Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming

Mcmillen, I. Caroline; Robinson, Jeffrey S.

doi:10.1152/physrev.00053.2003

Cited by 1,910Birth, Development, and HealthPrenatal Substance Exposure EffectsPregnancy and preeclampsia studies

Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming

Mcmillen, I. Caroline, Robinson, Jeffrey S.·2005·Physiological Reviews

DOI 10.1152/physrev.00053.2003

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Abstract

The “fetal” or “early” origins of adult disease hypothesis was originally put forward by David Barker and colleagues and stated that environmental factors, particularly nutrition, act in early life to program the risks for adverse health outcomes in adult life. This hypothesis has been supported by a worldwide series of epidemiological studies that have provided evidence for the association between the perturbation of the early nutritional environment and the major risk factors (hypertension, insulin resistance, and obesity) for cardiovascular disease, diabetes, and the metabolic syndrome in adult life. It is also clear from experimental studies that a range of molecular, cellular, metabolic, neuroendocrine, and physiological adaptations to changes in the early nutritional environment result in a permanent alteration of the developmental pattern of cellular proliferation and differentiation in key tissue and organ systems that result in pathological consequences in adult life. This review focuses on those experimental studies that have investigated the critical windows during which perturbations of the intrauterine environment have major effects, the nature of the epigenetic, structural, and functional adaptive responses which result in a permanent programming of cardiovascular and metabolic function, and the role of the interaction between the pre- and postnatal environment in determining final health outcomes.

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Perturbation of gene expression or cell proliferation and differentiation during vulnerable periods by nutritional and other environmental influences can alter the structure and functional capacity of major organ systems for life, a process known as developmental programming.
“Perturbation of gene expression or cell proliferation and differentiation during vulnerable periods by nutritional and other environmental influences can alter the structure and functional capacity of major organ systems for life, a process known as developmental programming.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [374]
The end result of deficient remodeling will be altered development of the fetal organs, as seen in cases of severe maternal undernutrition.
“The end result will be altered development of the fetal organs, as seen in cases of severe maternal undernutrition (215, 374, 565).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [374]

1 retracted

Isocaloric balanced protein supplementation in pregnancy
Kramer, M. S. (1996) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd000118 · Cited by 29 · see citing works
Retracted
Summary of the second report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel II)
Grundy, S. M., Bilheimer, D. W., Chait, A., Clark, L. T., Denke, M. A., Havel, R. J., Hazzard, W. R., Hulley, S. B., Hunninghake, D. B., Kreisberg, R. A., et al. (1993) · JAMA · doi:10.1001/jama.269.23.3015 · Cited by 27,944 · see citing works
Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III)
Expert Panel on Detection, E. (2001) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.285.19.2486 · Cited by 26,011 · see citing works
Role of Insulin Resistance in Human Disease
Reaven, G. M. (1988) · Diabetes · doi:10.2337/diab.37.12.1595 · Cited by 12,154 · see citing works
Prevalence and trends in obesity among US adults, 1999–2000
Flegal, K. M. (2002) · JAMA · doi:10.1001/jama.288.14.1723 · Cited by 6,190 · see citing works
Leptin and the regulation of body weight in mammals
Friedman, J. M., & Halaas, J. L. (1998) · Nature · doi:10.1038/27376 · Cited by 5,405 · see citing works
Prevalence and Trends in Overweight Among US Children and Adolescents, 1999-2000
Ogden, C. L. (2002) · JAMA · doi:10.1001/jama.288.14.1728 · Cited by 4,060 · see citing works
Banting lecture 1988. Role of insulin resistance in human disease.
Reaven, G. (1988) · Diabetes · doi:10.2337/diabetes.37.12.1595 · Cited by 3,801 · see citing works
WEIGHT IN INFANCY AND DEATH FROM ISCHAEMIC HEART DISEASE
Barker, D. J. P., Osmond, C., Winter, P. D., Margetts, B., & Simmonds, S. J. (1989) · The Lancet · doi:10.1016/s0140-6736(89)90710-1 · Cited by 3,574 · see citing works
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. P. (1992) · Diabetologia · doi:10.1007/bf00400248 · Cited by 3,294 · see citing works
Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?
Neel, J. V. (1962) · Europe PMC (PubMed Central) · Cited by 3,147 · see citing works
INFANT MORTALITY, CHILDHOOD NUTRITION, AND ISCHAEMIC HEART DISEASE IN ENGLAND AND WALES
BARKER, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)91340-1 · Cited by 2,892 · see citing works
The thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. (2001) · British Medical Bulletin · doi:10.1093/bmb/60.1.5 · Cited by 2,749 · see citing works
Fetal and infant growth and impaired glucose tolerance at age 64
Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., & Winter, P. D. (1991) · BMJ · doi:10.1136/bmj.303.6809.1019 · Cited by 2,708 · see citing works
Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth
Barker, D. J. P., Hales, C. N., Fall, C. H. D., Osmond, C., Phipps, K., & Clark, P. M. S. (1993) · Diabetologia · doi:10.1007/bf00399095 · Cited by 2,468 · see citing works
Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease.
Barker, D. J., Osmond, C., Golding, J., Kuh, D., & Wadsworth, M. E. (1989) · BMJ · doi:10.1136/bmj.298.6673.564 · Cited by 2,415 · see citing works
Genomic imprinting: parental influence on the genome
Reik, W., & Walter, J. (2001) · Nature Reviews Genetics · doi:10.1038/35047554 · Cited by 2,288 · see citing works
Fetal origins of adult disease: strength of effects and biological basis
Barker, D., Eriksson, J., Forsén, T., & Osmond, C. (2002) · International Journal of Epidemiology · doi:10.1093/ije/31.6.1235 · Cited by 2,024 · see citing works
Transposable elements: targets for early nutritional effects on epigenetic gene regulation
Waterland, R. A., & Jirtle, R. L. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.15.5293-5300.2003 · Cited by 2,019 · see citing works
Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1
Yoon, J. C., Puigserver, P., Chen, G., Donovan, J., Wu, Z., Rhee, J., Adelmant, G., Stafford, J., Kahn, C. R., Granner, D. K., et al. (2001) · Nature · doi:10.1038/35093050 · Cited by 1,821 · see citing works
Developmental plasticity and human health
Bateson, P., Barker, D., Clutton-Brock, T., Deb, D., D'Udine, B., Foley, R. A., Gluckman, P., Godfrey, K., Kirkwood, T., Lahr, M. M., et al. (2004) · Nature · doi:10.1038/nature02725 · Cited by 1,742 · see citing works
Fetal and placental size and risk of hypertension in adult life.
Barker, D. J., Bull, A. R., Osmond, C., & Simmonds, S. J. (1990) · BMJ · doi:10.1136/bmj.301.6746.259 · Cited by 1,728 · see citing works
Early development and fitness in birds and mammals
Lindström, J., & Lindström, J. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(99)01639-0 · Cited by 1,706 · see citing works
Association between postnatal catch-up growth and obesity in childhood: prospective cohort study
Ong, K. K. (2000) · BMJ · doi:10.1136/bmj.320.7240.967 · Cited by 1,659 · see citing works
Obesity in Young Men after Famine Exposure in Utero and Early Infancy
Ravelli, G.-P., Stein, Z. A., & Susser, M. W. (1976) · New England Journal of Medicine · doi:10.1056/nejm197608122950701 · Cited by 1,647 · see citing works
Mutations in the hepatocyte nuclear factor-1α gene in maturity-onset diabetes of the young (MODY3)
Yamagata, K., Oda, N., Kaisaki, P. J., Menzel, S., Furuta, H., Vaxillaire, M., Southam, L., Cox, R., Lathrop, M. G., Boriraj, V. V., et al. (1996) · Nature · doi:10.1038/384455a0 · Cited by 1,610 · see citing works
Adipose Tissue as an Endocrine Organ
Ahima, R. S., & Flier, J. S. (2000) · Trends in Endocrinology & Metabolism · doi:10.1016/s1043-2760(00)00301-5 · Cited by 1,608 · see citing works
Glucose tolerance in adults after prenatal exposure to famine
Ravelli, A., van der Meulen, J., Michels, R., Osmond, C., Barker, D., Hales, C., & Bleker, O. (1998) · The Lancet · doi:10.1016/s0140-6736(97)07244-9 · Cited by 1,606 · see citing works
COMPARISON OF THE EFFECTS OF UNILATERAL AND BILATERAL EYE CLOSURE ON CORTICAL UNIT RESPONSES IN KITTENS
Wiesel, T. N., & Hubel, D. H. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.6.1029 · Cited by 1,598 · see citing works
Glomeruli and Blood Pressure: Less of One, More the Other?
Brenner, B. M., Garcia, D. L., & Anderson, S. (1988) · American Journal of Hypertension · doi:10.1093/ajh/1.4.335 · Cited by 1,313 · see citing works
Nonadipose tissue production of leptin: Leptin as a novel placenta-derived hormone in humans
Masuzaki, H., Ogawa, Y., Sagawa, N., Hosoda, K., Matsumoto, T., Mise, H., Nishimura, H., Yoshimasa, Y., Tanaka, I., Mori, T., et al. (1997) · Nature Medicine · doi:10.1038/nm0997-1029 · Cited by 1,277 · see citing works
Catch-up growth in childhood and death from coronary heart disease: longitudinal study
Eriksson, J. G., Forsén, T., Tuomilehto, J. O., Winter, P. D., Osmond, C., & Barker, D. J. P. (1999) · Ambulatory Child Health · doi:10.1136/bmj.318.7181.427 · Cited by 1,144 · see citing works
Perinatal outcome of singletons and twins after assisted conception: a systematic review of controlled studies
Helmerhorst, F. M. (2004) · BMJ · doi:10.1136/bmj.37957.560278.ee · Cited by 1,123 · see citing works
Maternal epigenetics and methyl supplements affect agouti gene expression in A vy /a mice
Wolff, G. L., Kodell, R. L., Moore, S. R., & Cooney, C. A. (1998) · The FASEB Journal · doi:10.1096/fasebj.12.11.949 · Cited by 1,057 · see citing works
The role of size at birth and postnatal catch-up growth in determining systolic blood pressure
Huxley, R., Shiell, A. W., & Law, C. (2000) · Journal of Hypertension · doi:10.1097/00004872-200018070-00002 · Cited by 1,046 · see citing works
Variations in maternal care in the rat as a mediating influence for the effects of environment on development
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works
Early growth and coronary heart disease in later life: longitudinal study
Eriksson, J. G., Forsén, T., Tuomilehto, J., Osmond, C., & Barker, D. J. P. (2001) · BMJ · doi:10.1136/bmj.322.7292.949 · Cited by 1,004 · see citing works
Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition
Vickers, M. H., Breier, B. H., Cutfield, W. S., Hofman, P. L., & Gluckman, P. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.1.e83 · Cited by 999 · see citing works
Mutations in the hepatocyte nuclear factor-4α gene in maturity-onset diabetes of the young (MODY1)
Yamagata, K., Furuta, H., Oda, N., Kaisaki, P. J., Menzel, S., Cox, N. J., Fajans, S. S., Signorini, S. G., Stoffel, M., & Bell, G. I. (1996) · Nature · doi:10.1038/384458a0 · Cited by 975 · see citing works
Cellular Response in Rats during Malnutrition at Various Ages
Winick, M., & Noble, A. (1966) · Journal of Nutrition · doi:10.1093/jn/89.3.300 · Cited by 959 · see citing works
Birth Weight and Adult Hypertension, Diabetes Mellitus, and Obesity in US Men
Curhan, G. C., Willett, W. C., Rimm, E. B., Spiegelman, D. L., Ascherio, A., & Stampfer, M. J. (1996) · Circulation · doi:10.1161/01.cir.94.12.3246 · Cited by 917 · see citing works
Programming by Early Nutrition in Man
Lucas, A. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514047.ch4 · Cited by 914 · see citing works
The fetal insulin hypothesis: an alternative explanation of the association of low bir thweight with diabetes and vascular disease
Hattersley, A. T., & Tooke, J. E. (1999) · The Lancet · doi:10.1016/s0140-6736(98)07546-1 · Cited by 909 · see citing works
Glucocorticoid exposure in utero: new model for adult hypertension
Benediktsson, R., Lindsay, R. S., Noble, J., Seckl, J. R., & Edwards, C. R. W. (1993) · The Lancet · doi:10.1016/0140-6736(93)90138-7 · Cited by 862 · see citing works
Rapid Transition of Cardiac Myocytes from Hyperplasia to Hypertrophy During Postnatal Development
Li, F. (1996) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1996.0163 · Cited by 837 · see citing works
Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture
Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutiérrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., & Sinclair, K. D. (2001) · Nature Genetics · doi:10.1038/84769 · Cited by 830 · see citing works
Self-citation
Early growth and death from cardiovascular disease in women.
Osmond, C., BARKER, D. J. P., Winter, P. D., Fall, C. H. D., & Simmonds, S. J. (1993) · BMJ · doi:10.1136/bmj.307.6918.1519 · Cited by 822 · see citing works
Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976
Rich-Edwards, J. W., Stampfer, M. J., Manson, J. E., ROSNER, B. A., Hankinson, S. E., Colditz, G. A., Hennekens, C. H., & Willett, W. C. (1997) · BMJ · doi:10.1136/bmj.315.7105.396 · Cited by 814 · see citing works
Fetal origins of adult disease---the hypothesis revisited
Lucas, A., Fewtrell, M. S., & Cole, T. J. (1999) · BMJ · doi:10.1136/bmj.319.7204.245 · Cited by 798 · see citing works
Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension
Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., & Fleming, T. P. (2000) · Development · doi:10.1242/dev.127.19.4195 · Cited by 798 · see citing works
Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases
Waterland, R. A., & Jirtle, R. L. (2003) · Nutrition · doi:10.1016/j.nut.2003.09.011 · Cited by 783 · see citing works
Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, Angiopoietins, and ephrins in vascular developmentPreprint
Gale, N. W., & Yancopoulos, G. D. (1999) · Genes & Development · doi:10.1101/gad.13.9.1055 · Cited by 776 · see citing works
Glomerular number and size in autopsy kidneys: The relationship to birth weight
Hughson, M. D., Farris, A. B., Douglas-Denton, R. N., Hoy, W. E., & Bertram, J. F. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.00018.x · Cited by 754 · see citing works
Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease?
Forsdahl, A. (1977) · Journal of Epidemiology & Community Health · doi:10.1136/jech.31.2.91 · Cited by 747 · see citing works
Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature
Law, C., & Shiell, A. W. (1996) · Journal of Hypertension · doi:10.1097/00004872-199608000-00002 · Cited by 733 · see citing works
Cardiomyocyte DNA synthesis and binucleation during murine development
Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. T., & Field, L. J. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.5.h2183 · Cited by 718 · see citing works
Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure?
Huxley, R., Neil, A., & Collins, R. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09834-3 · Cited by 710 · see citing works
EXTENT OF RECOVERY FROM THE EFFECTS OF VISUAL DEPRIVATION IN KITTENS
Wiesel, T. N., & Hubel, D. H. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.6.1060 · Cited by 704 · see citing works
Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype, or surviving small baby genotype?
McCance, D. R., Pettitt, D. J., Hanson, R. L., Jacobsson, L., Knowler, W. C., & Bennett, P. H. (1994) · BMJ · doi:10.1136/bmj.308.6934.942 · Cited by 693 · see citing works
Increased Systolic Blood Pressure in Adult Rats Induced by Fetal Exposure to Maternal Low Protein Diets
Langley‐Evans, S. C., & Jackson, A. A. (1994) · Clinical Science · doi:10.1042/cs0860217 · Cited by 688 · see citing works
Birth Weight and Adult Hypertension and Obesity in Women
Curhan, G. C., Chertow, G. M., Willett, W. C., Spiegelman, D. L., Colditz, G. A., Manson, J. E., Speizer, F. E., & Stampfer, M. J. (1996) · Circulation · doi:10.1161/01.cir.94.6.1310 · Cited by 671 · see citing works
Effect of a Low Protein Diet during Pregnancy on the Fetal Rat Endocrine Pancreas
Snoeck, A., Remacle, C., Reusens, B., & Hoet, J. J. (2009) · Biology of the Neonate · doi:10.1159/000243170 · Cited by 652 · see citing works
Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8 years, or both?
Bavdekar, A., Yajnik, C. S., Fall, C. H. D., Bapat, S. A., Pandit, A. N., Deshpande, V., Bhave, S., Kellingray, S., & Joglekar, C. V. (1999) · Diabetes · doi:10.2337/diabetes.48.12.2422 · Cited by 652 · see citing works
The use of the glycemie Index in predicting the blood glucose response to mixed meals
Wolever, T., & Jenkins, D. (1986) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/43.1.167 · Cited by 645 · see citing works
Initiation of hypertension in utero and its amplification throughout life.
Law, C., de Swiet, M., Osmond, C., Fayers, P. M., Barker, D. J., Cruddas, A. M., & Fall, C. H. D. (1993) · BMJ · doi:10.1136/bmj.306.6869.24 · Cited by 643 · see citing works
The developmental origins of the metabolic syndrome
Gluckman, P. D., & Hanson, M. A. (2004) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2004.03.002 · Cited by 638 · see citing works
Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat
Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2279 · Cited by 638 · see citing works
International Small for Gestational Age Advisory Board Consensus Development Conference Statement: Management of Short Children Born Small for Gestational Age, April 24–October 1, 2001
Lee, P. A., Chernausek, S. D., Hokken-Koelega, A. C. S., Czernichow, P., & for the International SGA Advisory Board (2003) · Pediatrics · doi:10.1542/peds.111.6.1253 · Cited by 613 · see citing works
Maternal Cigarette Smoking, Metabolic Gene Polymorphism, and Infant Birth Weight
Wang, X. (2002) · JAMA · doi:10.1001/jama.287.2.195 · Cited by 612 · see citing works
Fetal growth and coronary heart disease in South India
Stein, C., Fall, C., Kumaran, K., Osmond, C., Barker, D. J. P., & Cox, V. (1996) · The Lancet · doi:10.1016/s0140-6736(96)04547-3 · Cited by 607 · see citing works
Dynamics of β-cell Mass in the Growing Rat Pancreas: Estimation With a Simple Mathematical Model
Finegood, D. T., Scaglia, L., & Bonner‐Weir, S. (1995) · Diabetes · doi:10.2337/diab.44.3.249 · Cited by 604 · see citing works
Maternal nutrition in early and late pregnancy in relation to placental and fetal growth
Godfrey, K., Robinson, S., Barker, D., Osmond, C., & Cox, V (1996) · BMJ · doi:10.1136/bmj.312.7028.410 · Cited by 604 · see citing works
Nonsense mutation in the glucokinase gene causes early-onset non-insulin-dependent diabetes mellitus
Vionnet, N., Stoffel, M., Takeda, J., Yasuda, K., Bell, G. I., Zouali, H., Lesage, S., Velho, G., Iris, F., Passa, P., et al. (1992) · Nature · doi:10.1038/356721a0 · Cited by 604 · see citing works
Congenital Oligonephropathy and the Etiology of Adult Hypertension and Progressive Renal Injury
Brenner, B. M., & Chertow, G. M. (1994) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(12)80967-x · Cited by 602 · see citing works
Elevated Plasma Cortisol Concentrations: A Link between Low Birth Weight and the Insulin Resistance Syndrome?1
Phillips, D. I. W., Barker, D. J. P., Fall, C. H. D., Seckl, J. R., Whorwood, C. B., Wood, P. J., & Walker, B. R. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.3.4634 · Cited by 602 · see citing works
Relationship between weight at birth and the number and size of renal glomeruli in humans: A histomorphometric study
Mañalich, R., Reyes, L., Herrera, M., Melendi, C., & Mayor, I. F. (2000) · Kidney International · doi:10.1046/j.1523-1755.2000.00225.x · Cited by 599 · see citing works
Low nutrient intake and early growth for later insulin resistance in adolescents born preterm
Singhal, A., Fewtrell, M. S., Cole, T. J., & Lucas, A. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12895-4 · Cited by 594 · see citing works
Mutations in the glucokinase gene of the fetus result in reduced birth weight
Hattersley, A. T., Beards, F., Ballantyne, E., Appleton, M., Harvey, R., & Ellard, S. (1998) · Nature Genetics · doi:10.1038/953 · Cited by 592 · see citing works
Maternal Protein Restriction Suppresses the Newborn Renin-Angiotensin System and Programs Adult Hypertension in Rats
Woods, L. L., Ingelfinger, J. R., Nyengaard, J. R., & Rasch, R. (2001) · Pediatric Research · doi:10.1203/00006450-200104000-00005 · Cited by 583 · see citing works
Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring.
Nyirenda, M., Lindsay, R. S., Kenyon, C. J., Burchell, A. N., & Seckl, J. R. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1567 · Cited by 574 · see citing works
The effect of intrauterine growth retardation on the development of renal nephrons
Hinchliffe, S. A., Lynch, M. R. J., Sargent, P. H., Howard, C. V., & van Velzen, D. (1992) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1992.tb13726.x · Cited by 571 · see citing works
Potential mechanisms of metabolic imprinting that lead to chronic disease
Waterland, R. A., & Garza, C. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.2.179 · Cited by 565 · see citing works
The nutritional basis of the fetal origins of adult disease
Harding, J. E. (2001) · International Journal of Epidemiology · doi:10.1093/ije/30.1.15 · Cited by 561 · see citing works
Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension?
Edwards, C. R. W., Benediktsson, R., Lindsay, R. S., & Seckl, J. R. (1993) · The Lancet · doi:10.1016/0140-6736(93)90148-a · Cited by 549 · see citing works
Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat
Langley‐Evans, S. C., Welham, S. J. M., & Jackson, A. A. (1999) · Life Sciences · doi:10.1016/s0024-3205(99)00022-3 · Cited by 547 · see citing works
Birthweight and the Risk for Type 2 Diabetes Mellitus in Adult Women
Rich-Edwards, J. W., Colditz, G. A., Stampfer, M. J., Willett, W. C., Gillman, M. W., Hennekens, C. H., Speizer, F. E., & Manson, J. E. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-130-4_part_1-199902160-00005 · Cited by 544 · see citing works
Dexamethasone in the Last Week of Pregnancy Attenuates Hippocampal Glucocorticoid Receptor Gene Expression and Elevates Blood Pressure in the Adult Offspring in the Rat
Levitt, N. S., Lindsay, R. S., Holmes, M. C., & Seckl, J. R. (2008) · Neuroendocrinology · doi:10.1159/000127146 · Cited by 535 · see citing works
Expression of the Functional Leptin Receptor mRNA in Pancreatic Islets and Direct Inhibitory Action of Leptin on Insulin Secretion
Emilsson, V., Liu, Y.-L., Cawthorne, M. A., Morton, N. M., & Davenport, M. (1997) · Diabetes · doi:10.2337/diab.46.2.313 · Cited by 532 · see citing works
Early programming of the hypothalamo–pituitary–adrenal axis
MATTHEWS, S. (2002) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00690-2 · Cited by 513 · see citing works
Birthweight, body-mass index in middle age, and incident coronary heart disease
Frankel, S., Elwood, P. C., Smith, G. D., Sweetnam, P. M., & Yarnell, J. (1996) · The Lancet · doi:10.1016/s0140-6736(96)03482-4 · Cited by 507 · see citing works
Fetal growth and impaired glucose tolerance in men and women
Phipps, K. P., Barker, D. J. P., Hales, C. N., Fall, C. H. D., Osmond, C., & Clark, P. M. (1993) · Diabetologia · doi:10.1007/bf00399954 · Cited by 490 · see citing works
Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study
Forsen, T., Eriksson, J. G., Tuomilehto, J., Osmond, C., & Barker, D. J. P. (1999) · BMJ · doi:10.1136/bmj.319.7222.1403 · Cited by 481 · see citing works
Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: longitudinal study
Parsons, T. J., Power, C., & Manor, O. (2001) · BMJ · doi:10.1136/bmj.323.7325.1331 · Cited by 472 · see citing works
Fetal and infant growth and cardiovascular risk factors in women
Fall, C. H. D., Osmond, C., Barker, D. J., Clark, P. M., Hales, C. N., Stirling, Y., & Meade, T. W. (1995) · BMJ · doi:10.1136/bmj.310.6977.428 · Cited by 461 · see citing works
Diabetes mellitus · A
Cerasi, E., Dieterlé, P., Ege, H., Englhardt, A., Frerichs, H., Gepts, W., Hasselblatt, A., Henrichs, H. R., Herberg, L., Hoet, J., et al. (1975) · Springer eBooks · doi:10.1007/978-3-642-66033-7 · Cited by 456 · see citing works
Developmental origins of adult health and disease
Barker, D. J. P. (2004) · Journal of Epidemiology & Community Health · doi:10.1136/jech.58.2.114 · Cited by 454 · see citing works
Mother's weight in pregnancy and coronary heart disease in a cohort of finnish men: follow up study
Forsén, T., Eriksson, J. G., Tuomilehto, J. O., Teramo, K., Osmond, C., & Barker, D. J. P. (1997) · BMJ · doi:10.1136/bmj.315.7112.837 · Cited by 452 · see citing works
Long-term prospective evaluation of offspring of diabetic mothers
Silverman, B. L., Rizzo, T., Green, O. C., Cho, N. H., Winter, R. J., Ogata, E. S., Richards, G. E., & Metzger, B. E. (1991) · Diabetes · doi:10.2337/diab.40.2.s121 · Cited by 452 · see citing works
Islet Function in Offspring of Mothers on Low-Protein Diet During Gestation
Dahri, S., Snoeck, A., Reusens-Billen, B., Remacle, C., & Hote, J. J. (1991) · Diabetes · doi:10.2337/diab.40.2.s115 · Cited by 445 · see citing works
Insulin Sensitivity and Secretion Are Related to Catch-Up Growth in Small-for-Gestational-Age Infants at Age 1 Year: Results from a Prospective Cohort
Néstor Soto, I., Bazaes, R. A., Peña, V., Salazar, T., Ávila, A., Íñiguez, G., Ong, K. K., Dunger, D. B., & Verónica Mericq, G. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-030031 · Cited by 436 · see citing works
Catch-up Growth
Boersma, B., & Wit, J. M. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.5.0313 · Cited by 434 · see citing works
Energy and protein intake in pregnancy
Kramer, M. S., & Kakuma, R. (2003) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd000032 · Cited by 431 · see citing works
Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor
Coles, H., Burne, J. F., & RAFF, M. C. (1993) · Development · doi:10.1242/dev.118.3.777 · Cited by 426 · see citing works
Early growth and abdominal fatness in adult life.
Law, C., Barker, D. J. P., Osmond, C., Fall, C. H. D., & Simmonds, S. J. (1992) · Journal of Epidemiology & Community Health · doi:10.1136/jech.46.3.184 · Cited by 424 · see citing works
Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour
Welberg, L., Seckl, J. R., & Holmes, M. C. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00065-3 · Cited by 420 · see citing works
The adipoinsular axis: effects of leptin on pancreatic β-cells
Kieffer, T. J., & Habener, J. F. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.1.e1 · Cited by 418 · see citing works
Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat
Langley‐Evans, S. C., Phillips, G. J., Benediktsson, R., Gardner, D. S., Edwards, C. R. W., Jackson, A. A., & Seckl, J. R. (1996) · Placenta · doi:10.1016/s0143-4004(96)80010-5 · Cited by 415 · see citing works
Effects on birth weight and perinatal mortality of maternal dietary supplements in rural gambia: 5 year randomised controlled trial
CEESAY, S. M., Prentice, A. M., Cole, T. J., Foord, F., Poskitt, E. M. E., Weaver, L. T., & Whitehead, R. G. (1997) · BMJ · doi:10.1136/bmj.315.7111.786 · Cited by 398 · see citing works
Prenatal programming of adult hypertension in the rat
Vehaskari, V. M., Avilés, D., & Manning, J. M. (2001) · Kidney International · doi:10.1046/j.1523-1755.2001.00484.x · Cited by 396 · see citing works
EVIDENCE THAT THE HYPOTHALAMUS IS RESPONSIBLE FOR ANDROGEN-INDUCED STERILITY IN THE FEMALE RAT1
Barraclough, C. A., & Gorski, R. A. (1961) · Endocrinology · doi:10.1210/endo-68-1-68 · Cited by 391 · see citing works
Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype
Topper, J. N., & Gimbrone, M. A. (1999) · Molecular Medicine Today · doi:10.1016/s1357-4310(98)01372-0 · Cited by 390 · see citing works
Low Birth Weight Predicts Elevated Plasma Cortisol Concentrations in Adults From 3 Populations
Phillips, D. I. W., Walker, B. R., Reynolds, R. M., Flanagan, D., Wood, P. J., Osmond, C., Barker, D. J. P., & Whorwood, C. B. (2000) · Hypertension · doi:10.1161/01.hyp.35.6.1301 · Cited by 389 · see citing works
The Maternal Diet during Pregnancy Programs Altered Expression of the Glucocorticoid Receptor and Type 2 11 -Hydroxysteroid Dehydrogenase: Potential Molecular Mechanisms Underlying the Programming of Hypertension in Utero
Bertram, C. E., Trowern, A. R., Copin, N., Jackson, A. A., & Whorwood, C. B. (2001) · Endocrinology · doi:10.1210/endo.142.7.8238 · Cited by 385 · see citing works
Mothers' pelvic size, fetal growth, and death from stroke and coronary heart disease in men in the UK
Martyn, C., Barker, D., & Osmond, C. (1996) · The Lancet · doi:10.1016/s0140-6736(96)04257-2 · Cited by 381 · see citing works
Maternal Undernutrition during Late Gestation Induces Fetal Overexposure to Glucocorticoids and Intrauterine Growth Retardation, and Disturbs the Hypothalamo-Pituitary Adrenal Axis in the Newborn Rat1
Lésage, J., Blondeau, B., Grino, M., Bréant, B., & Dupouy, J. (2001) · Endocrinology · doi:10.1210/endo.142.5.8139 · Cited by 380 · see citing works
Impact of Low Birth Weight and Cardiovascular Risk Factors on Endothelial Function in Early Adult Life
Leeson, C. P. M., Kattenhorn, M., Morley, R., Lucas, A., & Deanfield, J. E. (2001) · Circulation · doi:10.1161/01.cir.103.9.1264 · Cited by 379 · see citing works
Chronic Maternal Undernutrition in the Rat Leads to Delayed Postnatal Growth and Elevated Blood Pressure of Offspring
Woodall, S., Johnston, B. M., Breier, B. H., & Gluckman, P. D. (1996) · Pediatric Research · doi:10.1203/00006450-199609000-00012 · Cited by 372 · see citing works
Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease?
Singhal, A., Wells, J. C. K., Cole, T. J., Fewtrell, M. S., & Lucas, A. (2003) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/77.3.726 · Cited by 372 · see citing works
Experimental growth retardation in the foetal rat
Wigglesworth, J. S. (1964) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700880102 · Cited by 372 · see citing works
Temperature of egg incubation determines sex in Alligator mississippiensis
Ferguson, M. W. J., & Joanen, T. (1982) · Nature · doi:10.1038/296850a0 · Cited by 371 · see citing works
Organ-selective growth in the offspring of protein-restricted mothers
Desai, M., Crowther, N. J., Lucas, A., & Hales, C. N. (1996) · British Journal Of Nutrition · doi:10.1079/bjn19960065 · Cited by 367 · see citing works
Gender-linked hypertension in offspring of lard-fed pregnant rats
Khan, I. Y., Taylor, P. D., Dekou, V., Seed, P. T., Lakasing, L., Graham, D., Dominiczak, A. F., Hanson, M. A., & Poston, L. (2003) · Hypertension · doi:10.1161/01.hyp.0000047511.97879.fc · Cited by 365 · see citing works
DEATH-RATES IN GREAT BRITAIN AND SWEDEN SOME GENERAL REGULARITIES AND THEIR SIGNIFICANCE
Kermack, W. O., McKendrick, A. G., & Mckinlay, P. L. (1934) · The Lancet · doi:10.1016/s0140-6736(00)92530-3 · Cited by 356 · see citing works
Intrauterine growth retardation leads to a permanent nephron deficit in the rat
Merlet-Bénichou, C., Gilbert, T., Muffat‐Joly, M., Leli�vre-P�gorier, M., & Leroy, B. (1994) · Pediatric Nephrology · doi:10.1007/bf00865473 · Cited by 351 · see citing works
Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition
Vickers, M. H., Breier, B. H., McCarthy, D., & Gluckman, P. D. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00051.2003 · Cited by 346 · see citing works
Elevated Plasma Cortisol Concentrations: A Link between Low Birth Weight and the Insulin Resistance Syndrome?
Phillips, D. I. W. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.3.757 · Cited by 343 · see citing works
Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals
Eriksson, J. G., Forsén, T., Tuomilehto, J. O., Jaddoe, V. W. V., Osmond, C., & Barker, D. J. (2002) · Diabetologia · doi:10.1007/s00125-001-0757-6 · Cited by 341 · see citing works
A Low Protein Diet Alters the Balance of Islet Cell Replication and Apoptosis in the Fetal and Neonatal Rat and Is Associated with a Reduced Pancreatic Expression of Insulin-Like Growth Factor-II1
Petrik, J., Reusens, B., Arany, E. J., Remacle, C., Coelho, C., Hoet, J., & Hill, D. J. (1999) · Endocrinology · doi:10.1210/endo.140.10.7042 · Cited by 337 · see citing works
Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome X-like alterations in adulthood of neonatally overfed rats
Plagemann, A., Harder, T., Rake, A., Voits, M., Fink, H., Rohde, W., & Dörner, G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01662-5 · Cited by 331 · see citing works
The "thrifty genotype" in 1998.
Neel, J. V. (2009) · Nutrition reviews · doi:10.1111/j.1753-4887.1999.tb01782.x · Cited by 330 · see citing works
Fetal environment and subsequent obesity: a study of maternal smoking
Power, C., & Jefferis, B. J. (2002) · International Journal of Epidemiology · doi:10.1093/ije/31.2.413 · Cited by 330 · see citing works
Leptin Receptors Expressed on Pancreatic β-Cells
Kieffer, T. J., Heller, R. S., & Habener, J. F. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1059 · Cited by 326 · see citing works
An Early Prenatal Exposure to Excess Glucocorticoid Leads to Hypertensive Offspring in Sheep
Dodic, M., May, C. N., Wintour, E. M., & Coghlan, J. P. (1998) · Clinical Science · doi:10.1042/cs0940149 · Cited by 324 · see citing works
Dietary restriction in pregnant rats causes gender‐related hypertension and vascular dysfunction in offspring
Ozaki, T., Nishina, H., Hanson, M. A., & Poston, L. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0141m.x · Cited by 321 · see citing works
In utero undernutrition impairs rat beta-cell development
Garofano, A., Czernichow, P., & Bréant, B. (1997) · Diabetologia · doi:10.1007/s001250050812 · Cited by 320 · see citing works
Early programming of glucose–insulin metabolism
Ozanne, S. E., & Hales, C. N. (2002) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00666-5 · Cited by 316 · see citing works
Nestlé Nutrition workshop series
Nutrition, N. (1983) · Raven Press eBooks · Cited by 314 · see citing works
Inhibition of 11β-Hydroxysteroid Dehydrogenase in Pregnant Rats and the Programming of Blood Pressure in the Offspring
Lindsay, R. S., Lindsay, R. M., Edwards, C. R. W., & Seckl, J. R. (1996) · Hypertension · doi:10.1161/01.hyp.27.6.1200 · Cited by 310 · see citing works
Apoptosis in metanephric development.
Koseki, C., HERZLINGER, D. A., & Al‐Awqati, Q. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.5.1327 · Cited by 307 · see citing works
Phylogeny and ontogeny of hormone receptors: the selection theory of receptor formation and hormonal imprinting
CSABA, G. (1980) · Biological Reviews · doi:10.1111/j.1469-185x.1980.tb00687.x · Cited by 305 · see citing works
Fishing in the Stream of Diabetes: From Measuring Insulin to the Control of Fetal Organogenesis
Hales, C. N., Desai, M., Ozanne, S. E., & Crowther, N. J. (1996) · Biochemical Society Transactions · doi:10.1042/bst0240341 · Cited by 299 · see citing works
Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs
Poulsen, P., Vaag, A. A., Kyvik, K. O., Jensen, D. M., & Beck‐Nielsen, H. (1997) · Diabetologia · doi:10.1007/s001250050698 · Cited by 295 · see citing works
Impaired Endothelial Function and Increased Carotid Stiffness in 9-Year-Old Children With Low Birthweight
Martin, H., Hu, J., Gennser, G. M., & Norman, M. (2000) · Circulation · doi:10.1161/01.cir.102.22.2739 · Cited by 295 · see citing works
Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice.
Krzysztof Reiss, F., Cheng, W. N., Ferbér, A., Kajstura, J., Li, P., Li, B., Olivetti, G., Homcy, C. J., Baserga, R., & Anversa, P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8630 · Cited by 292 · see citing works
Nephron mass as a risk factor for progression of renal disease.
Brenner, B. M., & Mackenzie, H. S. (1997) · PubMed · Cited by 287 · see citing works
NO EVIDENCE OF ACCELERATED LOSS OF KIDNEY FUNCTION IN LIVING KIDNEY DONORS: RESULTS FROM A CROSS-SECTIONAL FOLLOW-UP1
Fehrman‐Ekholm, I., r, F. D., Brink, B., Tyd�n, G., & Elinder, C. (2001) · Transplantation · doi:10.1097/00007890-200108150-00015 · Cited by 280 · see citing works
Australian national birthweight percentiles by gestational age
Roberts, C. L., & Lancaster, P. A. L. (1999) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1999.tb127678.x · Cited by 280 · see citing works
Leptin Suppression of Insulin Secretion and Gene Expression in Human Pancreatic Islets: Implications for the Development of Adipogenic Diabetes Mellitus1
Seufert, J., Kieffer, T. J., Leech, C. A., Holz, G. G., Moritz, W., Ricordi, C., & Habener, J. F. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5460 · Cited by 278 · see citing works
Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney
Pham, T. D., MacLennan, N. K., Chiu, C. T., Laksana, G. S., Hsu, J. L., & Lane, R. H. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00201.2003 · Cited by 278 · see citing works
Mortality among twins after age 6: fetal origins hypothesis versus twin method
Christensen, K., Vaupel, J. W., Holm, N. V., & Yashin, A. I. (1995) · BMJ · doi:10.1136/bmj.310.6977.432 · Cited by 277 · see citing works
Ontogeny of Leptin in Human Fetuses and Newborns: Effect of Intrauterine Growth Retardation on Serum Leptin Concentrations
Jaquet, D., Léger, J., Lévy‐Marchal, C., Oury, J., & Czernichow, P. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.4.4731 · Cited by 275 · see citing works
A Randomized Controlled Trial of Prenatal Nutritional Supplementation in New York City
Rush, D., STEIN, Z. A., & Susser, M. W. (1980) · PEDIATRICS · doi:10.1542/peds.65.4.683 · Cited by 274 · see citing works
Perinatal Hyperinsulinism as Possible Predisposing Factor for Diabetes Mellitus, Obesity and Enhanced Cardiovascular Risk in Later Life
Dörner, G., & Plagemann, A. (1994) · Hormone and Metabolic Research · doi:10.1055/s-2007-1001668 · Cited by 274 · see citing works
Impaired Glucose Tolerance and Elevated Blood Pressure in Low Birth Weight, Nonobese, Young South African Adults: Early Programming of Cortisol Axis1
Levitt, N. S., Lambert, E. V., Woods, D., Hales, C. N., Andrew, R., & Seckl, J. R. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.12.7039 · Cited by 272 · see citing works
Review lecture - The determinants of growth and form
McCance, R. A., & Widdowson, E. M. (1974) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1974.0001 · Cited by 272 · see citing works
A Periconceptional Nutritional Origin for Noninfectious Preterm Birth
Bloomfield, F. H., Oliver, M. H., Hawkins, P., Campbell, M. E., Phillips, D. J., Gluckman, P. D., Challis, J. R. G., & Harding, J. E. (2003) · Science · doi:10.1126/science.1080803 · Cited by 271 · see citing works
Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer
Dean, W., Santos, F., & Reik, W. (2003) · Seminars in Cell and Developmental Biology · doi:10.1016/s1084-9521(02)00141-6 · Cited by 270 · see citing works
The dangerous road of catch-up growth
Hales, C. N., & Ozanne, S. E. (2002) · The Journal of Physiology · doi:10.1111/j..2002.00005.x · Cited by 268 · see citing works
Formation of binucleated myocardial cells in the neonatal rat. An index for growth hypertrophy.
Clubb, F. J., & Bishop, S. P. (1984) · PubMed · Cited by 265 · see citing works
Weanling Rats Exposed to Maternal Low-Protein Diets during Discrete Periods of Gestation Exhibit Differing Severity of Hypertension
Langley‐Evans, S. C., Welham, S. J. M., Sherman, R. C., & Jackson, A. A. (1996) · Clinical Science · doi:10.1042/cs0910607 · Cited by 265 · see citing works
Transcription factor families: muscling in on the myogenic program.
Ludolph, D. C., & Konieczny, S. F. (1995) · The FASEB Journal · doi:10.1096/fasebj.9.15.8529839 · Cited by 262 · see citing works
Fetal growth restriction: adaptations and consequences
McMillen, I. C., Adams, M. B., Ross, J. T., Coulter, C. L., Simonetta, G., Owens, J. A., Robinson, J. S., & Edwards, L. J. (2001) · Reproduction · doi:10.1530/rep.0.1220195 · Cited by 262 · see citing works
Self-citation
Fewer nephrons at birth: A missing link in the etiology of essential hypertension?
Mackenzie, H. S., & Brenner, B. M. (1995) · American Journal of Kidney Diseases · doi:10.1016/0272-6386(95)90161-2 · Cited by 261 · see citing works
Prenatal Dexamethasone Programs Hypertension and Renal Injury in the Rat
Ortiz, L. A., Quan, A. H., Zarzar, F., Weinberg, A., & Baum, M. (2003) · HYPERTENSION · doi:10.1161/01.hyp.0000049763.51269.51 · Cited by 261 · see citing works
Diabetes in old male offspring of rat dams fed a reduced protein diet
Petry, C. J., Dorling, M. W., Pawlak, D. B., Ozanne, S. E., & Hales, C. N. (2001) · Journal of Diabetes Research · doi:10.1155/edr.2001.139 · Cited by 254 · see citing works
Serum Leptin Concentration in Cord Blood: Relationship to Birth Weight and Gender
Matsuda, J., Yokota, I., Iida, M., Murakami, T., Naito, E., Ito, M., Shima, K., & Kuroda, Y. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.5.4063 · Cited by 254 · see citing works
Fetal programming of appetite and obesity
Breier, B. H., Vickers, M. H., Ikenasio, B. A., Chan, Y., & Wong, W. P. S. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00634-7 · Cited by 252 · see citing works
Effect of prenatal dexamethasone on rat renal development.
Ortiz, L. A., Quan, A. H., Weinberg, A., & Baum, M. (2001) · Kidney International · doi:10.1046/j.1523-1755.2001.0590051663.x · Cited by 251 · see citing works
Review of the Evidence on Fetal and Early Childhood Antecedents of Adult Chronic Disease
Joseph, K. S., & Kramer, M. S. (1996) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a017923 · Cited by 251 · see citing works
Reduced Nephron Number in Adult Sheep, Hypertensive as a Result of Prenatal Glucocorticoid Treatment
Wintour, E. M., Moritz, K. M., Johnson, K., Ricardo, S. D., Samuel, C. S., & Dodic, M. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.042408 · Cited by 251 · see citing works
Relation between weight and length at birth and body mass index in young adulthood: cohort study: Table 1
Sørensen, H. T., Sabroe, S., Rothman, K. J., Gillman, M. W., Fischer, P., & Sørensen, T. I. A. (1997) · BMJ · doi:10.1136/bmj.315.7116.1137 · Cited by 249 · see citing works
Maternal Undernutrition from Early- to Mid-Gestation Leads to Growth Retardation, Cardiac Ventricular Hypertrophy, and Increased Liver Weight in the Fetal Sheep
Vonnahme, K. A., Hess, B. W., Hansen, T. R., McCormick, R. J., Rule, D. C., Moss, G. E., Murdoch, W. J., Nijland, M. J., Skinner, D. C., Nathanielsz, P. W., et al. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.012120 · Cited by 246 · see citing works
Obesity and Enhanced Diabetes and Cardiovascular Risk in Adult Rats due to Early Postnatal Overfeeding
Plagemann, A., Heidrich, I., Götz, F., Rohde, W., & Dörner, G. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211159 · Cited by 245 · see citing works
Dietary Protein Restriction in Pregnancy Induces Hypertension and Vascular Defects in Rat Male Offspring
Brawley, L., Itoh, S., Torrens, C., Barker, A. C., Bertram, C. E., Poston, L., & Hanson, M. A. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000065731.00639.02 · Cited by 244 · see citing works
Predictive Adaptive Responses to Maternal High-Fat Diet Prevent Endothelial Dysfunction but Not Hypertension in Adult Rat Offspring
Khan, I. Y., Dekou, V., Hanson, M. A., Poston, L., & Taylor, P. D. (2004) · Circulation · doi:10.1161/01.cir.0000139843.05436.a0 · Cited by 242 · see citing works
Twin studies in medical research: can they tell us whether diseases are genetically determined?
Phillips, D. I. W. (1993) · The Lancet · doi:10.1016/0140-6736(93)91086-2 · Cited by 241 · see citing works
Maternal Undernutrition during Early to Midgestation Programs Tissue-Specific Alterations in the Expression of the Glucocorticoid Receptor, 11β-Hydroxysteroid Dehydrogenase Isoforms, and Type 1 Angiotensin II Receptor in Neonatal Sheep*
Whorwood, C. B., Firth, K., Budge, H., & Symonds, M. E. (2001) · Endocrinology · doi:10.1210/endo.142.7.8264 · Cited by 241 · see citing works
Maternal Endocrine Adaptation throughout Pregnancy to Nutritional Manipulation: Consequences for Maternal Plasma Leptin and Cortisol and the Programming of Fetal Adipose Tissue Development
Bispham, J., Gopalakrishnan, G. S., Dandrea, J., Wilson, V., Budge, H., Keisler, D. H., Broughton Pipkin, F., Stephenson, T., & Symonds, M. E. (2003) · Endocrinology · doi:10.1210/en.2003-0320 · Cited by 240 · see citing works
Low birthweight and adult insulin resistance: the “catch-up growth” hypothesis: Figure 1
Cianfarani, S., Germani, D., & Branca, F. (1999) · Archives of Disease in Childhood Fetal & Neonatal · doi:10.1136/fn.81.1.f71 · Cited by 239 · see citing works
Effects of birth weight and postnatal nutrition on neonatal sheep: II. Skeletal muscle growth and development.
Greenwood, P. L., Hunt, A. S., Hermanson, J. W., & Bell, A. W. (2000) · Journal of Animal Science · doi:10.2527/2000.78150x · Cited by 237 · see citing works
Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine
Jackson, A. A., Dunn, R. L., Marchand, M. C., & Langley‐Evans, S. C. (2002) · Clinical Science · doi:10.1042/cs1030633 · Cited by 234 · see citing works
Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development
Hoet, J. J., & Hanson, M. A. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.617ad.x · Cited by 232 · see citing works
Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle
Ozanne, S. E., Olsen, G., Hansen, L., Tingey, K., NAVÉ, B. T., Wang, C., Hartil, K., Petry, C. J., Buckley, A., & Mosthaf, L. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1770235 · Cited by 230 · see citing works
Maternal Protein Restriction Influences the Programming of the Rat Hypothalamic-Pituitary-Adrenal Axis
Langley‐Evans, S. C., Gardner, D. S., & Jackson, A. A. (1996) · Journal of Nutrition · doi:10.1093/jn/126.6.1578 · Cited by 229 · see citing works
Size at Birth and Cord Blood Levels of Insulin, Insulin-Like Growth Factor I (IGF-I), IGF-II, IGF-Binding Protein-1 (IGFBP-1), IGFBP-3, and the Soluble IGF-II/Mannose-6-Phosphate Receptor in Term Human Infants
Ong, K. K., Kratzsch, J., Kieß, W., Costello, M., Scott, C. D., & Dunger, D. B. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.11.6998 · Cited by 228 · see citing works
Gluconeogenesis, glucose handling, and structural changes in livers of the adult offspring of rats partially deprived of protein during pregnancy and lactation.
BURNS, S. P., Desai, M., Cohen, R. D., Hales, C. N., Iles, R. A., Germain, J., GOING, T. C. H., & Bailey, R. A. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119703 · Cited by 228 · see citing works
Weight in infancy and prevalence of coronary heart disease in adult life
Fall, C. H. D., Vijayakumar, M., Barker, D. J. P., Osmond, C., & Duggleby, S. (1995) · BMJ · doi:10.1136/bmj.310.6971.17 · Cited by 227 · see citing works
Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat
Garofano, A., Czernichow, P., & Bréant, B. (1998) · Diabetologia · doi:10.1007/s001250051038 · Cited by 226 · see citing works
Early nutrition and leptin concentrations in later life
Singhal, A., Farooqi, I. S., O’Rahilly, S., Cole, T. J., Fewtrell, M. S., & Lucas, A. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.6.993 · Cited by 225 · see citing works
An intact renin – angiotensin system is a prerequisite for normal renal development
Guron, G., & Friberg, P. (2000) · Journal of Hypertension · doi:10.1097/00004872-200018020-00001 · Cited by 222 · see citing works
Low birth weight and risk of high blood pressure in adulthood
Gennser, G. M., Rymark, P., & Isberg, P. (1988) · BMJ · doi:10.1136/bmj.296.6635.1498 · Cited by 216 · see citing works
Hypertension induced by foetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockade of maternal glucocorticoid synthesis
Langley‐Evans, S. C. (1997) · Journal of Hypertension · doi:10.1097/00004872-199715050-00010 · Cited by 216 · see citing works
Maternal diabetes during pregnancy: Consequences for the offspring
Aerts, L., Holemans, K., & Assche, F. A. V. (1990) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610060303 · Cited by 215 · see citing works
Apoptosis in the Pancreatic Islet Cells of the Neonatal Rat Is Associated with a Reduced Expression of Insulin-Like Growth Factor II that May Act as a Survival Factor
Petrik, J., Arany, E. J., McDonald, T. J., & Hill, D. J. (1998) · Endocrinology · doi:10.1210/endo.139.6.6042 · Cited by 211 · see citing works
Apoptosis contributes to the involution of beta cell mass in the post partum rat pancreas.
Scaglia, L., Smith, F. E., & Bonner‐Weir, S. (1995) · Endocrinology · doi:10.1210/endo.136.12.7588296 · Cited by 211 · see citing works
Type 2 diabetes in pregnancy: a growing concern
Feig, D. S., & Palda, V. A. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08599-9 · Cited by 210 · see citing works
The dangerous road of catch-up growth
Hales, C. N., & Ozanne, S. E. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.024406 · Cited by 210 · see citing works
Muscle cellularity and postnatal growth in the pig1
Dwyer, C. M., Fletcher, J. M., & Stickland, N. C. (1993) · Journal of Animal Science · doi:10.2527/1993.71123339x · Cited by 208 · see citing works
Observations on the Orexigenic Hypothalamic Neuropeptide Y‐System in Neonatally Overfed Weanling Rats
Plagemann, Harder, Rake, Waas, Melchior, Ziska, Rohde, & Dörner (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00357.x · Cited by 208 · see citing works
Obesity and Adipocyte Abnormalities in Offspring of Rats Undernourished During Pregnancy
Jones, A. P., & Friedman, M. I. (1982) · Science · doi:10.1126/science.7063860 · Cited by 208 · see citing works

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Weight Gain During Pregnancy: Reexamining the Guidelines
Rasmussen, K. M., & Yaktine, A. L. (2009) · Cited by 4,052 · see citing works
Effect of In Utero and Early-Life Conditions on Adult Health and Disease
Gluckman, P. D., Hanson, M. A., Cooper, C., & Thornburg, K. L. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708473 · Cited by 3,898 · see citing works
Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development
Dolinoy, D. C., Huang, D., & Jirtle, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703739104 · Cited by 1,369 · see citing works
Early Developmental Conditioning of Later Health and Disease: Physiology or Pathophysiology?
Hanson, M. A., & Gluckman, P. D. (2014) · Physiological Reviews · doi:10.1152/physrev.00029.2013 · Cited by 1,188 · see citing works
BOARD-INVITED REVIEW: Intrauterine growth retardation: Implications for the animal sciences1
Wu, G., Bazer, F. W., Wallace, J. M., & Spencer, T. E. (2006) · Journal of Animal Science · doi:10.2527/jas.2006-156 · Cited by 1,180 · see citing works
Epigenetic Modifications
Handy, D. E., Castro, R., & Loscalzo, J. (2011) · Circulation · doi:10.1161/circulationaha.110.956839 · Cited by 1,074 · see citing works
Early life events and their consequences for later disease: a life history and evolutionary perspective
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · American Journal of Human Biology · doi:10.1002/ajhb.20590 · Cited by 1,006 · see citing works
Epigenetic Epidemiology of the Developmental Origins Hypothesis
Waterland, R. A., & Michels, K. B. (2007) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.27.061406.093705 · Cited by 883 · see citing works
DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status
Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J. F., Rees, W. D., Maloney, C. A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707258104 · Cited by 812 · see citing works
Developmental Origins of Health and Disease
Gillman, M. W. (2005) · New England Journal of Medicine · doi:10.1056/nejme058187 · Cited by 756 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Ten Putative Contributors to the Obesity Epidemic
McAllister, E. J., Dhurandhar, N. V., Keith, S. W., Aronne, L. J., Barger, J., Baskin, M., Benca, R. M., Biggio, J., Boggiano, M. M., Eisenmann, J. C., et al. (2009) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408390903372599 · Cited by 710 · see citing works
Nutrients, foods, and colorectal cancer prevention
Song, M., Garrett, W. S., & Chan, A. T. (2015) · Gastroenterology · doi:10.1053/j.gastro.2014.12.035 · Cited by 700 · see citing works
Understanding transgenerational epigenetic inheritance via the gametes in mammals
Daxinger, L., & Whitelaw, E. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3188 · Cited by 700 · see citing works
Epigenetics and the embodiment of race: Developmental origins of US racial disparities in cardiovascular health
Kuzawa, C. W., & Sweet, E. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20822 · Cited by 683 · see citing works
Child Health, Developmental Plasticity, and Epigenetic Programming
Hochberg, Z., Feil, R., Constância, M., Fraga, M. F., Junien, C., Carel, J., Boileau, P., Bouc, Y. L., Deal, C., Lillycrop, K. A., et al. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0039 · Cited by 631 · see citing works
DNA methylation signatures link prenatal famine exposure to growth and metabolism
Tobi, E. W., Goeman, J. J., Monajemi, R., Gu, H., Putter, H., Zhang, Y., Slieker, R. C., Stok, A. P., Thijssen, P. E., Müller, F., et al. (2014) · Nature Communications · doi:10.1038/ncomms6592 · Cited by 630 · see citing works
The evolution of growth trajectories: what limits growth rate?
Dmitriew, C. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00136.x · Cited by 601 · see citing works
Epigenetic Mechanisms and the Mismatch Concept of the Developmental Origins of Health and Disease
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Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases
Kell, D. B. (2009) · BMC Medical Genomics · doi:10.1186/1755-8794-2-2 · Cited by 554 · see citing works
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Bateson, P., Gluckman, P., & Hanson, M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271460 · Cited by 533 · see citing works
Acute kidney injury: a springboard for progression in chronic kidney disease
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Intrauterine Programming of Physiological Systems: Causes and Consequences
Fowden, A. L., Giussani, D. A., & Forhead, A. J. (2006) · Physiology · doi:10.1152/physiol.00050.2005 · Cited by 511 · see citing works
Maternal methyl supplements increase offspring DNA methylation at <i>Axin fused</i>
Waterland, R. A., Dolinoy, D. C., Lin, J., Smith, C. A., Shi, X., & Tahiliani, K. G. (2006) · genesis · doi:10.1002/dvg.20230 · Cited by 480 · see citing works
Eating behaviour and weight in children
Webber, L., Hill, C., Saxton, J., van Jaarsveld, C. H. M., & Wardle, J. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.219 · Cited by 454 · see citing works
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Iacobini, C., Pugliese, G., Blasetti Fantauzzi, C., Federici, M., & Menini, S. (2019) · Metabolism · doi:10.1016/j.metabol.2018.11.009 · Cited by 453 · see citing works
Recommendations for Prevention of Childhood Obesity
Davis, M. M., Gance‐Cleveland, B., Hassink, S. G., Johnson, R. M., Paradis, G., & Resnicow, K. (2007) · PEDIATRICS · doi:10.1542/peds.2007-2329e · Cited by 452 · see citing works
Cell aging in relation to stress arousal and cardiovascular disease risk factors
Epel, E. S., Lin, J., Wilhelm, F. H., Wolkowitz, O. M., Cawthon, R., Adler, N. E., Dolbier, C., Mendes, W. B., & Blackburn, E. H. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.08.011 · Cited by 450 · see citing works
Programming of body composition by early growth and nutrition
Wells, J. C. K., Chomtho, S., & Fewtrell, M. S. (2007) · Proceedings of The Nutrition Society · doi:10.1017/s0029665107005691 · Cited by 441 · see citing works
Age-Related Change in Mobility: Perspectives From Life Course Epidemiology and Geroscience
Ferrucci, L., Cooper, R., Shardell, M. D., Simonsick, E. M., Schrack, J. A., & Kuh, D. J. (2016) · The Journals of Gerontology Series A · doi:10.1093/gerona/glw043 · Cited by 418 · see citing works
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Shankar, K., Harrell, A., Liu, X., Gilchrist, J. M., Ronis, M. J. J., & Badger, T. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00316.2007 · Cited by 385 · see citing works
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Kirk, S. L., Samuelsson, A., Argenton, M., Dhonye, H., Κalamatianos, T., Poston, L., Taylor, P. D., & Coen, C. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005870 · Cited by 384 · see citing works
Cardiometabolic Differences in Children Born After in Vitro Fertilization: Follow-Up Study
Ceelen, M., van Weissenbruch, M. M., Vermeiden, J. P. W., van Leeuwen, F. E., & de Waal, H. A. D. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2432 · Cited by 383 · see citing works
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Nutritional programming of the metabolic syndrome
Symonds, M. E., Sebert, S. P., Hyatt, M. A., & Budge, H. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.195 · Cited by 368 · see citing works
Prevalence of obesity, hypertension, and diabetes, and cascade of care in sub-Saharan Africa: a cross-sectional, population-based study in rural and urban Malawi
Price, A., Crampin, A. C., Amberbir, A., Kayuni-Chihana, N., Musicha, C., Tafatatha, T., Branson, K. R., Lawlor, D. A., Mwaiyeghele, E., Nkhwazi, L., et al. (2018) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(17)30432-1 · Cited by 340 · see citing works
Social Determinants of Racial Disparities in CKD
Norton, J. M., Moxey-Mims, M. M., Eggers, P. W., Narva, A. S., Star, R. A., Kimmel, P. L., & Rodgers, G. P. (2016) · Journal of the American Society of Nephrology · doi:10.1681/asn.2016010027 · Cited by 345 · see citing works
A life-course approach to the aetiology of late-onset dementias
Whalley, L. J., Dick, F. D., & McNeill, G. (2005) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70286-6 · Cited by 346 · see citing works
Nutritional programming of gastrointestinal tract development. Is the pig a good model for man?
Guilloteau, P., Zabielski, R., Hammon, H. M., & Metges, C. C. (2010) · Nutrition Research Reviews · doi:10.1017/s0954422410000077 · Cited by 341 · see citing works
Programming placental nutrient transport capacity
Fowden, A. L., Ward, J. W., Wooding, F. P. B., Forhead, A. J., & Constancia, M. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.104141 · Cited by 334 · see citing works
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Gluckman, P. D., & Hanson, M. A. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.240 · Cited by 333 · see citing works
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Luyckx, V. A., & Brenner, B. M. (2010) · Journal of the American Society of Nephrology · doi:10.1681/asn.2009121248 · Cited by 332 · see citing works
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Heude, B., Forhan, A., Slama, R., Douhaud, L., Bedel, S., Saurel‐Cubizolles, M., Hankard, R., Thiébaugeorges, O., Agostini, M. D., Annesi‐Maesano, I., et al. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyv151 · Cited by 331 · see citing works
Food Insecurity and Weight Status Among U.S. Children and Families
Larson, N. I., & Story, M. T. (2011) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2010.10.028 · Cited by 330 · see citing works
Evolution in Health and Disease
(2007) · doi:10.1093/acprof:oso/9780199207466.001.0001 · Cited by 322 · see citing works
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Case, A. C., & Paxson, C. H. (2010) · Demography · doi:10.1353/dem.2010.0007 · Cited by 321 · see citing works
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Wang, J., Chen, L., Li, D., Yin, Y., Wang, X., Li, P., Dangott, L. J., Hu, W., & Wu, G. (2008) · Journal of Nutrition · doi:10.1093/jn/138.1.60 · Cited by 318 · see citing works
Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve?
Nettle, D., & Melissa Bateson, B. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1005 · Cited by 309 · see citing works
Metabolic plasticity during mammalian development is directionally dependent on early nutritional status
Gluckman, P. D., Lillycrop, K. A., Vickers, M. H., Pleasants, A. B., Phillips, E. S., Beedle, A. S., Burdge, G. C., & Hanson, M. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705667104 · Cited by 309 · see citing works
Central role of E3 ubiquitin ligase MG53 in insulin resistance and metabolic disorders
Song, R., Peng, W., Zhang, Y., Lv, F., Wu, H., Guo, J., Cao, Y., Pi, Y., Zhang, X., Li, J., et al. (2013) · Nature · doi:10.1038/nature11834 · Cited by 306 · see citing works
Adult Hypertension and Kidney Disease
Zandi‐Nejad, K., Luyckx, V. A., & Brenner, B. M. (2006) · Hypertension · doi:10.1161/01.hyp.0000198544.09909.1a · Cited by 300 · see citing works
Brain function and chromatin plasticity
Dulac, C. G. (2010) · Nature · doi:10.1038/nature09231 · Cited by 299 · see citing works
Intergenerational Transmission of Glucose Intolerance and Obesity by In Utero Undernutrition in Mice
Jiménez‐Chillarón, J. C., ISGANAITIS, E. M., Charalambous, M., Gesta, S., Pentinat, T., Faucette, R., Otis, J. P., Chow, A., Díaz, R., Ferguson‐Smith, A. C., et al. (2008) · Diabetes · doi:10.2337/db08-0490 · Cited by 299 · see citing works
Birth weight, malnutrition and kidney-associated outcomes—a global concern
Luyckx, V. A., & Brenner, B. M. (2015) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.251 · Cited by 289 · see citing works
SHEEP MODELS OF INTRAUTERINE GROWTH RESTRICTION: FETAL ADAPTATIONS AND CONSEQUENCES
Morrison, J. L. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2008.04975.x · Cited by 289 · see citing works
Developmental Programming of Cardiovascular Dysfunction by Prenatal Hypoxia and Oxidative Stress
Giussani, D. A., Camm, E. J., Niu, Y., Richter, H. G., Blanco, C. E., Gottschalk, R., Blake, E. Z., Horder, K. A., Thakor, A. S., Hansell, J. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031017 · Cited by 278 · see citing works
Epigenomics, gestational programming and risk of metabolic syndrome
Desai, M., Jellyman, J. K., & Ross, M. G. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.13 · Cited by 277 · see citing works
Depressive Symptoms and Stressful Life Events Predict Metabolic Syndrome Among Middle-Aged Women
Räikkönen, K., Matthews, K. A., & Kuller, L. H. (2007) · Diabetes Care · doi:10.2337/dc06-1857 · Cited by 276 · see citing works
Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Müllerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle
Ireland, J. J., Smith, G. W., Scheetz, D. M., Jimenez‐Krassel, F., Folger, J. K., Ireland, J. L. H., Mossa, F., Lonergan, P., & Evans, A. C. O. (2010) · Reproduction Fertility and Development · doi:10.1071/rd10226 · Cited by 275 · see citing works
Imprinted Genes, Placental Development and Fetal Growth
Fowden, A. L., Sibley, C. P., Reik, W., & Constância, M. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091506 · Cited by 273 · see citing works
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Christian, P. S., & Stewart, C. P. (2010) · Journal of Nutrition · doi:10.3945/jn.109.116327 · Cited by 273 · see citing works
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Rando, O. J., & Simmons, R. A. (2015) · Cell · doi:10.1016/j.cell.2015.02.021 · Cited by 271 · see citing works
The Placenta and Intrauterine Programming
Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01663.x · Cited by 267 · see citing works
The role of nutrition on epigenetic modifications and their implications on health
Jiménez-Chillarón, J. C., Díaz, R., Martínez, D., Pentinat, T., Ramón-Krauel, M., Ribó, S., & Plösch, T. (2012) · Biochimie · doi:10.1016/j.biochi.2012.06.012 · Cited by 266 · see citing works
Metastable Epialleles, Imprinting, and the Fetal Origins of Adult Diseases
Dolinoy, D. C., Das, R., Weidman, J. R., & Jirtle, R. L. (2007) · Pediatric Research · doi:10.1203/pdr.0b013e31804575f7 · Cited by 265 · see citing works
A systematic review and meta-analysis of micronutrient intakes during pregnancy in developed countries
Blumfield, M., Hure, A. J., MacDonald‐Wicks, L. K., Smith, R., & Collins, C. E. (2013) · Nutrition Reviews · doi:10.1111/nure.12003 · Cited by 264 · see citing works
Developmental Origins of Adult Disease
Langley‐Evans, S. C., & McMullen, S. (2010) · Medical Principles and Practice · doi:10.1159/000273066 · Cited by 261 · see citing works
Placental Adaptations in Growth Restriction
Zhang, S., Regnault, T. R. H., Barker, P., Botting, K. J., McMillen, I. C., McMillan, C., Roberts, C. T., & Morrison, J. L. (2015) · Nutrients · doi:10.3390/nu7010360 · Cited by 261 · see citing works
Self-citation
Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos
Lonergan, P., Fair, T., Corcoran, D., & Evans, A. C. O. (2005) · Theriogenology · doi:10.1016/j.theriogenology.2005.09.028 · Cited by 262 · see citing works
Early-Life Risk Factors for Alzheimer Disease
Borenstein, A. R., Copenhaver, C. I., & Mortimer, J. A. (2006) · Alzheimer Disease & Associated Disorders · doi:10.1097/01.wad.0000201854.62116.d7 · Cited by 259 · see citing works
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Adverse renal consequences of obesity
Griffin, K. A., Kramer, H., & BIDANI, A. K. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00324.2007 · Cited by 250 · see citing works
Fetal Programming and Metabolic Syndrome
Rinaudo, P. F., & Wang, E. T. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153245 · Cited by 250 · see citing works
Developmental Origins of Adult Health and Disease: The Role of Periconceptional and Foetal Nutrition
McMillen, I. C., MacLaughlin, S. M., Mühlhäusler, B. S., Gentili, S., Duffield, J. A., & Morrison, J. L. (2008) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00188.x · Cited by 247 · see citing works
Self-citation
Pathophysiology, phenotypes and management of type 2 diabetes mellitus in Indian and Chinese populations
Ke, C., Narayan, K. M. V., Chan, J. C. N., Jha, P., & Shah, B. R. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00669-4 · Cited by 253 · see citing works
Multigenerational and transgenerational effects of endocrine disrupting chemicals: A role for altered epigenetic regulation?
Xin, F., Susiarjo, M., & Bartolomei, M. S. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.05.008 · Cited by 238 · see citing works
Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine
de Rooij, S. R., Painter, R. C., Roseboom, T. J., Phillips, D. I. W., Osmond, C., Barker, D. J. P., Tanck, M. W. T., Michels, R. P. J., Bossuyt, P. M., & Bleker, O. P. (2006) · Diabetologia · doi:10.1007/s00125-005-0136-9 · Cited by 237 · see citing works
Impact of maternal body mass index on neonate birthweight and body composition
Hull, H. R., Dinger, M. K., KNEHANS, A. W., Thompson, D. M., & Fields, D. A. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.10.796 · Cited by 236 · see citing works
Maternal “junk‐food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring
Ong, Z. Y., & Mühlhäusler, B. S. (2011) · The FASEB Journal · doi:10.1096/fj.10-178392 · Cited by 234 · see citing works
Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings
Entringer, S., Buß, C., & Wadhwa, P. D. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283405921 · Cited by 236 · see citing works
Adaptive Responses by Mouse Early Embryos to Maternal Diet Protect Fetal Growth but Predispose to Adult Onset Disease1
Watkins, A. J., Ursell, E., Panton, R. W., Papenbrock, T., Hollis, L. J., Cunningham, C. M., Wilkins, A., Perry, V. H., Sheth, B., Kwong, W. Y., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.064220 · Cited by 227 · see citing works
The Programming Power of the Placenta
Sferruzzi-Perri, A. N., & Camm, E. J. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00033 · Cited by 223 · see citing works
Developmental Origins of Adult Function and Health: Evolutionary Hypotheses
Kuzawa, C. W., & Quinn, E. A. (2009) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-091908-164350 · Cited by 222 · see citing works
Enamel hypoplasia and early mortality: Bioarcheological support for the Barker hypothesis
Armelagos, G. J., Goodman, A. H., Harper, K. N., & Blakey, M. L. (2009) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20239 · Cited by 221 · see citing works
Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance
Nivoit, P., Morens, C., Assche, F. A. V., Jansen, E. H. J. M., Poston, L., Remacle, C., & Reusens, B. (2009) · Diabetologia · doi:10.1007/s00125-009-1316-9 · Cited by 221 · see citing works
Maternal Undernutrition in Cows Impairs Ovarian and Cardiovascular Systems in Their Offspring1
Mossa, F., Carter, F., Walsh, S. W., Kenny, D. A., Smith, G. W., Ireland, J. L. H., Hildebrandt, T. B., Lonergan, P., Ireland, J. J., & Evans, A. C. O. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.112.107235 · Cited by 214 · see citing works
The health implications of birth by Caesarean section
Hyde, M. J., Mostyn, A., Modi, N., & Kemp, P. R. (2011) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2011.00195.x · Cited by 214 · see citing works
The Epigenetic Basis of Twin Discordance in Age-Related Diseases
Poulsen, P., Esteller, M., Vaag, A. A., & Fraga, M. F. (2007) · Pediatric Research · doi:10.1203/pdr.0b013e31803c7b98 · Cited by 211 · see citing works
Fetal programming: link between early nutrition, DNA methylation, and complex diseases
Chmurzyńska, A. (2010) · Nutrition Reviews · doi:10.1111/j.1753-4887.2009.00265.x · Cited by 211 · see citing works
Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows
Symonds, M. E., Stephenson, T. J., Gardner, D. S., & Budge, H. (2006) · Reproduction Fertility and Development · doi:10.1071/rd06130 · Cited by 205 · see citing works
Developmental Origins of Health and Disease
Rass, E. (2017) · Routledge eBooks · doi:10.4324/9781315445564-6 · Cited by 200 · see citing works
Sex differences in the fetal programming of hypertension
Grigore, D., Ojeda, N. B., & Alexander, B. T. (2008) · Gender Medicine · doi:10.1016/j.genm.2008.03.012 · Cited by 203 · see citing works
Putative biological mechanisms for the association between early life adversity and the subsequent development of PTSD
Yehuda, R., Flory, J. D., Pratchett, L. C., Buxbaum, J. D., Ising, M., & Holsboer, F. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1969-6 · Cited by 202 · see citing works
Maternal obesity, diabetes during pregnancy and epigenetic mechanisms that influence the developmental origins of cardiometabolic disease in the offspring
Agarwal, P., Morriseau, T. S., Kereliuk, S. M., Doucette, C. A., Wicklow, B. A., & Dolinsky, V. W. (2018) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2017.1422109 · Cited by 202 · see citing works
The vascular endothelial growth factor family in adverse pregnancy outcomes
Andraweera, P. H., Dekker, G., & Roberts, C. T. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms011 · Cited by 199 · see citing works
Redox Biology in Transition Periods of Dairy Cattle: Role in the Health of Periparturient and Neonatal Animals
Abuelo, Á., Bermúdez, J. H., Benedito, J. L., & Castillo, C. (2019) · Antioxidants · doi:10.3390/antiox8010020 · Cited by 201 · see citing works
Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice: Undernutrition and placental phenotype
Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., & Fowden, A. L. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2009.181214 · Cited by 199 · see citing works
Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood
Criscuolo, F., Monaghan, P., Nasir, L., & Metcalfe, N. B. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.0148 · Cited by 199 · see citing works
Gestational Hypoxia and Developmental Plasticity
Ducsay, C. A., Goyal, R., Pearce, W. J., Wilson, S. M., Hu, X., & Zhang, L. (2018) · Physiological Reviews · doi:10.1152/physrev.00043.2017 · Cited by 203 · see citing works
Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice
Coan, P. M., Angiolini, E., Sandovici, I., Burton, G. J., Constância, M., & Fowden, A. L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.156133 · Cited by 194 · see citing works

Developmental origins of adult diseases
Mathew, V., & Ayyar, S. (2012) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.98005 · Cited by 13 · see citing works
Nutritional programming of the metabolic syndrome
Symonds, M. E., Sebert, S. P., Hyatt, M. A., & Budge, H. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.195 · Cited by 368 · see citing works
Mechanisms involved in the developmental programming of adulthood disease
Warner, M. J., & Ozanne, S. E. (2010) · Biochemical Journal · doi:10.1042/bj20091861 · Cited by 316 · see citing works
Current Opinion in Developmental Origins of Health and Disease
Hui-xi, Y., & Zeng, C. (2011) · Journal of International Obstetrics and Gynecology
Endocrine programming and fetal origins of adult disease
PHILLIPS, D. (2002) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00696-3 · Cited by 68 · see citing works

Authors: Mcmillen, I. C., & Robinson, J. S.
Affiliations: The University of Adelaide (AU)
ORCID: Robinson, Jeffrey S.
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2005-04
Volume: 85
Issue: 2
Pages: 571-633
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00053.2003
OpenAlex: W2140498210
Cited by: 1,910
References: 590
Citations by year: 2026: 27 · 2025: 32 · 2024: 43 · 2023: 45 · 2022: 48 · 2021: 72 · 2020: 70 · 2019: 73 · 2018: 83 · 2017: 91 · 2016: 93 · 2015: 116 · 2014: 112 · 2013: 120 · 2012: 135
FWCI: 21.36
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: developmental origins of adult disease, fetal origins of adult disease, metabolic syndrome, intrauterine environment, fetal programming, epigenetic adaptation, early life nutrition, hypertension, insulin resistance, obesity, cardiovascular disease, diabetes mellitus, developmental plasticity
MeSH terms: Aging, Animals, Humans, Models, Biological, Phenotype, Metabolic Syndrome, Epigenesis, Genetic

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Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming

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