European Journal of Epidemiology

, Volume 21, Issue 2, pp 91–102

Hypotheses on the Fetal Origins of Adult Diseases: Contributions of Epidemiological Studies

  • Vincent W. V. Jaddoe
  • Jacqueline C. M. Witteman
Review

Abstract

Epidemiological studies have demonstrated associations between low birth weight and cardiovascular disease, type 2 diabetes and their risk factors in adult life. These findings have led to sharp debates in the literature concerning potential methodological study flaws and the effect size and causality of the associations. More recent studies seem to have overcome most methodological flaws and suggest a small effect size of low birth weight on adult diseases for the individual. However, the effect size may still be important on a population level. Various causal pathways have been hypothesized as mechanisms underlying these associations. These hypotheses have proposed central roles for (1) fetal undernutrition, (2) increased cortisol exposure, (3) genetic susceptibility and (4) accelerated post-natal growth. These hypotheses have been studied in various epidemiological study designs. Thus far, it is still not known which mechanisms underlie the associations between low birth weight and diseases in adult life. The causal pathways linking low birth weight to diseases in later life seem to be complex and may include combined environmental and genetic mechanisms in various periods of life. Well-designed epidemiological studies are necessary to estimate the population effect size and to identify the underlying mechanisms. This knowledge is needed to develop strategies for identifying groups at risk and prevention focused on early life.

Key words

Birth weight Cardiovascular disease Type 2 diabetes mellitus 

Abbreviations

11βHSD

11beta-hydroxysteroid-dehydrogenase

BMI

body mass index

IGF-1

insulin like growth factor-1

IGF-2

insulin like growth factor 2

INS VNTR

insulin variable number tandem repeat gene

PPARγ2

peroxisome proliferator-activated receptor gamma 2 gene

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Poulter, NR 2001Birthweights, maternal cardiovascular events, and Barker hypothesisLancet35719901991CrossRefPubMedGoogle Scholar
  2. 2.
    Kramer, MS, Joseph, KS 1996Enigma of fetal/infant-origins hypothesisLancet34812541255CrossRefPubMedGoogle Scholar
  3. 3.
    Paneth, N, Susser, M 1995Early origin of coronary heart disease (the “Barker hypothesis”)BMJ310411412PubMedGoogle Scholar
  4. 4.
    Frankel, S, Elwood, P, Sweetnam, P, Yarnell, J, Smith, GD 1996Birthweight, body-mass index in middle age, and incident coronary heart diseaseLancet34814781480PubMedGoogle Scholar
  5. 5.
    Curhan, GC, Willett, WC, Rimm, EB, Spiegelman, D, Ascherio, AL, Stampfer, MJ 1996Birth weight and adult hypertension, diabetes mellitus, and obesity in US menCirculation9432463250PubMedGoogle Scholar
  6. 6.
    Rich-Edwards, JW, Colditz, GA, Stampfer, MJ, Willett, WC, Gillman, MW, Hennekens, CH,  et al. 1999Birthweight and the risk for type 2 diabetes mellitus in adult womenAnn Intern Med130278284PubMedGoogle Scholar
  7. 7.
    Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ 1989Weight in infancy and death from ischaemic heart diseaseLancet2577580PubMedGoogle Scholar
  8. 8.
    Barker, DJ, Godfrey, KM, Osmond, C, Bull, A 1992The relation of fetal length, ponderal index and head circumference to blood pressure and the risk of hypertension in adult lifePaediatr Perinat Epidemiol63544PubMedGoogle Scholar
  9. 9.
    Huxley, R, Neil, A, Collins, R 2002Unravelling the fetal origins hypothesis: Is there really an inverse association between birthweight and subsequent blood pressure?Lancet360659665PubMedGoogle Scholar
  10. 10.
    Newsome, CA, Shiell, AW, Fall, CH, Phillips, DI, Shier, R, Law, CM 2003Is birth weight related to later glucose and insulin metabolism? – A systematic reviewDiabet Med20339348CrossRefPubMedGoogle Scholar
  11. 11.
    Tu, YK, West, R, Ellison, GT, Gilthorpe, MS 2005Why evidence for the fetal origins of adult disease might be a statistical artifact: The “reversal paradox” for the relation between birth weight and blood pressure in later lifeAm J Epidemiol1612732PubMedGoogle Scholar
  12. 12.
    Lucas, A, Fewtrell, MS, Cole, TJ 1999Fetal origins of adult disease-the hypothesis revisitedBMJ319245249PubMedGoogle Scholar
  13. 13.
    Kramer, MS 2000Invited commentary: association between restricted fetal growth and adult chronic disease: Is it causal? Is it important?Am J Epidemiol152605608CrossRefPubMedGoogle Scholar
  14. 14.
    Huxley, R, Owen, CG, Whincup, PH, Cook, DG, Colman, S, Collins, R 2004Birth weight and subsequent cholesterol levels: Exploration of the “fetal origins” hypothesisJAMA29227552764CrossRefPubMedGoogle Scholar
  15. 15.
    Schluchter, MD 2003Publication bias and heterogeneity in the relationship between systolic blood pressure, birth weight, and catch-up growth – A meta analysisJ Hypertens21273279CrossRefPubMedGoogle Scholar
  16. 16.
    Gluckman, PD, Hanson, MA 2004Living with the past: Evolution, development, and patterns of diseaseScience30517331736CrossRefPubMedGoogle Scholar
  17. 17.
    Barker, DJ, Gluckman, PD, Godfrey, KM, Harding, JE, Owens, JA., Robinson, JS 1993Fetal nutrition and cardiovascular disease in adult lifeLancet341938941CrossRefPubMedGoogle Scholar
  18. 18.
    Edwards, CR, Benediktsson, R, Lindsay, RS, Seckl, JR 1993Dysfunction of placental glucocorticoid barrier: Link between fetal environment and adult hypertension?Lancet341355357CrossRefPubMedGoogle Scholar
  19. 19.
    Hattersley, AT, Tooke, JE 1999The fetal insulin hypothesis: An alternative explanation of the association of low birthweight with diabetes and vascular diseaseLancet35317891792CrossRefPubMedGoogle Scholar
  20. 20.
    Singhal, A, Lucas, A 2004Early origins of cardiovascular disease: Is there a unifying hypothesis?Lancet36316421645PubMedGoogle Scholar
  21. 21.
    Barker, DJ 1995Fetal origins of coronary heart diseaseBMJ311171174PubMedGoogle Scholar
  22. 22.
    Bateson, P, Barker, D, Clutton-Brock, T, Deb, D, D’Udine, B, Foley, RA,  et al. 2004Developmental plasticity and human healthNature430419421CrossRefPubMedGoogle Scholar
  23. 23.
    Forsen, T, Eriksson, JG, Tuomilehto, J, Teramo, K, Osmond, C, Barker, DJ 1997Mother’s weight in pregnancy and coronary heart disease in a cohort of Finnish men: Follow up studyBMJ315837840PubMedGoogle Scholar
  24. 24.
    Shiell, AW, Campbell, DM, Hall, MH, Barker, DJ 2000Diet in late pregnancy and glucose–insulin metabolism of the offspring 40 years laterBJOG107890895PubMedGoogle Scholar
  25. 25.
    Mi, J, Law, C, Zhang, KL, Osmond, C, Stein, C, Barker, D 2000Effects of infant birthweight and maternal body mass index in pregnancy on components of the insulin resistance syndrome in ChinaAnn Intern Med132253260PubMedGoogle Scholar
  26. 26.
    Margetts, BM, Rowland, MG, Foord, FA, Cruddas, AM, Cole, TJ, Barker, DJ 1991The relation of maternal weight to the blood pressures of Gambian childrenInt J Epidemiol20938943PubMedGoogle Scholar
  27. 27.
    Godfrey, KM, Forrester, T, Barker, DJ, Jackson, AA, Landman, JP, Hall, JS,  et al. 1994Maternal nutritional status in pregnancy and blood pressure in childhoodBr J Obstet Gynaecol101398403PubMedGoogle Scholar
  28. 28.
    Laor, A, Stevenson, DK, Shemer, J, Gale, R, Seidman, DS 1997Size at birth, maternal nutritional status in pregnancy, and blood pressure at age 17: Population based analysisBMJ315449453PubMedGoogle Scholar
  29. 29.
    Clark, PM, Atton, C, Law, CM, Shiell, A, Godfrey, K, Barker, DJ 1998Weight gain in pregnancy, triceps skinfold thickness, and blood pressure in offspringObstet Gynecol91103107CrossRefPubMedGoogle Scholar
  30. 30.
    Adair, LS, Kuzawa, CW, Borja, J 2001Maternal energy stores and diet composition during pregnancy program adolescent blood pressureCirculation10410341039PubMedGoogle Scholar
  31. 31.
    Roseboom, TJ, Meulen, JH, Osmond, C, Barker, DJ, Ravelli, AC, Schroeder-Tanka, JM,  et al. 2000Coronary heart disease after prenatal exposure to the Dutch famine, 1944–1945Heart84595598CrossRefPubMedGoogle Scholar
  32. 32.
    Ravelli, AC, Meulen, JH, Michels, RP, Osmond, C, Barker, DJ, Hales, CN,  et al. 1998Glucose tolerance in adults after prenatal exposure to famineLancet351173177PubMedGoogle Scholar
  33. 33.
    Stanner, SA, Bulmer, K, Andres, C, Lantseva, OE, Borodina, V, Poteen, VV,  et al. 1997Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional studyBMJ31513421348PubMedGoogle Scholar
  34. 34.
    Sparen, P, Vagero, D, Shestov, DB, Plavinskaja, S, Parfenova, N, Hoptiar, V,  et al. 2004Long term mortality after severe starvation during the siege of Leningrad: prospective cohort studyBMJ3281114CrossRefPubMedGoogle Scholar
  35. 35.
    Campbell, DM, Hall, MH, Barker, DJ, Cross, J, Shiell, AW, Godfrey, KM 1996Diet in pregnancy and the offspring’s blood pressure 40 years laterBr J Obstet Gynaecol103273280PubMedGoogle Scholar
  36. 36.
    Shiell, AW, Campbell-Brown, M, Haselden, S, Robinson, S, Godfrey, KM, Barker, DJ 2001High-meat, low-carbohydrate diet in pregnancy: relation to adult blood pressure in the offspringHypertension3812821288PubMedGoogle Scholar
  37. 37.
    Huh, SY, Rifas-Shiman, SL, Kleinman, KP, Rich-Edwards, JW, Lipshultz, SE, Gillman, MW. 2004Maternal protein intake is not associated with infant blood pressureInt J Epidemiol34378384PubMedGoogle Scholar
  38. 38.
    Belizan, JM, Villar, J, Bergel, E, Pino, A, Di Fulvio, S, Galliano, SV,  et al. 1997Long-term effect of calcium supplementation during pregnancy on the blood pressure of offspring: follow up of a randomised controlled trialBMJ315281285PubMedGoogle Scholar
  39. 39.
    Hatton, DC, Harrison-Hohner, J, Coste, S, Reller, M, McCarron, D 2003Gestational calcium supplementation and blood pressure in the offspringAm J Hypertens16801805CrossRefPubMedGoogle Scholar
  40. 40.
    Gillman, MW, Rifas-Shiman, SL, Kleinman, KP, Rich-Edwards, JW, Lipshultz, SE 2004Maternal calcium intake and offspring blood pressureCirculation11019901995CrossRefPubMedGoogle Scholar
  41. 41.
    Morley, R, Carlin, JB, Dwyer, T 2004Maternal calcium supplementation and cardiovascular risk factors in twin offspringInt J Epidemiol3313041309CrossRefPubMedGoogle Scholar
  42. 42.
    Godfrey, KM, Barker, DJ 2000Fetal nutrition and adult diseaseAm J Clin Nutr711344S1352SPubMedGoogle Scholar
  43. 43.
    Smith, GC, Pell, JP, Walsh, D 2001Pregnancy complications and maternal risk of ischaemic heart disease: A retrospective cohort study of 129,290 birthsLancet35720022006PubMedGoogle Scholar
  44. 44.
    Mackenzie, HS, Brenner, BM 1995Fewer nephrons at birth: A missing link in the etiology of essential hypertension?Am J Kidney Dis269198PubMedGoogle Scholar
  45. 45.
    Martyn, CN, Greenwald, SE 1997Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertensionLancet350953955PubMedGoogle Scholar
  46. 46.
    Hinchliffe, SA, Lynch, MR, Sargent, PH, Howard, CV, Velzen, D 1992The effect of intrauterine growth retardation on the development of renal nephronsBr J Obstet Gynaecol99296301PubMedGoogle Scholar
  47. 47.
    Keller, G, Zimmer, G, Mall, G, Ritz, E, Amann, K 2003Nephron number in patients with primary hypertensionN Engl J Med348101108CrossRefPubMedGoogle Scholar
  48. 48.
    Spencer, J, Wang, Z, Hoy, W 2001Low birth weight and reduced renal volume in aboriginal childrenAm J Kidney Dis37915920PubMedGoogle Scholar
  49. 49.
    Singh, GR, Hoy, WE 2004Kidney volume, blood pressure, and albuminuria: Findings in an Australian aboriginal communityAm J Kidney Dis43254259CrossRefPubMedGoogle Scholar
  50. 50.
    Cheung, YF, Wong, KY, Lam, BC, Tsoi, NS 2004Relation of arterial stiffness with gestational age and birth weightArch Dis Child89217221CrossRefPubMedGoogle Scholar
  51. 51.
    Martyn, CN, Barker, DJ, Jespersen, S, Greenwald, S, Osmond, C, Berry, C 1995Growth in utero, adult blood pressure, and arterial complianceBr Heart J73116121PubMedGoogle Scholar
  52. 52.
    Seckl, JR 2004Prenatal glucocorticoids and long-term programmingEur J Endocrinol151U49U62PubMedGoogle Scholar
  53. 53.
    Schoof, E, Girstl, M, Frobenius, W, Kirschbaum, M, Dorr, HG, Rascher, W,  et al. 2001Decreased gene expression of 11beta-hydroxysteroid dehydrogenase type 2 and 15-hydroxyprostaglandin dehydrogenase in human placenta of patients with preeclampsiaJ Clin Endocrinol Metab8613131317CrossRefPubMedGoogle Scholar
  54. 54.
    Rogerson, FM, Kayes, KM, White, PC 1997Variation in placental type 2 11beta-hydroxysteroid dehydrogenase activity is not related to birth weight or placental weightMol Cell Endocrinol128103109CrossRefPubMedGoogle Scholar
  55. 55.
    Bocchi, B, Kenouch, S, Lamarre-Cliche, M, Muffat-Joly, M, Capron, MH, Fiet, J,  et al. 2004Impaired 11-beta hydroxysteroid dehydrogenase type 2 activity in sweat gland ducts in human essential hypertensionHypertension43803808CrossRefPubMedGoogle Scholar
  56. 56.
    Clark, PM 1998Programming of the hypothalamo–pituitary–adrenal axis and the fetal origins of adult disease hypothesisEur J Pediatr157S7S10PubMedGoogle Scholar
  57. 57.
    Phillips, DI, Walker, BR, Reynolds, RM, Flanagan, DE, Wood, PJ, Osmond, C,  et al. 2000Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populationsHypertension3513011306PubMedGoogle Scholar
  58. 58.
    Ward, AM, Syddall, HE, Wood, PJ, Chrousos, GP, Phillips, DI 2004Fetal programming of the hypothalamic–pituitary–adrenal (HPA) axis: Low birth weight and central HPA regulationJ Clin Endocrinol Metab8912271233PubMedGoogle Scholar
  59. 59.
    Pell, JP, Smith, GC, Walsh, D 2004Pregnancy complications and subsequent maternal cerebrovascular events: A retrospective cohort study of 119,668 birthsAm J Epidemiol159336342CrossRefPubMedGoogle Scholar
  60. 60.
    Lawlor, DA, Davey Smith, G, Ebrahim, S 2002Birth weight of offspring and insulin resistance in late adulthood: Cross sectional surveyBMJ325359362PubMedGoogle Scholar
  61. 61.
    Lindsay, RS, Dabelea, D, Roumain, J, Hanson, RL, Bennett, PH, Knowler, WC 2000Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetesDiabetes49445449PubMedGoogle Scholar
  62. 62.
    Yajnik, CS, Coyaji, KJ, Joglekar, CV, Kellingray, S, Fall, C 2001Paternal insulin resistance and fetal growth: Problem for the ‘fetal insulin’ and the ‘fetal origins’ hypothesesDiabetologia4411971198PubMedGoogle Scholar
  63. 63.
    Hypponen, E, Smith, GD, Power, C 2003Parental diabetes and birth weight of offspring: Intergenerational cohort studyBMJ3261920CrossRefPubMedGoogle Scholar
  64. 64.
    Yajnik, CS, Joglekar, CV, Pandit, AN, Bavdekar, AR, Bapat, SA, Bhave, SA,  et al. 2003Higher offspring birth weight predicts the metabolic syndrome in mothers but not fathers 8 years after delivery: The Pune children’s studyDiabetes5220902096PubMedGoogle Scholar
  65. 65.
    Wannamethee, SG, Lawlor, DA, Whincup, PH, Walker, M, Ebrahim, S, Davey-Smith, G 2004Birth weight of offspring and paternal insulin resistance and paternal diabetes in late adulthood: Cross sectional surveyDiabetologia471218PubMedGoogle Scholar
  66. 66.
    Poulsen, P, Vaag, AA, Kyvik, KO, Moller Jensen, D, Beck-Nielsen, H 1997Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairsDiabetologia40439446PubMedGoogle Scholar
  67. 67.
    Poulter, NR, Chang, CL, MacGregor, AJ, Snieder, H, Spector, TD 1999Association between birth weight and adult blood pressure in twins: Historical cohort studyBMJ31913301333PubMedGoogle Scholar
  68. 68.
    Dwyer, T, Blizzard, L, Morley, R, Ponsonby, AL 1999Within pair association between birth weight and blood pressure at age 8 in twins from a cohort studyBMJ31913251329PubMedGoogle Scholar
  69. 69.
    Loos, RJ, Fagard, R, Beunen, G, Derom, C, Vlietinck, R 2001Birth weight and blood pressure in young adults: A prospective twin studyCirculation10416331638PubMedGoogle Scholar
  70. 70.
    Iliadou, A, Cnattingius, S, Lichtenstein, P 2004Low birth weight and Type 2 diabetes: A study on 11,162 Swedish twinsInt J Epidemiol33948953; discussion 953–954CrossRefPubMedGoogle Scholar
  71. 71.
    Yzerman, RG, Stehouwer, CD, Boomsma, DI 2000Evidence for genetic factors explaining the birth weight-blood pressure relation. Analysis in twinsHypertension3610081012Google Scholar
  72. 72.
    Christensen, K, Stovring, H, McGue, M 2001Do genetic factors contribute to the association between birth weight and blood pressure?J Epidemiol Community Health55583587PubMedGoogle Scholar
  73. 73.
    Johansson-Kark, M, Rasmussen, F, Stavola, B, Leon, DA 2002Fetal growth and systolic blood pressure in young adulthood: The Swedish young male twins studyPaediatr Perinat Epidemiol16200209CrossRefPubMedGoogle Scholar
  74. 74.
    Hubinette, A, Cnattingius, S, Ekbom, A, Faire, U, Kramer, M, Lichtenstein, P 2001Birth weight, early environment, and genetics: A study of twins discordant for acute myocardial infarctionLancet35719972001CrossRefPubMedGoogle Scholar
  75. 75.
    Vagero, D, Leon, D 1994Ischaemic heart disease and low birth weight: A test of the fetal-origins hypothesis from the Swedish Twin RegistryLancet343260263PubMedGoogle Scholar
  76. 76.
