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. 2000 Jun;108(Suppl 3):545–553. doi: 10.1289/ehp.00108s3545

Fetal, infant, and childhood growth are predictors of coronary heart disease, diabetes, and hypertension in adult men and women.

C Osmond 1, D J Barker 1
PMCID: PMC1637808  PMID: 10852853

Abstract

Many human fetuses have to adapt to a limited supply of nutrients. In doing so they permanently change their structure and metabolism. These programmed changes may be the origins of a number of diseases in later life, including coronary heart disease, hypertension, and noninsulin- dependent diabetes. We review epidemiologic studies in which the incidence of these diseases has been related to the recorded, early growth of individuals, while considering factors in the adult lifestyle, such as obesity and socioeconomic status. We discuss possible mechanisms. For hypertension these mechanisms include placentation, maternal blood pressure, fetal undernutrition; childhood growth, activation of the renin-angiotensin system, renal structure, programming of the hypothalamic-pituitary-adrenal axis, vascular structure, and sympathetic nervous activity. For noninsulin-dependent diabetes we discuss mechanisms concerning both insulin resistance and insulin deficiency. We include a review of evidence for the programming of serum cholesterol and clotting factor concentrations. We address the timing of critical windows for coronary heart disease, reviewing studies that allow assessment of the relative importance of fetal, infant, and childhood growth. We argue for a research strategy that combines clinical, animal, and epidemiological studies.

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Selected References

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  1. Alvarsson M., Efendic S., Grill V. E. Insulin responses to glucose in healthy males are associated with adult height but not with birth weight. J Intern Med. 1994 Sep;236(3):275–279. doi: 10.1111/j.1365-2796.1994.tb00796.x. [DOI] [PubMed] [Google Scholar]
  2. Barker D. J., Bull A. R., Osmond C., Simmonds S. J. Fetal and placental size and risk of hypertension in adult life. BMJ. 1990 Aug 4;301(6746):259–262. doi: 10.1136/bmj.301.6746.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barker D. J. Fetal origins of coronary heart disease. BMJ. 1995 Jul 15;311(6998):171–174. doi: 10.1136/bmj.311.6998.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barker D. J., Gluckman P. D., Godfrey K. M., Harding J. E., Owens J. A., Robinson J. S. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993 Apr 10;341(8850):938–941. doi: 10.1016/0140-6736(93)91224-a. [DOI] [PubMed] [Google Scholar]
  5. Barker D. J., Godfrey K. M., Osmond C., Bull A. The relation of fetal length, ponderal index and head circumference to blood pressure and the risk of hypertension in adult life. Paediatr Perinat Epidemiol. 1992 Jan;6(1):35–44. doi: 10.1111/j.1365-3016.1992.tb00741.x. [DOI] [PubMed] [Google Scholar]
  6. Barker D. J., Hales C. N., Fall C. H., Osmond C., Phipps K., Clark P. M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993 Jan;36(1):62–67. doi: 10.1007/BF00399095. [DOI] [PubMed] [Google Scholar]
  7. Barker D. J., Martyn C. N., Osmond C., Hales C. N., Fall C. H. Growth in utero and serum cholesterol concentrations in adult life. BMJ. 1993 Dec 11;307(6918):1524–1527. doi: 10.1136/bmj.307.6918.1524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Barker D. J., Martyn C. N., Osmond C., Wield G. A. Abnormal liver growth in utero and death from coronary heart disease. BMJ. 1995 Mar 18;310(6981):703–704. doi: 10.1136/bmj.310.6981.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Barker D. J., Meade T. W., Fall C. H., Lee A., Osmond C., Phipps K., Stirling Y. Relation of fetal and infant growth to plasma fibrinogen and factor VII concentrations in adult life. BMJ. 1992 Jan 18;304(6820):148–152. doi: 10.1136/bmj.304.6820.148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Barker D. J., Osmond C., Golding J., Kuh D., Wadsworth M. E. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989 Mar 4;298(6673):564–567. doi: 10.1136/bmj.298.6673.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Barker D. J., Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986 May 10;1(8489):1077–1081. doi: 10.1016/s0140-6736(86)91340-1. [DOI] [PubMed] [Google Scholar]
  12. Barker D. J., Osmond C., Simmonds S. J., Wield G. A. The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. BMJ. 1993 Feb 13;306(6875):422–426. doi: 10.1136/bmj.306.6875.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ben-Shlomo Y., Smith G. D. Deprivation in infancy or in adult life: which is more important for mortality risk? Lancet. 1991 Mar 2;337(8740):530–534. doi: 10.1016/0140-6736(91)91307-g. [DOI] [PubMed] [Google Scholar]
  14. Brenner B. M., Chertow G. M. Congenital oligonephropathy: an inborn cause of adult hypertension and progressive renal injury? Curr Opin Nephrol Hypertens. 1993 Sep;2(5):691–695. [PubMed] [Google Scholar]
  15. Campbell A. G., Dawes G. S., Fishman A. P., Hyman A. I. Regional redistribution of blood flow in the mature fetal lamb. Circ Res. 1967 Aug;21(2):229–235. doi: 10.1161/01.res.21.2.229. [DOI] [PubMed] [Google Scholar]
  16. Campbell D. M., Hall M. H., Barker D. J., Cross J., Shiell A. W., Godfrey K. M. Diet in pregnancy and the offspring's blood pressure 40 years later. Br J Obstet Gynaecol. 1996 Mar;103(3):273–280. doi: 10.1111/j.1471-0528.1996.tb09718.x. [DOI] [PubMed] [Google Scholar]
  17. Chapman N., Mohamudally A., Cerutti A., Stanton A., Sayer A. A., Cooper C., Barker D., Rauf A., Evans J., Wormald R. Retinal vascular network architecture in low-birth-weight men. J Hypertens. 1997 Dec;15(12 Pt 1):1449–1453. doi: 10.1097/00004872-199715120-00012. [DOI] [PubMed] [Google Scholar]
  18. Churchill D., Perry I. J., Beevers D. G. Ambulatory blood pressure in pregnancy and fetal growth. Lancet. 1997 Jan 4;349(9044):7–10. doi: 10.1016/s0140-6736(96)06297-6. [DOI] [PubMed] [Google Scholar]
  19. Clark P. M., Atton C., Law C. M., Shiell A., Godfrey K., Barker D. J. Weight gain in pregnancy, triceps skinfold thickness, and blood pressure in offspring. Obstet Gynecol. 1998 Jan;91(1):103–107. doi: 10.1016/s0029-7844(97)00581-4. [DOI] [PubMed] [Google Scholar]
  20. Clark P. M., Hindmarsh P. C., Shiell A. W., Law C. M., Honour J. W., Barker D. J. Size at birth and adrenocortical function in childhood. Clin Endocrinol (Oxf) 1996 Dec;45(6):721–726. doi: 10.1046/j.1365-2265.1996.8560864.x. [DOI] [PubMed] [Google Scholar]
  21. DeFronzo R. A. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes. 1988 Jun;37(6):667–687. doi: 10.2337/diab.37.6.667. [DOI] [PubMed] [Google Scholar]
  22. Diamond J. Pearl Harbor and the Emperor's physiologists. Nat Hist. 1991;(12):2–7. [PubMed] [Google Scholar]
  23. Edwards C. R., Benediktsson R., Lindsay R. S., Seckl J. R. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet. 1993 Feb 6;341(8841):355–357. doi: 10.1016/0140-6736(93)90148-a. [DOI] [PubMed] [Google Scholar]
  24. Elford J., Whincup P., Shaper A. G. Early life experience and adult cardiovascular disease: longitudinal and case-control studies. Int J Epidemiol. 1991 Dec;20(4):833–844. doi: 10.1093/ije/20.4.833. [DOI] [PubMed] [Google Scholar]
  25. Eriksson J. G., Forsén T., Tuomilehto J., Winter P. D., Osmond C., Barker D. J. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ. 1999 Feb 13;318(7181):427–431. doi: 10.1136/bmj.318.7181.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Esler M., Julius S., Zweifler A., Randall O., Harburg E., Gardiner H., DeQuattro V. Mild high-renin essential hypertension. Neurogenic human hypertension? N Engl J Med. 1977 Feb 24;296(8):405–411. doi: 10.1056/NEJM197702242960801. [DOI] [PubMed] [Google Scholar]
  27. Fall C. H., Osmond C., Barker D. J., Clark P. M., Hales C. N., Stirling Y., Meade T. W. Fetal and infant growth and cardiovascular risk factors in women. BMJ. 1995 Feb 18;310(6977):428–432. doi: 10.1136/bmj.310.6977.428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Fall C. H., Pandit A. N., Law C. M., Yajnik C. S., Clark P. M., Breier B., Osmond C., Shiell A. W., Gluckman P. D., Barker D. J. Size at birth and plasma insulin-like growth factor-1 concentrations. Arch Dis Child. 1995 Oct;73(4):287–293. doi: 10.1136/adc.73.4.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Fall C. H., Stein C. E., Kumaran K., Cox V., Osmond C., Barker D. J., Hales C. N. Size at birth, maternal weight, and type 2 diabetes in South India. Diabet Med. 1998 Mar;15(3):220–227. doi: 10.1002/(SICI)1096-9136(199803)15:3<220::AID-DIA544>3.0.CO;2-O. [DOI] [PubMed] [Google Scholar]
  30. Farmer G., Russell G., Hamilton-Nicol D. R., Ogenbede H. O., Ross I. S., Pearson D. W., Thom H., Kerridge D. F., Sutherland H. W. The influence of maternal glucose metabolism on fetal growth, development and morbidity in 917 singleton pregnancies in nondiabetic women. Diabetologia. 1988 Mar;31(3):134–141. doi: 10.1007/BF00276845. [DOI] [PubMed] [Google Scholar]
  31. Ferns G. A., Motani A. S., Anggård E. E. The insulin-like growth factors: their putative role in atherogenesis. Artery. 1991;18(4):197–225. [PubMed] [Google Scholar]
  32. Folkow B. Structure and function of the arteries in hypertension. Am Heart J. 1987 Oct;114(4 Pt 2):938–948. doi: 10.1016/0002-8703(87)90591-6. [DOI] [PubMed] [Google Scholar]
  33. Forrester T. E., Wilks R. J., Bennett F. I., Simeon D., Osmond C., Allen M., Chung A. P., Scott P. Fetal growth and cardiovascular risk factors in Jamaican schoolchildren. BMJ. 1996 Jan 20;312(7024):156–160. doi: 10.1136/bmj.312.7024.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Forsén T., Eriksson J. G., Tuomilehto J., Teramo K., Osmond C., Barker D. J. Mother's weight in pregnancy and coronary heart disease in a cohort of Finnish men: follow up study. BMJ. 1997 Oct 4;315(7112):837–840. doi: 10.1136/bmj.315.7112.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Fowden A. L. Endocrine regulation of fetal growth. Reprod Fertil Dev. 1995;7(3):351–363. doi: 10.1071/rd9950351. [DOI] [PubMed] [Google Scholar]
  36. Fowden A. L. The role of insulin in prenatal growth. J Dev Physiol. 1989 Oct;12(4):173–182. [PubMed] [Google Scholar]
  37. Frankel S., Elwood P., Sweetnam P., Yarnell J., Smith G. D. Birthweight, body-mass index in middle age, and incident coronary heart disease. Lancet. 1996 Nov 30;348(9040):1478–1480. doi: 10.1016/S0140-6736(96)03482-4. [DOI] [PubMed] [Google Scholar]
  38. Godfrey K. M., Forrester T., Barker D. J., Jackson A. A., Landman J. P., Hall J. S., Cox V., Osmond C. Maternal nutritional status in pregnancy and blood pressure in childhood. Br J Obstet Gynaecol. 1994 May;101(5):398–403. doi: 10.1111/j.1471-0528.1994.tb11911.x. [DOI] [PubMed] [Google Scholar]
  39. Gompels U. A., Kasolo F. C. HHV-8 serology and Kaposi's sarcoma. Lancet. 1996 Dec 7;348(9041):1587–1588. doi: 10.1016/s0140-6736(05)66203-4. [DOI] [PubMed] [Google Scholar]
  40. Hales C. N., Barker D. J., Clark P. M., Cox L. J., Fall C., Osmond C., Winter P. D. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991 Oct 26;303(6809):1019–1022. doi: 10.1136/bmj.303.6809.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Hales C. N., Barker D. J. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992 Jul;35(7):595–601. doi: 10.1007/BF00400248. [DOI] [PubMed] [Google Scholar]
  42. Hales C. N., Desai M., Ozanne S. E., Crowther N. J. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans. 1996 May;24(2):341–350. doi: 10.1042/bst0240341. [DOI] [PubMed] [Google Scholar]
  43. Harding J. E., Johnston B. M. Nutrition and fetal growth. Reprod Fertil Dev. 1995;7(3):539–547. doi: 10.1071/rd9950539. [DOI] [PubMed] [Google Scholar]
  44. Hinchliffe S. A., Lynch M. R., Sargent P. H., Howard C. V., Van Velzen D. The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynaecol. 1992 Apr;99(4):296–301. doi: 10.1111/j.1471-0528.1992.tb13726.x. [DOI] [PubMed] [Google Scholar]
  45. Julius S., Krause L., Schork N. J., Mejia A. D., Jones K. A., van de Ven C., Johnson E. H., Sekkarie M. A., Kjeldsen S. E., Petrin J. Hyperkinetic borderline hypertension in Tecumseh, Michigan. J Hypertens. 1991 Jan;9(1):77–84. doi: 10.1097/00004872-199101000-00012. [DOI] [PubMed] [Google Scholar]
  46. Kingdom J. C., McQueen J., Connell J. M., Whittle M. J. Fetal angiotensin II levels and vascular (type I) angiotensin receptors in pregnancies complicated by intrauterine growth retardation. Br J Obstet Gynaecol. 1993 May;100(5):476–482. doi: 10.1111/j.1471-0528.1993.tb15276.x. [DOI] [PubMed] [Google Scholar]
  47. Konje J. C., Bell S. C., Morton J. J., de Chazal R., Taylor D. J. Human fetal kidney morphometry during gestation and the relationship between weight, kidney morphometry and plasma active renin concentration at birth. Clin Sci (Lond) 1996 Aug;91(2):169–175. doi: 10.1042/cs0910169. [DOI] [PubMed] [Google Scholar]
  48. Koupilová I., Leon D. A., Vågerö D. Can confounding by sociodemographic and behavioural factors explain the association between size at birth and blood pressure at age 50 in Sweden? J Epidemiol Community Health. 1997 Feb;51(1):14–18. doi: 10.1136/jech.51.1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kramer M. S., Joseph K. S. Enigma of fetal/infant-origins hypothesis. Lancet. 1996 Nov 9;348(9037):1254–1255. doi: 10.1016/s0140-6736(05)65750-9. [DOI] [PubMed] [Google Scholar]
  50. Langley S. C., Jackson A. A. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond) 1994 Feb;86(2):217–121. doi: 10.1042/cs0860217. [DOI] [PubMed] [Google Scholar]
  51. Law C. M., Barker D. J., Bull A. R., Osmond C. Maternal and fetal influences on blood pressure. Arch Dis Child. 1991 Nov;66(11):1291–1295. doi: 10.1136/adc.66.11.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Law C. M., Gordon G. S., Shiell A. W., Barker D. J., Hales C. N. Thinness at birth and glucose tolerance in seven-year-old children. Diabet Med. 1995 Jan;12(1):24–29. doi: 10.1111/j.1464-5491.1995.tb02057.x. [DOI] [PubMed] [Google Scholar]
  53. Law C. M., Shiell A. W. Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens. 1996 Aug;14(8):935–941. [PubMed] [Google Scholar]
  54. Law C. M., de Swiet M., Osmond C., Fayers P. M., Barker D. J., Cruddas A. M., Fall C. H. Initiation of hypertension in utero and its amplification throughout life. BMJ. 1993 Jan 2;306(6869):24–27. doi: 10.1136/bmj.306.6869.24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Leeson C. P., Whincup P. H., Cook D. G., Donald A. E., Papacosta O., Lucas A., Deanfield J. E. Flow-mediated dilation in 9- to 11-year-old children: the influence of intrauterine and childhood factors. Circulation. 1997 Oct 7;96(7):2233–2238. doi: 10.1161/01.cir.96.7.2233. [DOI] [PubMed] [Google Scholar]
  56. Leger J., Levy-Marchal C., Bloch J., Pinet A., Chevenne D., Porquet D., Collin D., Czernichow P. Reduced final height and indications for insulin resistance in 20 year olds born small for gestational age: regional cohort study. BMJ. 1997 Aug 9;315(7104):341–347. doi: 10.1136/bmj.315.7104.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Leon D. A., Koupilova I., Lithell H. O., Berglund L., Mohsen R., Vagero D., Lithell U. B., McKeigue P. M. Failure to realise growth potential in utero and adult obesity in relation to blood pressure in 50 year old Swedish men. BMJ. 1996 Feb 17;312(7028):401–406. doi: 10.1136/bmj.312.7028.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lever A. F., Harrap S. B. Essential hypertension: a disorder of growth with origins in childhood? J Hypertens. 1992 Feb;10(2):101–120. doi: 10.1097/00004872-199202000-00001. [DOI] [PubMed] [Google Scholar]
  59. Levy D., Garrison R. J., Savage D. D., Kannel W. B., Castelli W. P. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med. 1990 May 31;322(22):1561–1566. doi: 10.1056/NEJM199005313222203. [DOI] [PubMed] [Google Scholar]
  60. Lithell H. O., McKeigue P. M., Berglund L., Mohsen R., Lithell U. B., Leon D. A. Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ. 1996 Feb 17;312(7028):406–410. doi: 10.1136/bmj.312.7028.406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Lucas A. Role of nutritional programming in determining adult morbidity. Arch Dis Child. 1994 Oct;71(4):288–290. doi: 10.1136/adc.71.4.288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Mackenzie H. S., Brenner B. M. Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis. 1995 Jul;26(1):91–98. doi: 10.1016/0272-6386(95)90161-2. [DOI] [PubMed] [Google Scholar]
  63. Margetts B. M., Rowland M. G., Foord F. A., Cruddas A. M., Cole T. J., Barker D. J. The relation of maternal weight to the blood pressures of Gambian children. Int J Epidemiol. 1991 Dec;20(4):938–943. doi: 10.1093/ije/20.4.938. [DOI] [PubMed] [Google Scholar]
  64. Martyn C. N., Barker D. J., Jespersen S., Greenwald S., Osmond C., Berry C. Growth in utero, adult blood pressure, and arterial compliance. Br Heart J. 1995 Feb;73(2):116–121. doi: 10.1136/hrt.73.2.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Martyn C. N., Barker D. J., Osmond C. Mothers' pelvic size, fetal growth, and death from stroke and coronary heart disease in men in the UK. Lancet. 1996 Nov 9;348(9037):1264–1268. doi: 10.1016/s0140-6736(96)04257-2. [DOI] [PubMed] [Google Scholar]
  66. Martyn C. N., Greenwald S. E. Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertension. Lancet. 1997 Sep 27;350(9082):953–955. doi: 10.1016/s0140-6736(96)10508-0. [DOI] [PubMed] [Google Scholar]
  67. Martyn C. N., Lever A. F., Morton J. J. Plasma concentrations of inactive renin in adult life are related to indicators of foetal growth. J Hypertens. 1996 Jul;14(7):881–886. doi: 10.1097/00004872-199607000-00011. [DOI] [PubMed] [Google Scholar]
  68. Mather H. M., Keen H. The Southall Diabetes Survey: prevalence of known diabetes in Asians and Europeans. Br Med J (Clin Res Ed) 1985 Oct 19;291(6502):1081–1084. doi: 10.1136/bmj.291.6502.1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. McCance D. R., Pettitt D. J., Hanson R. L., Jacobsson L. T., Knowler W. C., Bennett P. H. Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype, or surviving small baby genotype? BMJ. 1994 Apr 9;308(6934):942–945. doi: 10.1136/bmj.308.6934.942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. McCrabb G. J., Egan A. R., Hosking B. J. Maternal undernutrition during mid-pregnancy in sheep. Placental size and its relationship to calcium transfer during late pregnancy. Br J Nutr. 1991 Mar;65(2):157–168. doi: 10.1079/bjn19910077. [DOI] [PubMed] [Google Scholar]
  71. McKeigue P. M., Shah B., Marmot M. G. Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asians. Lancet. 1991 Feb 16;337(8738):382–386. doi: 10.1016/0140-6736(91)91164-p. [DOI] [PubMed] [Google Scholar]
  72. Mitchell B. D., Valdez R., Hazuda H. P., Haffner S. M., Monterrosa A., Stern M. P. Differences in the prevalence of diabetes and impaired glucose tolerance according to maternal or paternal history of diabetes. Diabetes Care. 1993 Sep;16(9):1262–1267. doi: 10.2337/diacare.16.9.1262. [DOI] [PubMed] [Google Scholar]
  73. Moore V. M., Miller A. G., Boulton T. J., Cockington R. A., Craig I. H., Magarey A. M., Robinson J. S. Placental weight, birth measurements, and blood pressure at age 8 years. Arch Dis Child. 1996 Jun;74(6):538–541. doi: 10.1136/adc.74.6.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Murotsuki J., Challis J. R., Han V. K., Fraher L. J., Gagnon R. Chronic fetal placental embolization and hypoxemia cause hypertension and myocardial hypertrophy in fetal sheep. Am J Physiol. 1997 Jan;272(1 Pt 2):R201–R207. doi: 10.1152/ajpregu.1997.272.1.R201. [DOI] [PubMed] [Google Scholar]
  75. Oliver M. H., Harding J. E., Breier B. H., Evans P. C., Gluckman P. D. Glucose but not a mixed amino acid infusion regulates plasma insulin-like growth factor-I concentrations in fetal sheep. Pediatr Res. 1993 Jul;34(1):62–65. doi: 10.1203/00006450-199307000-00015. [DOI] [PubMed] [Google Scholar]
  76. Osmond C., Barker D. J., Winter P. D., Fall C. H., Simmonds S. J. Early growth and death from cardiovascular disease in women. BMJ. 1993 Dec 11;307(6918):1519–1524. doi: 10.1136/bmj.307.6918.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Paneth N., Susser M. Early origin of coronary heart disease (the "Barker hypothesis") BMJ. 1995 Feb 18;310(6977):411–412. doi: 10.1136/bmj.310.6977.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Phillips D. I., Barker D. J. Association between low birthweight and high resting pulse in adult life: is the sympathetic nervous system involved in programming the insulin resistance syndrome? Diabet Med. 1997 Aug;14(8):673–677. doi: 10.1002/(SICI)1096-9136(199708)14:8<673::AID-DIA458>3.0.CO;2-9. [DOI] [PubMed] [Google Scholar]
  79. Phillips D. I., Barker D. J., Hales C. N., Hirst S., Osmond C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994 Feb;37(2):150–154. doi: 10.1007/s001250050086. [DOI] [PubMed] [Google Scholar]
  80. Phillips D. I., Hirst S., Clark P. M., Hales C. N., Osmond C. Fetal growth and insulin secretion in adult life. Diabetologia. 1994 Jun;37(6):592–596. doi: 10.1007/BF00403378. [DOI] [PubMed] [Google Scholar]
  81. Phipps K., Barker D. J., Hales C. N., Fall C. H., Osmond C., Clark P. M. Fetal growth and impaired glucose tolerance in men and women. Diabetologia. 1993 Mar;36(3):225–228. doi: 10.1007/BF00399954. [DOI] [PubMed] [Google Scholar]
  82. Ravelli A. C., van der Meulen J. H., Michels R. P., Osmond C., Barker D. J., Hales C. N., Bleker O. P. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998 Jan 17;351(9097):173–177. doi: 10.1016/s0140-6736(97)07244-9. [DOI] [PubMed] [Google Scholar]
  83. Rich-Edwards J. W., Stampfer M. J., Manson J. E., Rosner B., Hankinson S. E., Colditz G. A., Willett W. C., Hennekens C. H. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ. 1997 Aug 16;315(7105):396–400. doi: 10.1136/bmj.315.7105.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Rizzo G., Arduini D. Fetal cardiac function in intrauterine growth retardation. Am J Obstet Gynecol. 1991 Oct;165(4 Pt 1):876–882. doi: 10.1016/0002-9378(91)90431-p. [DOI] [PubMed] [Google Scholar]
  85. Robinson S. M., Wheeler T., Hayes M. C., Barker D. J., Osmond C. Fetal heart rate and intrauterine growth. Br J Obstet Gynaecol. 1991 Dec;98(12):1223–1227. doi: 10.1111/j.1471-0528.1991.tb15393.x. [DOI] [PubMed] [Google Scholar]
  86. Robinson S., Walton R. J., Clark P. M., Barker D. J., Hales C. N., Osmond C. The relation of fetal growth to plasma glucose in young men. Diabetologia. 1992 May;35(5):444–446. doi: 10.1007/BF02342441. [DOI] [PubMed] [Google Scholar]
  87. Rose G. Sick individuals and sick populations. Int J Epidemiol. 1985 Mar;14(1):32–38. doi: 10.1093/ije/14.1.32. [DOI] [PubMed] [Google Scholar]
  88. Rucker R. B., Dubick M. A. Elastin metabolism and chemistry: potential roles in lung development and structure. Environ Health Perspect. 1984 Apr;55:179–191. doi: 10.1289/ehp.8455179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Rucker R. B., Tinker D. Structure and metabolism of arterial elastin. Int Rev Exp Pathol. 1977;17:1–47. [PubMed] [Google Scholar]
  90. Rudolph A. M. The fetal circulation and its response to stress. J Dev Physiol. 1984 Feb;6(1):11–19. [PubMed] [Google Scholar]
  91. Seckl J. R. Glucocorticoids and small babies. Q J Med. 1994 May;87(5):259–262. [PubMed] [Google Scholar]
  92. Sobey W. J., Beer S. F., Carrington C. A., Clark P. M., Frank B. H., Gray I. P., Luzio S. D., Owens D. R., Schneider A. E., Siddle K. Sensitive and specific two-site immunoradiometric assays for human insulin, proinsulin, 65-66 split and 32-33 split proinsulins. Biochem J. 1989 Jun 1;260(2):535–541. doi: 10.1042/bj2600535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Stein C. E., Fall C. H., Kumaran K., Osmond C., Cox V., Barker D. J. Fetal growth and coronary heart disease in south India. Lancet. 1996 Nov 9;348(9037):1269–1273. doi: 10.1016/s0140-6736(96)04547-3. [DOI] [PubMed] [Google Scholar]
  94. Taylor D. J., Thompson C. H., Kemp G. J., Barnes P. R., Sanderson A. L., Radda G. K., Phillips D. I. A relationship between impaired fetal growth and reduced muscle glycolysis revealed by 31P magnetic resonance spectroscopy. Diabetologia. 1995 Oct;38(10):1205–1212. doi: 10.1007/BF00422370. [DOI] [PubMed] [Google Scholar]
  95. Taylor S. J., Whincup P. H., Cook D. G., Papacosta O., Walker M. Size at birth and blood pressure: cross sectional study in 8-11 year old children. BMJ. 1997 Feb 15;314(7079):475–480. doi: 10.1136/bmj.314.7079.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Temple R. C., Carrington C. A., Luzio S. D., Owens D. R., Schneider A. E., Sobey W. J., Hales C. N. Insulin deficiency in non-insulin-dependent diabetes. Lancet. 1989 Feb 11;1(8633):293–295. doi: 10.1016/s0140-6736(89)91306-8. [DOI] [PubMed] [Google Scholar]
  97. Valdez R., Athens M. A., Thompson G. H., Bradshaw B. S., Stern M. P. Birthweight and adult health outcomes in a biethnic population in the USA. Diabetologia. 1994 Jun;37(6):624–631. doi: 10.1007/BF00403383. [DOI] [PubMed] [Google Scholar]
  98. Veille J. C., Hanson R., Sivakoff M., Hoen H., Ben-Ami M. Fetal cardiac size in normal, intrauterine growth retarded, and diabetic pregnancies. Am J Perinatol. 1993 Jul;10(4):275–279. doi: 10.1055/s-2007-994739. [DOI] [PubMed] [Google Scholar]
  99. Vijayakumar M., Fall C. H., Osmond C., Barker D. J. Birth weight, weight at one year, and left ventricular mass in adult life. Br Heart J. 1995 Apr;73(4):363–367. doi: 10.1136/hrt.73.4.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Weder A. B., Schork N. J. Adaptation, allometry, and hypertension. Hypertension. 1994 Aug;24(2):145–156. doi: 10.1161/01.hyp.24.2.145. [DOI] [PubMed] [Google Scholar]
  101. Whincup P. H., Cook D. G., Adshead F., Taylor S. J., Walker M., Papacosta O., Alberti K. G. Childhood size is more strongly related than size at birth to glucose and insulin levels in 10-11-year-old children. Diabetologia. 1997 Mar;40(3):319–326. doi: 10.1007/s001250050681. [DOI] [PubMed] [Google Scholar]
  102. Whincup P. H., Cook D. G., Shaper A. G. Early influences on blood pressure: a study of children aged 5-7 years. BMJ. 1989 Sep 2;299(6699):587–591. doi: 10.1136/bmj.299.6699.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Whincup P., Cook D., Papacosta O., Walker M. Birth weight and blood pressure: cross sectional and longitudinal relations in childhood. BMJ. 1995 Sep 23;311(7008):773–776. doi: 10.1136/bmj.311.7008.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Whincup P., Cook D., Papacosta O., Walker M., Perry I. Maternal factors and development of cardiovascular risk: evidence from a study of blood pressure in children. J Hum Hypertens. 1994 May;8(5):337–343. [PubMed] [Google Scholar]
  105. Widdowson E. M., McCance R. A. A review: new thoughts on growth. Pediatr Res. 1975 Mar;9(3):154–156. doi: 10.1203/00006450-197503000-00010. [DOI] [PubMed] [Google Scholar]
  106. Wills J., Watson J. M., Hales C. N., Phillips D. I. The relation of fetal growth to insulin secretion in young men. Diabet Med. 1996 Aug;13(8):773–774. doi: 10.1002/(SICI)1096-9136(199608)13:8<773::AID-DIA175>3.0.CO;2-Q. [DOI] [PubMed] [Google Scholar]
  107. Yajnik C. S., Fall C. H., Vaidya U., Pandit A. N., Bavdekar A., Bhat D. S., Osmond C., Hales C. N., Barker D. J. Fetal growth and glucose and insulin metabolism in four-year-old Indian children. Diabet Med. 1995 Apr;12(4):330–336. doi: 10.1111/j.1464-5491.1995.tb00487.x. [DOI] [PubMed] [Google Scholar]
  108. Zureik M., Bonithon-Kopp C., Lecomte E., Siest G., Ducimetiere P. Weights at birth and in early infancy, systolic pressure, and left ventricular structure in subjects aged 8 to 24 years. Hypertension. 1996 Mar;27(3 Pt 1):339–345. doi: 10.1161/01.hyp.27.3.339. [DOI] [PubMed] [Google Scholar]
  109. al-Ghazali W., Chita S. K., Chapman M. G., Allan L. D. Evidence of redistribution of cardiac output in asymmetrical growth retardation. Br J Obstet Gynaecol. 1989 Jun;96(6):697–704. doi: 10.1111/j.1471-0528.1989.tb03285.x. [DOI] [PubMed] [Google Scholar]
  110. van Assche F. A., Aerts L. The fetal endocrine pancreas. Contrib Gynecol Obstet. 1979;5:44–57. [PubMed] [Google Scholar]

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