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

The DOI matches its Crossref record; 93 of the 94 references it cites were found in a registry or an index.

Fetal programming of cardiovascular function through exposure to maternal undernutrition

Open access

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

DOI 10.1079/pns2001111

Open this paper in CoChat — free account Open PDF

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1079/pns2001111

Cites

93 of 93 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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

Flagged first, then by citations

Show all 94 references

1 of the 94 references couldn’t be matched to a known paper.

Research works printed but not linked: 9

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

Sorted by citations

Items 101–200 of 203

Developmental programming of cardiovascular disorders: Focus on hypertension
MohanKumar, S. M. J., King, A., Shin, A. C., Sirivelu, M. P., MohanKumar, P. S., & Fink, G. D. (2007) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-007-9047-z · Cited by 21
Effects of maternal undernutrition on renal angiotensin II and chymase in hypertensive offspring
Chou, H., Wang, L.-F., Lu, K., & Chen, C. (2008) · Acta Histochemica · doi:10.1016/j.acthis.2008.01.002 · Cited by 19
Diabetes in low-resourced countries
Ashwal‏, E., Hadar, E., & Hod, M. (2014) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2014.05.009 · Cited by 19
Role of nutrition in the development of the fetal cardiovascular system
Tappia, P. S., & Gabriel, C. A. M. (2006) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.4.2.211 · Cited by 18
Society for Reproductive Biology Founders’ Lecture 2003. The making of an embryo: short-term goals and long-term implications
Fleming, T. P., Wilkins, A., Mears, A., Miller, D. J., Thomas, F. C., Ghassemifar, R., Fesenko, I., Sheth, B., Kwong, W. Y., & Eckert, J. J. (2004) · Reproduction Fertility and Development · doi:10.1071/rd03070 · Cited by 18
The epigenetics of the hypothalamic‐pituitary‐adrenal axis in fetal development
Montenegro, Y. H. A., Nascimento, D. D. Q., Assis, T. D. O., & Lopes, S. S. D. S. (2019) · Annals of Human Genetics · doi:10.1111/ahg.12306 · Cited by 17
Birth weight, gestational age, and blood pressure: Early life management strategy and population health perspective
Salmi, I. A., Shaheen, F., & Hannawi, S. (2019) · Saudi Journal of Kidney Diseases and Transplantation · doi:10.4103/1319-2442.256836 · Cited by 18
Experimental Evidence for Long-Term Programming Effects of Early Diet
Symonds, M. E., Budge, H., Stephenson, T. J., & Gardner, D. S. (2005) · Springer eBooks · doi:10.1007/1-4020-3535-7_4 · Cited by 17
Developmental Conditioning of the Vasculature
Clough, G. F. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140037 · Cited by 22
Retrospective analysis on the efficacy of corticosteroid prophylaxis prior to elective caesarean section to reduce neonatal respiratory complications at term of pregnancy: review of literature
Paganelli, S., Soncini, E., Gargano, G., Capodanno, F., Vezzani, C., & Sala, G. B. L. (2013) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-013-3035-1 · Cited by 16
Gestational programming of offspring obesity/hypertension
Novak, D. A., Desai, M., & Ross, M. G. (2006) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050600708233 · Cited by 15
Intrauterine growth restriction promotes vascular remodelling following carotid artery ligation in rats
Menendez‐Castro, C., Cordasic, N., Schmid, M. C., Fahlbusch, F. B., Rascher, W., Amann, K., Hilgers, K. F., & Hartner, A. (2012) · Clinical Science · doi:10.1042/cs20110637 · Cited by 14
Pathophysiology of Primary Hypertension
Carey, R. M. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374530-9.00020-6 · Cited by 13
Interaction of the pre- and postnatal environment in the maternal immune activation model
Gundacker, A., Rico, L. C., Stöhrmann, P., Tillmann, K. E., Weber‐Stadlbauer, U., & Pollak, D. D. (2023) · Discover Mental Health · doi:10.1007/s44192-023-00042-5 · Cited by 15
Perinatal undernutrition increases meal size and neuronal activation of the nucleus of the solitary tract in response to feeding stimulation in adult rats
Lira, L. D. A., Almeida, L. C. D. A., da Silva, A. A. M., Cavalcante, T. C. F., de Melo, D. D. C. B., de Souza, J. A., Campina, R. C. D. F., & de Souza, S. L. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.07.007 · Cited by 13
Does in utero Exposure to Illness Matter? The 1918 Influenza Epidemic in Taiwan as a Natural Experiment
Lin, M., & Liu, E. M. (2014) · National Bureau of Economic Research · doi:10.3386/w20166 · Cited by 15
The effect of energy restriction during pregnancy on obesity-related peptide hormones in rat offspring
Hietaniemi, M., Malo, E., Jokela, M., Santaniemi, M., Ukkola, O. H., & Kesäniemi, Y. A. (2008) · Peptides · doi:10.1016/j.peptides.2008.12.021 · Cited by 12
Maternal pre‐pregnancy underweight as a risk factor for the offspring: Survey of Neonates in Pomerania
Domanski, G., Lange, A. E., Ittermann, T., Fallenberg, J., Allenberg, H., Zygmunt, M., & Heckmann, M. (2020) · Acta Paediatrica · doi:10.1111/apa.15701 · Cited by 13
Modes of imprinted gene action in learning disability
Isles, A. R., & Humby, T. (2006) · Journal of Intellectual Disability Research · doi:10.1111/j.1365-2788.2006.00843.x · Cited by 13
Prenatal protein level impacts homing behavior in Long-Evans rat pups
Fischer, L. K., McGaughy, J. A., Bradshaw, S., Weissner, W. J., Amaral, A. C. S., Rosene, D. L., Mokler, D. J., Fitzmaurice, G. M., & Galler, J. R. (2015) · Nutritional Neuroscience · doi:10.1179/1476830515y.0000000001 · Cited by 11
Environment and fetal programming: the origins of some current “pandemics”
Burgio, E. (2015) · Journal of pediatric and neonatal individualized medicine · doi:10.7363/040237 · Cited by 11
Perinatal High Methyl Donor Alters Gene Expression in IGF System in Male Offspring Without Altering DNA Methylation
Amarger, V., Giudicelli, F., Pagniez, A., & Parnet, P. (2016) · Future Science OA · doi:10.4155/fsoa-2016-0077 · Cited by 11
Long‐term impacts of early‐life exposure to malaria: Evidence from Taiwan's Eradication Campaign in the 1950s
Shih, H., & Lin, M. (2018) · Health Economics · doi:10.1002/hec.3781 · Cited by 11
Maternal low-quality protein diet exerts sex-specific effects on plasma amino acid profile and alters hepatic expression of methyltransferases in adult rat offspring
Akyol, A., Çetin, A. K., Güleç, A., Daşgın, H., Ayaz, A., & Onbaşılar, İ. (2018) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174418000132 · Cited by 11
The long‐term effects of perinatal glucocorticoid exposure on the host defence system of the respiratory tract
Theogaraj, E., John, C. S., Dewar, A. L., Buckingham, J. C., & Smith, S. (2006) · The Journal of Pathology · doi:10.1002/path.2017 · Cited by 11
Maternal supplementation with dietary arachidonic and docosahexaenoic acids during lactation elevates bone mass in weanling rat and guinea pig offspring even if born small sized
Weiler, H. A., Zhao, J., Park, L., Kohut, J., Burr, L. L., & Fitzpatrick-Wong, S. C. (2011) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2011.10.004 · Cited by 10
Green tea extract intake during lactation modified cardiac macrophage infiltration and AMP-activated protein kinase phosphorylation in weanling rats from undernourished mother during gestation and lactation
Matsumoto, E., Kataoka, S., Mukai, Y., Sato, M., & Sato, S. (2016) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000647 · Cited by 10
Prenatal Dietary Docosahexaenoic Acid Supplementation in Combination with Protein Restriction Does Not Affect Blood Pressure in Adult Wistar Rats
Martin, D., McCutcheon, D., & Wainwright, P. E. (2004) · Nutritional Neuroscience · doi:10.1080/10284150400002407 · Cited by 10
The significance of under- or overweight during childhood as a risk factor for hypertensive diseases in pregnancy
Leeners, B., Rath, W. H., KUSE, S., Irawan, C., & Neumaier-Wagner, P. M. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2005.12.012 · Cited by 10
Association between maternal pre-pregnancy body mass index and offspring’s outcomes at 9 to 15 years of age
Lichtwald, A., Weiss, C., Lange, A. E., Ittermann, T., Allenberg, H., Grabe, H. J., & Heckmann, M. (2023) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-023-07184-5 · Cited by 10
Gender differences in the expression of genes involved during cardiac development in offspring from dams on high fat diet
Elahi, M. M., & Matata, B. M. (2014) · Molecular Biology Reports · doi:10.1007/s11033-014-3605-8 · Cited by 9
Hypertension research in the 21st century
Beilin, L. J. (2004) · Journal of Hypertension · doi:10.1097/00004872-200412000-00002 · Cited by 8
Fetal Assessment Using Biomagnetometry: Neurobehaviors, Cardiac Autonomic Control, and Research Applications
Gustafson, K. M., & Popescu, E. A. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_23 · Cited by 9
Dietary curcumin supplementation ameliorates placental inflammation in rats with intra-uterine growth retardation by inhibiting the NF-κB signaling pathway
Qi, L., Jiang, J., Yu, G., Zhang, X., Qi, X. Y., Zhang, J., Zhang, L., & Wang, T. Z. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.108973 · Cited by 9
In utero programming of adult vascular function in transgenic mice lacking low-density lipoprotein receptor
Langenveld, J., Lu, F., Bytautiene, E., Anderson, G. D., Saade, G. R., & Longo, M. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.01.057 · Cited by 8
Antenatal micronutrients in undernourished people
West, K. P., & Christian, P. S. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60214-7 · Cited by 9
Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences
Schiera, G., Macajone, G., Volpes, S., Greco, L., Di Liegro, C. M., Serio, G., Caradonna, F., & Naselli, F. (2026) · Cells · doi:10.3390/cells15040366 · Cited by 8
Phylogeny and Ontogeny of the Renin-Angiotensin System
Nishimura, H. (2004) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-18495-6_2 · Cited by 8
Gender Determines Long-Lasting Effects on Adult Offspring Heart after Early-Life Malnourishment
Moura, A. S., Pereira, F. G., & Mandarim‐de‐Lacerda, C. A. (2004) · Neonatology · doi:10.1159/000076363 · Cited by 8
Pathophysiology of Primary Hypertension
Carey, R. M. (2008) · Comprehensive physiology · doi:10.1002/cphy.cp020418 · Cited by 9
Corticotropin‐releasing hormone and obesity: From fetal life to adulthood
Vasconcelos, I., von Hafe, M., Adão, R., Leite-Moreira, A. F., & Brás‐Silva, C. (2024) · Obesity Reviews · doi:10.1111/obr.13763 · Cited by 7
The Effects of Prenatal Protein Restriction on β -Adrenergic Signalling of the Adult Rat Heart during Ischaemia Reperfusion
Ryan, K. J. P., Elmes, M. J., & Langley‐Evans, S. C. (2012) · Journal of Nutrition and Metabolism · doi:10.1155/2012/397389 · Cited by 7
Self-citation
Birthweight and Gestational Age: Early Life Management Strategy to Population Health for Non-Communicable Diseases
Salmi, I. A., & Hannawi, S. (2018) · International Journal of Pediatric Research · doi:10.23937/2469-5769/1510042 · Cited by 6
Association of maternal hypertension during pregnancy with brain structure and behavioral problems in early adolescence
Ma, Q., Cui, Y., Han, X., Xiong, Y., Xu, J., Zhao, H., Li, X., Cheng, W., & Zhou, Q. (2023) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-023-02305-6 · Cited by 6
[Effect of pre and post natal undernutrition on components of metabolic syndrome later in life; systematic review].
Bacardí‐Gascón, M., Morán, E. J., Marín, E. S., & Cruz, A. J. (2014) · PubMed · doi:10.3305/nh.2014.29.5.7422 · Cited by 6
A mechanism linking perinatal 2,3,7,8 tetrachlorodibenzo-p-dioxin exposure to lower urinary tract dysfunction in adulthood
Turco, A., Oakes, S. R., Stietz, K. P. K., Dunham, C. L., Joseph, D., Chathurvedula, T. S., Girardi, N. M., Schneider, A. J., Gawdzik, J. C., Sheftel, C. M., et al. (2021) · Disease Models & Mechanisms · doi:10.1242/dmm.049068 · Cited by 4
Epigenetic changes in gene expression: focus on “The liver X-receptor gene promoter is hypermethylated in a mouse model of prenatal protein restriction”
Alexander, B. T. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00760.2009 · Cited by 6
Impulsive aggressiveness of pregnant women affects the development of the fetal heart
Koelsch, S., Wiebigke, C., Siebel, W. A., & Stepan, H. (2009) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2009.09.008 · Cited by 5
Body mass and attractivity of female offspring are negatively affected by food restriction of meadow vole (Microtus pennsylvanicus) dams during lactation
Sabau, R. M., Pierson, L. M., & Ferkin, M. (2014) · Behaviour · doi:10.1163/1568539x-00003219 · Cited by 5
Guidelines for in vivo models of developmental programming of cardiovascular disease risk
Warrington, J. P., Collins, H. E., Davidge, S. T., do Carmo, J. M., Goulopoulou, S., Intapad, S., Loria, A. S., Sones, J. L., Wold, L. E., Zinkhan, E. K., et al. (2024) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00060.2024 · Cited by 4
Effect of gestational protein restriction on left ventricle hypertrophy and heart angiotensin II signaling pathway in adult offspring rats
Silva, R. B., Mesquita, F. F., Andreo, M., Assalin, H. B., Gontijo, J. A. R., & Boer, P. A. (2013) · Health · doi:10.4236/health.2013.54a011 · Cited by 4
Maternal and Fetal Complications Due to Decreased Nitric Oxide Synthesis during Gestation
Jurado, S. R., Saraiva, K. V. D. O., Marceliano, C., de Souza, V. L., & Vieira, I. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.85383 · Cited by 4
Perinatal Programming and Blood Pressure
Kallash, M., Ingelfinger, J. R., & Vehaskari, V. M. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-490-6_7 · Cited by 4
Effect of prenatal micronutrient-fortified balanced energy-protein supplementation on maternal and newborn body composition: A sub-study from the MISAME-III randomized controlled efficacy trial in rural Burkina Faso
Argaw, A., Toe, L. C., Hanley‐Cook, G., Dailey-Chwalibóg, T., de Kok, B., Ouédraogo, L. O., Compaoré, A., Ouédraogo, M., Sawadogo, A., Ganaba, R., et al. (2023) · PLoS Medicine · doi:10.1371/journal.pmed.1004242 · Cited by 5
Food Insecurity and Nutritional Status Among Pregnant Women Living in Socio‐Economic Vulnerability in the Metropolitan Area of Buenos Aires (Argentina)
Bonfili, N., Garnis, M. L., Nievas, M. S., González, P., & Barbeito‐Andrés, J. (2025) · American Journal of Human Biology · doi:10.1002/ajhb.70033 · Cited by 3
MATERNAL BMI- HOW IT AFFECT OBSTETRIC BEHAVIOUR AND PREGNANCY OUTCOME
Saha, D., Roy, P., Koley, A. K., Saha, A., Dey, B. C., Ari, M., Ganguly, T. K., & Mukhopadhyaya, A. K. (2013) · Journal of Evolution of Medical and Dental Sciences · doi:10.14260/jemds/1185 · Cited by 3
Developmental origins of health and disease: implications for primary intervention for cardiovascular and metabolic disease
Forrester, T. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544699.034 · Cited by 3
Placental HSD2 Expression and Activity Is Unaffected by Maternal Protein Consumption or Gender in C57BL/6 Mice
Garbrecht, M. R., & Lamb, F. S. (2013) · ISRN Endocrinology · doi:10.1155/2013/867938 · Cited by 3
Effects of the Maternal Hypertension in Renal Development in Offspring of Rats
Jurado, S. R. (2014) · Journal of Clinical & Experimental Cardiology · doi:10.4172/2155-9880.1000306 · Cited by 3
Basic Experimental and Clinical Advances in the Mechanisms Underlying Abnormal Pregnancy Outcomes
Regnault, T. R. H., Nijland, M. J., Budge, H., & Morrison, J. L. (2013) · Journal of Pregnancy · doi:10.1155/2013/327638 · Cited by 3
Intrauterine undernutrition and inflammation: The story of our work
Landgraf, M. A. (2008) · Nutrition · doi:10.1016/j.nut.2008.10.001 · Cited by 2
Effects of Oxidative Stress on Vascular Reactivity in the Offspring of Protein-Restricted Stroke-Prone Spontaneously Hypertensive Rats
Takemori, K., TAHARA, A., Murakami, T., & Kometani, T. (2013) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.130244 · Cited by 2
Chemoreflex control of the cardiovascular system remains altered after recovery from low protein diet early in life
Sá, R. W. M., Borges, G. S. M., Chianca, D. A., de Oliveira, L. B., & Cardoso, L. M. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.06.008 · Cited by 2
Developmental Origins of Health and Disease
Poston, L., & Hanson, M. A. (2009) · Elsevier eBooks · doi:10.1016/b978-1-4160-4224-2.50013-2 · Cited by 2
Manipulation of the Maternal Diet in Rat Pregnancy
Langley‐Evans, S. C., Bellinger, L., Sculley, D., Langley-Evans, A. J., & McMullen, S. (2007) · Springer eBooks · doi:10.1007/0-387-32632-4_8 · Cited by 2
Self-citation
The Promise and Treachery of Nutrition in DOHaD
Moore, V., & Warin, M. J. (2024) · Cambridge University Press eBooks · doi:10.1017/9781009201704.007 · Cited by 1
Maternal under-nutrition during pregnancy alters the molecular response to over-nutrition in multiple organs and tissues in nonhuman primate juvenile offspring
Cox, L. A., Puppala, S., Chan, J., Riojas, A. M., Lange, K. J., Birnbaum, S., Dick, E. J., Comuzzie, A. G., Nijland, M. J., Li, C., et al. (2024) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174424000163 · Cited by 1
Mechanistic Aspects of Fetal Development Relating to Postnatal Fibre Production and Follicle Development in Ruminants
Bawden, C. S., Kleemann, D. O., McLaughlan, C. J., Nattrass, G. S., & Dunn, S. M. (2009) · Springer eBooks · doi:10.1007/978-90-481-3135-8_5 · Cited by 1
Can early protein restriction induce the development of binge eating?
Fechine, M. F., Borba, T. K. F., Cabral‐Filho, J. E., Bolaños, F. J., Lopes-de-Souza, S., & Manhães‐de‐Castro, R. (2016) · Behavioural Processes · doi:10.1016/j.beproc.2016.01.002 · Cited by 1
Prospect of potential intrauterine programming impacts associated with COVID-19
Khanal, P., & Duttaroy, A. K. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.986162 · Cited by 1
Maternofetal interaction and modulation in creating a new population: A review of current evidence on the relationship between fetal nutrition and the development of chronic diseases later in life
Novaković, I. V., Todorović, J., Dugalić, S., & Gojnić-Dugalić, M. (2023) · Srpski medicinski casopis Lekarske komore · doi:10.5937/smclk4-45480 · Cited by 1
Women, Biology, Obesity and Health: Implications of the Emerging Bioscience Research
Penny, S. (2013) · Bioenergetics Open access · doi:10.4172/2167-7662.1000106 · Cited by 1
Postnatal persistence of nonhuman primate sex‐dependent renal structural and molecular changes programmed by intrauterine growth restriction
Bishop, A. C., Spradling‐Reeves, K. D., Shade, R. E., Lange, K. J., Birnbaum, S., Favela, K. H., Dick, E. J., Nijland, M. J., Li, C., Nathanielsz, P. W., et al. (2022) · Journal of Medical Primatology · doi:10.1111/jmp.12601
Nutritionally Adequate Protein Sources in Diets During Gestation, Lactation and Weaning Influence Food Intake and the Risk of Characteristics of Metabolic Syndrome in Offspring of Wistar Rats
Jahan-Mihan, A. (2011) · TSpace (University of Toronto) · Cited by 1
Gender and Cardiovascular Disease in the Post-Genomic Era
Marı́n-Garcı́a, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-404599-6.00018-4
Prenatal glucocorticoid programming of 11-beta hydroxysteroid dehydrogenase type 2 and erythropoietin in the kidney
Tang, J. I.-S. (2011) · OpenGrey (Institut de l'Information Scientifique et Technique)
Baixo peso ao nascimento como marcador de alterações na pressão arterial e na microalbuminúria de crianças escolares
Salgado, C. M. (2008) · Americanae (AECID Library)
A influência do peso ao nascer sobre a pressão arterial e a composição corporal em crianças
Pereira, J. A. (2007) · doi:10.11606/d.6.2007.tde-05122007-134552
Divergent pathways of programming: prenatal vs. postnatal protein undernutrition
Alexander, B. T. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00448.2007
Maternal diet alters expression of specific PPARα transcripts in the hearts of their female offspring
Slater-Jefferies, J. L., Phillips, E. S., Lillycrop, K. A., Legg, G., Townsend, P. A., Hanson, M. A., & Burdge, G. C. (2008) · Proceedings of The Nutrition Society · doi:10.1017/s0029665108000293
The effect of an in utero high fat diet on the expression of transcription factors and glucose sensing in the developing rat pancreas
Cerf, M. E. (2005) · SUNScholar (Stellenbosch University)
Commentary: Early life determinants of blood pressure in childhood—where do we go from here?
Whincup, P. H., & Owen, C. G. (2006) · International Journal of Epidemiology · doi:10.1093/ije/dyl150
Programming Effects of Excess Glucocorticoid Exposure in Late Gestation
Moss, T. J. M., & Sloboda, D. M. (2007) · Springer eBooks · doi:10.1007/0-387-32632-4_14
SECTION 1: PERINATAL PROGRAMMING OF CHRONIC KIDNEY DISEASE Intrauterine Growth Restriction: Fetal Programming of Hypertension and Kidney Disease
Ojeda, N. B., Grigore, D., & Alexander, B. T. (2008)
Best Practice & Research Clinical Obstetrics and Gynaecology
Lee, V. C. Y., Ng, E. H. Y., Ho, P. C., & Block, P. (2010)
Developmental Origins of Adult Disease: Part 1: Cardiovascular Disease
Chan, P. Y. L., Morris, J. M., & Gallery, E. D. M. (2011) · NeoReviews · doi:10.1542/neo.12-12-e698
Avaliação morfoquantitativa do miocárdio de ratos Wistar submetidos à subnutrição proteica e à dieta padrão de Moçambique nos períodos pré e pós-natal
Ribeiro, L. D. S. (2016) · doi:10.11606/d.10.2016.tde-29032016-154617
Antenatal micronutrients in undernourished people
Krauss, R. M. (2008)
UNIVERSIDADE DE SÃO PAULO Faculdade de Ciências Farmacêuticas Programa de Pós-Graduação em Ciência dos Alimentos Área de Nutrição Experimental Suplementação com aminoácidos de cadeia ramificada atenua em proles os efeitos mediados pela dieta materna restrita em proteína
Fullin, G., & Teodoro, R. (2010)
Vascular and renal changes associated with hypertension in adult male rats exposed to maternal smoking during pregnancy
Bano, S. (2005) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/14386
Postnatal persistence of sex-dependent renal developmentally programmed structural and molecular changes in nonhuman primatesPreprint
Bishop, A. C., Spradling‐Reeves, K. D., Shade, R. E., Lange, K. J., Birnbaum, S., Favela, K. H., Dick, E. J., Nijland, M. J., Li, C., Nathanielsz, P. W., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.01.406355
How environmental exposures early in life might influence phenotypes of non-communicable diseases in Africa
Mirembe, M., Lule, S. A., & Nyirenda, M. (2020) · African Sun Media eBooks · doi:10.18820/9781928357759/08
The impact of different sources of fatty acids on the fetal programming of atherosclerosis
Gates, L. J. (2021) · Nottingham ePrints (University of Nottingham)
Maternal pre-pregnancy underweight as a risk factor for mother and child: analysis of the birth cohort Survey of Neonates in Pomerania IPreprint
Domanski, G., Lange, A. E., Ittermann, T., Fallenberg, J., Allenberg, H., Zygmunt, M., & Heckmann, M. (2020) · doi:10.21203/rs.3.rs-23082/v1
Suplementação com aminoácios de cadeia ramificada atenua em proles os efeitos mediados pela dieta materna restrita em proteína
Teodoro, G. F. R. (2011) · doi:10.11606/d.9.2011.tde-22122010-104816
Perinatal Programming and Blood Pressure
Ingelfinger, J. R. (2004) · Humana Press eBooks · doi:10.1007/978-1-59259-797-0_13
Abstracts of Original Communications (University of Leeds, Leeds, UK. 2–5 July 2002)
(2002) · Proceedings of The Nutrition Society · doi:10.1017/s0029665102000277
Pathophysiology of Primary Hypertension
Carey, R. M. (1984) · Comprehensive physiology · doi:10.1002/j.2040-4603.1984.tb01027.x
Maternal High-Salt Diet During Pregnancy in Sprague Dawley Rats Programs Exaggerated Stress-Induced Blood Pressure and Heart Rate Responses in Adult Female Offspring
King, S. H. (2007) · ScholarsArchive (Brigham Young University)
South Asian Cardiovascular Risk
Kalra, D. K., Vedamurthy, D., Hosadurg, N., Goyal, A., Gupta, M., Pagidipati, N., Slipczuk, L. N., Dey, D., Mehta, A., Joshi, P., et al. (2026) · JACC Asia · doi:10.1016/j.jacasi.2026.07.007

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Fetal programming of cardiovascular function through exposure to maternal undernutrition

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks