Cited by 203Birth, Development, and HealthPregnancy and preeclampsia studiesPrenatal Substance Exposure Effects

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Fetal programming of cardiovascular function through exposure to maternal undernutrition

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Langley-Evans, Simon C.·2001·Proceedings of the Nutrition Society

DOI 10.1079/pns2001111

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A substantial and robust body of epidemiological evidence indicates that prenatal dietary experience may be a factor determining cardiovascular disease risk. Retrospective cohort studies indicate that low birth weight and disproportion at birth are powerful predictors of later disease risk. This prenatal influence on non-communicable disease in later life has been termed programming. Maternal nutritional status has been proposed to be the major programming influence on the developing fetus. The evidence from epidemiological studies of nutrition, fetal development and birth outcome is, however, often weak and inconclusive. The validity of the nutritional programming concept is highly dependent on experimental studies in animals. The feeding of low-protein diets in rat pregnancy results in perturbations in fetal growth and dimensions at birth. The offspring of rats fed low-protein diets exhibit a number of metabolic and physiological disturbances, and are consistently found to have high blood pressure from early postnatal life. This experimental model has been used to explore potential mechanisms of programming through which maternal diet may programme the cardiovascular function of the fetus. Indications from this work are that fetal exposure to maternally-derived glucocorticoids plays a key role in the programming mechanism. Secondary to this activity, the fetal hypothalamic–pituitary–adrenal axis may stimulate renin–angiotensin system activity, resulting in increased vascular resistance and hypertension.

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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
Diet and Health: What Should We Eat?
Willett, W. C. (1994) · Science · doi:10.1126/science.8160011 · Cited by 1,008 · cited 1×
“As reviewed by Willett (1994), the consumption of a high-fat diet, low in starch and fibre, appears to substantially raise individual risk of cardio-vascular mortality.”
Mothers, Babies, and Disease in Later Life
Gillman, M. W. (1995) · BMJ · doi:10.1136/bmj.310.6971.68a · Cited by 880
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
Mothers, Babies and Disease in Later Life
Barker, D. J. P., & Barker, D. J. P. (1994) · Medical Entomology and Zoology · Cited by 860
PREMATURE DELIVERY OF FOETAL LAMBS INFUSED WITH GLUCOCORTICOIDS
LIGGINS, G. C. (1969) · Journal of Endocrinology · doi:10.1677/joe.0.0450515 · Cited by 817
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
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
Self-citation
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
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

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Pickard, 1996, Altered insulin response to a glucose load in rats following exposure to a low protein diet in utero, Proceedings of the Nutrition Society, 55, 44A
Dunn, 2001, Hypertension in the mouse following intrauterine exposure to a maternal low-protein diet, Proceedings of the Nutrition Society, 60, 51A
Leon, 1999, Fetal Programming: Influences on Development and Disease in Later Life, 12
Marchand, 2001, Programming of blood pressure and renal structure in rats exposed to nitrogen-supplemented maternal low protein diets, Proceedings of the Nutrition Society, 60, 139A
Celsi, 1997, Inhibition of renal growth by prenatal dexamethasone and the programming of blood pressure in the offspring, Journal of the American Society for Nephrology, 8, A1360
Jackson, 1996, Origins and Consequences of Obesity. CIBA Foundation Symposium no. 201, 407
Sherman RC (1999) The role of the renin-angiotensin system in the fetal programming of hypertension. PhD Thesis, University of Southampton.
Roach, 1999, Protein deficiencies during pregnancy affect skeletal development in the offspring, Journal of Bone and Mineral Research, 14, S394
Rich-Edwards, 1995, Birthweight, breastfeeding and the risk of coronary heart disease in the nurses health study, American Journal of Epidemiology, 141, S78

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Dodic, M., McAlinden, A. T., Jefferies, A. J., Wintour, E. M., Cock, M. L., May, C. N., Evans, R. G., & Moritz, K. M. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.102186 · Cited by 37
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Soya protein- and casein-based nutritionally complete diets fed during gestation and lactation differ in effects on characteristics of the metabolic syndrome in male offspring of Wistar rats
Jahan-Mihan, A., Szeto, I. M. Y., Luhovyy, B. L., Huot, P. S. P., & Anderson, G. H. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511002686 · Cited by 24
Effect of protein source in diets fed during gestation and lactation on food intake regulation in male offspring of Wistar rats
Jahan-Mihan, A., Smith, C. E., & Anderson, G. H. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00744.2010 · Cited by 24
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Authors: Langley-Evans, S. C.
Venue: Proceedings of the Nutrition Society
Publisher: Cambridge University Press (CUP)
Published: 2001-11
Volume: 60
Issue: 4
Pages: 505-513
ISSN: 0029-6651 (ISSN-L)
1475-2719
DOI: 10.1079/pns2001111
OpenAlex: W2135897417
Cited by: 203
References: 94
Citations by year: 2026: 2 · 2025: 1 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 4 · 2017: 3 · 2016: 6 · 2015: 6 · 2014: 15 · 2013: 9 · 2012: 6
FWCI: 2.22
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.cambridge.org/core/terms (unspecified, 1945 d)
Locations: Proceedings of The Nutrition Society (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Keywords: fetal programming, maternal undernutrition, cardiovascular risk, low birth weight, fetal growth restriction, prenatal nutrition, low-protein diet, hypertension, glucocorticoids, hypothalamic-pituitary-adrenal axis, renin-angiotensin system, vascular resistance
MeSH terms: Animals, Birth Weight, Cardiovascular Diseases, Disease Models, Animal, Female, Glucocorticoids, Humans, Hypertension, Kidney, Nutrition Disorders, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Renin-Angiotensin System, Risk Factors, Rats

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Fetal programming of cardiovascular function through exposure to maternal undernutrition

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