    Zhang, J, Brenner, RA, Klebanoff, MA 2001Differences in birth weight and blood pressure at age 7 years among twinsAm J Epidemiol153779782PubMedGoogle Scholar
  77. 77.
    Baird, J, Osmond, C, MacGregor, A, Snieder, H, Hales, CN, Phillips, DI 2001Testing the fetal origins hypothesis in twins: The Birmingham twin studyDiabetologia443339CrossRefPubMedGoogle Scholar
  78. 78.
    Leon, DA 2001The fetal origins of adult disease: Interpreting the evidence from twin studiesTwin Res4321326CrossRefPubMedGoogle Scholar
  79. 79.
    Casteels, K, Ong, K, Phillips, D, Bendall, H, Pembrey, M 1999Mitochondrial 16189 variant, thinness at birth, and type-2 diabetes. ALSPAC study team. Avon longitudinal study of pregnancy and childhoodLancet35314991500CrossRefPubMedGoogle Scholar
  80. 80.
    Dunger, DB, Ong, KK, Huxtable, SJ, Sherriff, A, Woods, KA, Ahmed, ML,  et al. 1998Association of the INS VNTR with size at birth. ALSPAC study team. Avon longitudinal study of pregnancy and childhoodNat Genet1998100PubMedGoogle Scholar
  81. 81.
    Ong, KK, Phillips, DI, Fall, C, Poulton, J, Bennett, ST, Golding, J,  et al. 1999The insulin gene VNTR, type 2 diabetes and birth weightNat Genet21262263PubMedGoogle Scholar
  82. 82.
    Bazaes, RA, Petry, CJ, Ong, KK, Avila, A, Dunger, DB, Mericq, MV 2003Insulin gene VNTR genotype is associated with insulin sensitivity and secretion in infancyClin Endocrinol (Oxf)59599603CrossRefGoogle Scholar
  83. 83.
    Ong, KK, Petry, CJ, Barratt, BJ, Ring, S, Cordell, HJ, Wingate, DL,  et al. 2004Maternal–fetal interactions and birth order influence insulin variable number of tandem repeats allele class associations with head size at birth and childhood weight gainDiabetes5311281133PubMedGoogle Scholar
  84. 84.
    Bennett, AJ, Sovio, U, Ruokonen, A, Martikainen, H, Pouta, A, Taponen, S,  et al. 2004Variation at the insulin gene VNTR (variable number tandem repeat) polymorphism and early growth: Studies in a large Finnish birth cohortDiabetes5321262131PubMedGoogle Scholar
  85. 85.
    Mitchell, SM, Hattersley, AT, Knight, B, Turner, T, Metcalf, BS, Voss, LD,  et al. 2004Lack of support for a role of the insulin gene variable number of tandem repeats minisatellite (INS-VNTR) locus in fetal growth or type 2 diabetes-related intermediate traits in United Kingdom populationsJ Clin Endocrinol Metab89310317PubMedGoogle Scholar
  86. 86.
    Vaessen, N, Heutink, P, Janssen, JA, Witteman, JC, Testers, L, Hofman, A,  et al. 2001A polymorphism in the gene for IGF-I: Functional properties and risk for type 2 diabetes and myocardial infarctionDiabetes50637642PubMedGoogle Scholar
  87. 87.
    Vaessen, N, Janssen, JA, Heutink, P, Hofman, A, Lamberts, SW, Oostra, BA,  et al. 2002Association between genetic variation in the gene for insulin-like growth factor-I and low birth weightLancet35910361037CrossRefPubMedGoogle Scholar
  88. 88.
    Frayling, TM, Hattersley, AT, McCarthy, A, Holly, J, Mitchell, SM, Gloyn, AL,  et al. 2002A putative functional polymorphism in the IGF-I gene: Association studies with type 2 diabetes, adult height, glucose tolerance, and fetal growth in U.K.populationsDiabetes5123132316PubMedGoogle Scholar
  89. 89.
    Arends, N, Johnston, L, Hokken-Koelega, A, Duijn, C, Ridder, M, Savage, M,  et al. 2002Polymorphism in the IGF-I gene: Clinical relevance for short children born small for gestational age (SGA)J Clin Endocrinol Metab8727202724CrossRefPubMedGoogle Scholar
  90. 90.
    Johnston, LB, Dahlgren, J, Leger, J, Gelander, L, Savage, MO, Czernichow, P,  et al. 2003Association between insulin-like growth factor I (IGF-I) polymorphisms, circulating IGF-I, and pre- and post-natal growth in two European small for gestational age populationsJ Clin Endocrinol Metab8848054810CrossRefPubMedGoogle Scholar
  91. 91.
    Eriksson, JG, Lindi, V, Uusitupa, M, Forsen, TJ, Laakso, M, Osmond, C,  et al. 2002The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma 2 gene on insulin sensitivity and insulin metabolism interact with size at birthDiabetes5123212324PubMedGoogle Scholar
  92. 92.
    Yliharsila, H, Eriksson, JG, Forsen, T, Laakso, M, Uusitupa, M, Osmond, C,  et al. 2004Interactions between peroxisome proliferator-activated receptor-gamma 2 gene polymorphisms and size at birth on blood pressure and the use of antihypertensive medicationJ Hypertens2212831287PubMedGoogle Scholar
  93. 93.
    Kennedy, GC, German, MS, Rutter, WJ 1995The minisatellite in the diabetes susceptibility locus IDDM2 regulates insulin transcriptionNat Genet9293298CrossRefPubMedGoogle Scholar
  94. 94.
    Paquette, J, Giannoukakis, N, Polychronakos, C, Vafiadis, P, Deal, C 1998The INS 5’ variable number of tandem repeats is associated with IGF-2 expression in humansJ Biol Chem2731415814164CrossRefPubMedGoogle Scholar
  95. 95.
    Deeb, SS, Fajas, L, Nemoto, M, Pihlajamaki, J, Mykkanen, L, Kuusisto, J,  et al. 1998A Pro12Ala substitution in PPARgamma 2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivityNat Genet20284287CrossRefPubMedGoogle Scholar
  96. 96.
    Frayling, TM, Hattersley, AT, Smith, GD, Ben-Shlomo, Y 2002Conflicting results on variation in the IGFI gene highlight methodological considerations in the design of genetic association studiesDiabetologia4516051606PubMedGoogle Scholar
  97. 97.
    Hokken-Koelega, AC, Ridder, MA, Lemmen, RJ, Hartog, H, Muinck Keizer-Schrama, SM, Drop, SL 1995Children born small for gestational age: Do they catch up?Pediatr Res38267271PubMedGoogle Scholar
  98. 98.
    Forsen, T, Eriksson, J, Tuomilehto, J, Reunanen, A, Osmond, C, Barker, D 2000The fetal and childhood growth of persons who develop type 2 diabetesAnn Intern Med133176182PubMedGoogle Scholar
  99. 99.
    Eriksson, JG, Forsen, T, Tuomilehto, J, Osmond, C, Barker, DJ 2001Early growth and coronary heart disease in later life: Longitudinal studyBMJ322949953PubMedGoogle Scholar
  100. 100.
    Bhargava, SK, Sachdev, HS, Fall, CH, Osmond, C, Lakshmy, R, Barker, DJ,  et al. 2004Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthoodN Engl J Med350865875CrossRefPubMedGoogle Scholar
  101. 101.
    Ong, KK, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB 2000Association between postnatal catch-up growth and obesity in childhood: prospective cohort studyBMJ320967971CrossRefPubMedGoogle Scholar
  102. 102.
    Stettler, N, Zemel, BS, Kumanyika, S, Stallings, VA 2002Infant weight gain and childhood overweight status in a multicenter, cohort studyPediatrics109194199CrossRefPubMedGoogle Scholar
  103. 103.
    Singhal, A, Cole, TJ, Lucas, A 2001Early nutrition in pre-term infants and later blood pressure: Two cohorts after randomised trialsLancet357413419PubMedGoogle Scholar
  104. 104.
    Singhal, A, Fewtrell, M, Cole, TJ, Lucas, A 2003Low nutrient intake and early growth for later insulin resistance in adolescents born pretermLancet36110891097PubMedGoogle Scholar
  105. 105.
    Hofman, A, Jaddoe, VW, Mackenbach, JP, Moll, HA, Snijders, RF, Steegers, EA,  et al. 2004Growth, development and health from early fetal life until young adulthood: The generation R studyPaediatr Perinat Epidemiol186172CrossRefPubMedGoogle Scholar
  106. 106.
    Inskip HM, Godfrey KM, Robinson SM, Law CM, Barker DJ, Cooper C. Cohort profile: The Southampton women’s survey. Int J Epidemiol 2005. 10.1093/ije/dyi/202Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Vincent W. V. Jaddoe
    • 1
    • 2
    • 3
  • Jacqueline C. M. Witteman
    • 1
  1. 1.Department of Epidemiology and BiostatisticsErasmus Medical CenterRotterdamThe Netherlands
  2. 2.Department of PediatricsErasmus Medical Center, Sophia Children’s HospitalRotterdamThe Netherlands
  3. 3.Department of Epidemiology and BiostatisticsErasmus Medical CenterDR RotterdamThe Netherlands

Personalised recommendations