled trial in children. J Pediatr 141, 357362.
241Specker, B, Binkley, T & Fahrenwald, N (2004) Increased periosteal circumference remains present 12 months after an exercise intervention in preschool children. Bone 35, 13831388.
242Iuliano-Burns, S, Saxon, L, Naughton, G, et al. (2003) Regional specificity of exercise and calcium during skeletal growth in girls: a randomized controlled trial. J Bone Miner Res 18, 156162.
243Hibbeln, JR, Davis, JM, Steer, C, et al. (2007) Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 369, 578585.
244Daniels, JL, Longnecker, MP, Rowland, AS, et al. (2004) Fish intake during pregnancy and early cognitive development of offspring. Epidemiology 15, 394402.
245Ong, KK, Emmett, PM, Noble, S, et al. (2006) Dietary energy intake at the age of 4 months predicts postnatal weight gain and childhood body mass index. Pediatrics 117, e503e508.
246Gunnell, D, Miller, LL, Rogers, I, et al. (2005) Association of insulin-like growth factor I and insulin-like growth factor-binding protein-3 with intelligence quotient among 8- to 9-year-old children in the Avon Longitudinal Study of Parents and Children. Pediatrics 116, e681e686.
247Shaheen, SO, Newson, RB, Henderson, AJ, et al. (2005) Prenatal paracetamol exposure and risk of asthma and elevated immunoglobulin E in childhood. Clin Exp Allergy 35, 1825.
248Lack, G, Fox, D, Northstone, K, et al. (2003) Factors associated with the development of peanut allergy in childhood. N Engl J Med 348, 977985.
249Ong, KK & Dunger, DB (2004) Birth weight, infant growth and insulin resistance. Eur J Endocrinol 151, U131U139.
250Gilbert, JS, Lang, AL, Grant, AR, et al. (2005) Maternal nutrient restriction in sheep: hypertension, decreased nephron number in offspring at 9 months of age. J Physiol (London) 565·1, 137148.
251Ford, SP, Hess, BW, Schwope, MM, et al. (2007) Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci 85, 12851294.
252Cleal, JK, Poore, KR, Boullin, JP, et al. (2007) Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. PNAS 104, 95299533.
253Fewtrell, MS, Williams, JE, Singhal, A, et al. (2009) Early diet and peak bone mass: 20 year follow-up of a randomized trial of early diet in infants born preterm. Bone 45, 142149.


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed