Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-5f56664f6-ldbxw Total loading time: 0 Render date: 2025-05-08T07:25:49.921Z Has data issue: false hasContentIssue false

21 - The role of vascular dysfunction in developmental origins of health and disease: evidence from human and animal studies

Published online by Cambridge University Press:  08 August 2009

By
Lucilla Poston ,
Christopher Torrens ,
James A. Armitage  and
Mark A. Hanson
Edited by
Peter Gluckman  and
Mark Hanson
Lucilla Poston
Affiliation:
King's College, London
Christopher Torrens
Affiliation:
University of Southampton
James A. Armitage
Affiliation:
King's College, London
Mark A. Hanson
Affiliation:
University of Southampton
Peter Gluckman
Affiliation:
University of Auckland
Mark Hanson
Affiliation:
University of Southampton
Get access

Summary

Introduction

Early studies in population cohorts proposed that perturbation of the environment in utero and in early life gives rise to marked and permanent alteration in offspring cardiovascular homeostasis, leading to increased risk of cardiovascular and metabolic disease in later life (reviewed in this volume). Clinical outcomes focused on the incidence of heart disease and hypertension in relation to birthweight, with little detailed investigation of other parameters of cardiovascular risk or outcome. More recent studies have given insight into underlying aetiological pathways, and the development of the different animal models of developmental plasticity has provided an opportunity to assess parameters of cardiovascular function at a depth which is not feasible, or indeed practicable, in humans.

The mechanisms contributing to cardiovascular homeostasis are complex and interwoven; they range from central control of the heart rate and vascular tone to paracrine, autocrine and genomic influences on the vascular smooth muscle and function of the endothelium. Fluid and volume homeostatic pathways, as well as the intricacy of haemostatic control, also contribute to the status quo. The complexity is such that common disorders such as essential hypertension remain poorly understood despite decades of research. The scientist wishing to investigate developmental programming of, for example, metabolic syndrome faces a bewildering choice of avenues to explore. Without a firm understanding of the early aetiology of hypertension or of insulin resistance, he or she has little choice but to follow the well-trodden paths which characterise research into these disorders in humans.

Type
Chapter
Information
Developmental Origins of Health and Disease , pp. 286 - 299
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Book purchase

Temporarily unavailable

References

Ahokas, R. A., Reynolds, S. L., Anderson, G. D. and Lipshitz, J. (1984). Maternal organ distribution of cardiac output in the diet-restricted pregnant rat. J. Nutr., 114, 2262–8.CrossRefGoogle ScholarPubMed
Anderson, T. J., Uehata, A., Gerhard, M. D.et al. (1995). Close relation of endothelial function in the human coronary and peripheral circulations. J. Am. Coll. Cardiol., 26, 1235–41.CrossRefGoogle ScholarPubMed
Armitage, J. A., Khan, I. Y., Taylor, P. D., Nathanielsz, P. W. and Poston, L. (2004a). Developmental programming of metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in animals?J. Physiol., 561, 355–77.CrossRefGoogle Scholar
Armitage, J. A., Jensen, R., Taylor, P. D. and Poston, L. (2004b). Exposure to a high fat diet during gestation and weaning results in reduced elasticity and endothelial function as well as altered gene expression and fatty acid content of rat aorta. J. Soc. Gynecol. Investig., 11, 183A.Google Scholar
Armitage, J. A., Ishibashi, A., Taylor, P. D. and Poston, L. (2004c). Developmental programming of aortic dysfunction by maternal fat-feeding does not persist to the second generation. J. Physiol., 565P, C165.Google Scholar
Barja-Fidalgo, C., Souza, E. P., Silva, S. V.et al. (2003). Impairment of inflammatory response in adult rats submitted to maternal undernutrition during early lactation: role of insulin and glucocorticoid. Inflamm. Res., 52, 470–6.CrossRefGoogle ScholarPubMed
Berry, C. L. and Looker, T. (1973). An alteration in the chemical structure of the aortic wall induced by a finite period of growth inhibition. J. Anat., 114, 83–94.Google ScholarPubMed
Black, H. R. (2004). The paradigm has shifted to systolic blood pressure. J. Hum. Hypertens., 18, S3–7.CrossRefGoogle ScholarPubMed
Boo, Y. C. and Jo, H. (2003). Flow-dependent regulation of endothelial nitric oxide synthase: role of protein kinases. Am. J. Physiol. Cell. Physiol., 285, C499–508.CrossRefGoogle ScholarPubMed
Brawley, L., Itoh, S., Torrens, C., Barker, A., Bertram, C., Poston, L. and Hanson, M. (2003). Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring. Pediatr. Res., 54, 83–90.CrossRefGoogle ScholarPubMed
Busse, R., Edwards, G., Feletou, M., Fleming, I., Vanhoutte, P. M. and Weston, A. H. (2002). EDHF: bringing the concepts together. Trends Pharmacol. Sci., 23, 374–80.CrossRefGoogle ScholarPubMed
Byberg, L., McKeigue, P. M., Zethelius, B. and Lithell, H. O. (2000). Birth weight and the insulin resistance syndrome: association of low birth weight with truncal obesity and raised plasminogen activator inhibitor-1 but not with abdominal obesity or plasma lipid disturbances. Diabetologia, 43, 54–60.CrossRefGoogle ScholarPubMed
Chan, N. and Vallance, P. (2002). Nitric oxide. In An Introduction to Vascular Biology (ed. Hunt, B., Poston, L., Schachter, M. and Halliday, A.). Cambridge: Cambridge University Press, pp. 216–58.CrossRefGoogle Scholar
Dance, C. S., Brawley, L., Dunn, R. L., Poston, L., Jackson, A. A. and Hanson, M. A. (2003). Folate supplementation of a protein restricted diet during pregnancy: restoration of vascular dysfunction in small mesenteric arteries of female adult rat offspring. Pediatr. Res., 53, 19A.Google Scholar
Dandrea, J., Cooper, S., Ramsay, M. M.et al. (2002). The effects of pregnancy and maternal nutrition on the maternal renin–angiotensin system in sheep. Exp. Physiol., 87, 353–9.CrossRefGoogle Scholar
Drake, A. J., Walker, B. R. and Seckl, J. R. (2005). Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R34–8.CrossRefGoogle ScholarPubMed
Edwards, L. J. and McMillen, I. C. (2001). Maternal undernutrition increases arterial blood pressure in the sheep fetus during late gestation. J. Physiol., 533, 561–70.CrossRefGoogle ScholarPubMed
Edwards, L. J., Bryce, A. E., Coulter, C. L. and McMillen, I. C. (2002). Maternal undernutrition throughout pregnancy increases adrenocorticotrophin receptor and steroidogenic acute regulatory protein gene expression in the adrenal gland of twin fetal sheep during late gestation. Mol. Cell. Endocrinol., 196, 1–10.CrossRefGoogle ScholarPubMed
Franco, M. C., Arruda, R. M., Dantas, A. P.et al. (2002). Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc. Res., 56, 145–53.CrossRefGoogle Scholar
Franco, M. C., Akamine, E. H., Di Marco, G. S.et al. (2003). NADPH oxidase and enhanced superoxide generation in intrauterine undernourished rats: involvement of the renin–angiotensin system. Cardiovasc. Res., 59, 767–75.CrossRefGoogle Scholar
Franco, M. C., Akamine, E. H., Fortes, Z. B.et al. (2004). Tetrahydrobiopterin improves endothelial dysfunction and vascular oxidative stress in microvessels of intrauterine undernourished rats. J. Physiol., 558, 239–48.CrossRefGoogle Scholar
Gardner, D. S., Pearce, S., Dandrea, J.et al. (2004). Peri-implantation undernutrition programs blunted angio-tensin II evoked baroreflex responses in young adult sheep. Hypertension, 43, 1290–6.CrossRefGoogle Scholar
Ghosh, P., Bitsanis, D., Ghebremeskel, K., Crawford, M. A. and Poston, L. (2001). Abnormal fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy. J. Physiol., 533, 815–22.CrossRefGoogle ScholarPubMed
Giussani, D. A., Spencer, J. A., Moore, P. J., Bennet, L. and Hanson, M. A. (1993). Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep. J. Physiol., 461, 431–49.CrossRefGoogle ScholarPubMed
Gluckman, P. D. and Hanson, M. A. (in press). Endothelial dysfunction and cardiovascular disease: the role of PARs. Heart.Google Scholar
Goh, K. L., Shore, A. C., Quinn, M. and Tooke, J. E. (2001). Impaired microvascular vasodilatory function in 3-month-old infants of low birth weight. Diabetes Care, 24, 1102–7.CrossRefGoogle ScholarPubMed
Goodfellow, J., Bellamy, N. F., Gorman, S. T.et al. (1998). Endothelial function is impaired in fit young adults of low birthweight. Cardiovasc. Res., 40, 600–6.CrossRefGoogle Scholar
Gopalakrishnan, G. S., Gardner, D. S., Rhind, S. M.et al. (2004). Programming of adult cardiovascular function after early maternal undernutrition in sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol., 287, R12–20.CrossRefGoogle Scholar
Goyal, H. O., Robateau, A., Braden, T. D., Williams, C. S., Srivastava, K. K. and Ali, K. (2003). Neonatal estrogen exposure of male rats alters reproductive functions at adulthood. Biol. Reprod., 68, 2081–91.CrossRefGoogle ScholarPubMed
Guo, F. and Jen, K. L. (1995). High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol. Behav., 57, 681–6.CrossRefGoogle ScholarPubMed
Halcox, J. P. J., Schenke, W. H., Zalos, G.et al. (2002). Prognostic value of coronary vascular endothelial dysfunction. Circulation, 106, 653–8.CrossRefGoogle ScholarPubMed
Hanson, M. A., Hawkins, P., Ozaki, T. et al. (1999). Effects of experimental dietary manipulation during early pregnancy on the cardiovascular and endocrine function in fetal sheep and young lambs. In Fetal Programming: Consequences for Health in Later Life (ed. Barker, D. J. P. and Wheeler, T.). London: RCOG Press, pp. 365–73.Google Scholar
Hawkins, P., Steyn, C., McGarrigle, H. H.et al. (1999). Effect of maternal nutrient restriction in early gestation on development of the hypothalamic–pituitary–adrenal axis in fetal sheep at 0.8–0.9 of gestation. J. Endocrinol., 163, 553–61.CrossRefGoogle ScholarPubMed
Hawkins, P., Steyn, C., Ozaki, T., Saito, T., Noakes, D. E. and Hanson, M. A. (2000a). Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes. Am. J. Physiol. Regul. Integr. Comp. Physiol., 279, R340–8.CrossRefGoogle Scholar
Hawkins, P., Steyn, C., McGarrigle, H. H.et al. (2000b). Cardiovascular and hypothalamic–pituitary–adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod. Fertil. Dev., 12, 443–56.CrossRefGoogle Scholar
Holemans, K., Gerber, R., Meurrens, K., De, Clerck, F., Poston, L. and Assche, F. A. (1999). Maternal food restriction in the second half of pregnancy affects vascular function but not blood pressure of rat female offspring. Br. J. Nutr., 81, 73–9.Google Scholar
Hsueh, W. A., Lyon, C. J. and Quinones, M. J. (2004). Insulin resistance and endothelium. Am. J. Med., 117, 109–17.CrossRefGoogle ScholarPubMed
Hunt, B. J. and Jurd, K. M. (2002). The endothelium in health and disease. In An Introduction to Vascular Biology (ed. Hunt, B., Poston, L., Schachter, M. and Halliday, A.). Cambridge: Cambridge University Press, pp. 186–215.CrossRefGoogle Scholar
Ijzerman, R. G., Weissenbruch, M. M., Voordouw, J. J.et al. (2002). The association between birth weight and capillary recruitment is independent of blood pressure and insulin sensitivity: a study in prepurbertal children. J. Hypertens., 20, 1957–63.CrossRefGoogle Scholar
Ijzerman, R. G., Stehouwer, C. D., Geus, E. J., Kluft, C. and Boomsma, D. I. (2003). The association between birth weight and plasma fibrinogen is abolished after the elimination of genetic influencesJ. Thromb. Haemost., 1, 239–42.CrossRefGoogle ScholarPubMed
Intengan, H. D., Thibault, G., Li, J. S. and Schiffrin, E. L. (1999). Resistance artery mechanics, structure, and extracellular components in spontaneously hypertensive rats: effects of angiotensin receptor antagonism and converting enzyme inhibition. Circulation, 100, 2267–75.CrossRefGoogle ScholarPubMed
Irving, R. J., Shore, A. C., Belton, N. R., Elton, R. A., Webb, D. J. and Walker, B. R. (2004). Low birth weight predicts higher blood pressure but not dermal capillary density in two populations. Hypertension, 43, 610–13.CrossRefGoogle Scholar
Kaati, G., Bygren, L. O. and Edvinsson, S. (2002). Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur. J. Hum. Genet., 10, 682–8.CrossRefGoogle ScholarPubMed
Karnik, H. B., Sonawane, B. R., Adkins, J. S. and Mohla, S. (1989). High dietary fat feeding during perinatal development of rats alters hepatic drug metabolism of progeny. Dev. Pharmacol. Ther., 14, 135–40.Google ScholarPubMed
Khan, I. Y., Taylor, P. D., Dekou, V.et al. (2003). Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension, 41, 168–75.CrossRefGoogle ScholarPubMed
Khan, I. Y., Dekou, V., Hanson, M., Poston, L. and Taylor, P. (2004). Predictive adaptive responses to maternal high fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation, 110, 1097–102.CrossRefGoogle Scholar
Khan, I. Y., Dekou, V., Douglas, G.et al. (2005). A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R127–33.CrossRefGoogle ScholarPubMed
Kind, K. L., Simonetta, G., Clifton, P. M., Robinson, J. S. and Owens, J. A. (2002). Effect of maternal feed restriction on blood pressure in the adult guinea pig. Exp. Physiol., 87, 469–77.CrossRefGoogle ScholarPubMed
Kind, K. L., Clifton, P. M., Grant, P. A.et al. (2003). Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am. J. Physiol. Regul. Integr. Comp. Physiol., 284, R140–52.CrossRefGoogle ScholarPubMed
Kingwell, B. A. and Gatzka, C. D. (2002). Aterial stiffness and prediction of cardiovascular risk. J. Hypertens., 20, 2337–40.CrossRefGoogle Scholar
Kumeran, K., Fall, C., Martyn, C. N., Vijayakumar, M., Stein, C. and Shier, R. (2000). Blood pressure, arterial compliance and left ventricular mass: no relation to small size at birth in south Indian adults. Heart, 83, 272–7.CrossRefGoogle Scholar
Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C. and Fleming, T. P. (2000). Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development, 127, 4195–202.Google ScholarPubMed
Lamireau, D., Nuyt, A. M., Hou, X.et al. (2002). Altered vascular function in fetal programming of hypertension. Stroke, 33, 2992–8.CrossRefGoogle ScholarPubMed
Landmesser, U., Hornig, B. and Drexler, H. (2004). Endothelial function: a critical determinant in atherosclerosis?Circulation, 109, 27–33.CrossRefGoogle ScholarPubMed
Langley, S. C. and Jackson, A. A. (1994). Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin. Sci., 86, 217–22.CrossRefGoogle ScholarPubMed
Langley-Evans, S. C. (1996). Intrauterine programming of hypertension in the rat: nutrient interactions. Comp. Biochem. Physiol. A Physiol., 114, 327–33.CrossRefGoogle ScholarPubMed
Langley-Evans, S. C. and Jackson, A. A. (1995). Captopril normalises systolic blood pressure in rats with hypertension induced by fetal exposure to maternal low protein diets. Comp. Biochem. Physiol. A. Physiol., 110, 223–8.CrossRefGoogle ScholarPubMed
Langley-Evans, S. C., Welham, S. J. and Jackson, A. A. (1999). Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci., 64, 965–74.CrossRefGoogle ScholarPubMed
Leeson, C. P., Whincupp, P. H., Cook, D. G.et al. (1997). Flow-mediated dilatation in 9–11 year old children: the influence of intrauterine and childhood factors. Circulation, 96, 2233–8.CrossRefGoogle Scholar
Leeson, C. P., Katternhorm, M., Morley, R., Lucas, A. and Deanfield, J. E. (2001a). Impact of low birthweight and cardiovascular risk factors on endothelial function in early adult life. Circulation, 103, 1264–8.CrossRefGoogle Scholar
Leeson, C. P., Katternhorm, M., Deanfield, J. E. and Lucas, A. (2001b). Duration of breast feeding and arterial distensibility in early life: population based study. BMJ, 332, 643–7.CrossRefGoogle Scholar
Lesage, J., Blondeau, B., Grino, M., Breant, B. and Dupouy, J. P. (2001). Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology, 142, 1692–702.CrossRefGoogle ScholarPubMed
Libby, P. (2002). Inflammation and atherosclerosis. Nature, 420, 868–74.CrossRefGoogle Scholar
Lillycrop, K. A., Phillips, G. S., Jackson, A. A., Hanson, M. A. and Burdge, G. C. (2005). Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J. Nutr., 135, 1382–6.CrossRefGoogle ScholarPubMed
Martin, H., Hu, J., Gennser, G. and Norman, M. (2000). Impaired endothelial function and increased carotid stiffness in 9-year old children with low birthweight. Circulation, 102, 2739–44.CrossRefGoogle ScholarPubMed
Martyn, C. N. and Greenwald, S. E. (1997). Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertension. Lancet, 350, 953–5.CrossRefGoogle Scholar
Martyn, C. N., Meade, T. W., Stirling, Y. and Barker, D. J. P. (1995a). Plasma concentrations of fibrinogen and factor VII in adult life and their relation to intra-uterine growth. Br. J. Haematol., 89, 142–6.CrossRefGoogle Scholar
Martyn, C. N., Barker, D. J. P., Jespersen, S., Greenwald, S., Osmond, C. and Berry, C. (1995b). Growth in utero, adult blood pressure, and arterial compliance. Br. Heart J., 73, 116–21.CrossRefGoogle Scholar
McAllister, A. S., Atkinson, A. B., Johnston, G. D. and McCance, D. R. (1999). Relationship of endothelial function to birth weight in humans. Diabetes Care, 22, 2061–6.CrossRefGoogle ScholarPubMed
McMullen, S., Gardner, D. S. and Langley-Evans, S. C. (2004). Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br. J. Nutr., 91, 133–40.CrossRefGoogle ScholarPubMed
McVeigh, G. E., Brennan, G. M., Johnston, G. D.et al. (1992). Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia, 35, 771–6.Google ScholarPubMed
Meigs, J. B., Hu, F. B., Rifai, N. and Manson, J. E. (2004). Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus. JAMA, 291, 1978–86.CrossRefGoogle ScholarPubMed
Merezak, S., Reusens, B., Renard, A.et al. (2004). Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia, 47, 669–75.Google ScholarPubMed
Molnar, J., Howe, D. C., Nijland, M. J. and Nathanielsz, P. W. (2003). Prenatal dexamethasone leads to both endothelial dysfunction and vasodilatory compensation in sheep. J. Physiol., 547, 61–6.CrossRefGoogle Scholar
Montgomery, A. A., Ben-Sholmo, Y., McCarthy, A., Davies, D., Elwood, P. and Smith, G. D. (2000). Birth size and arterial compliance in young adults. Lancet, 355, 2136–7.CrossRefGoogle ScholarPubMed
Morgan, H. D., Sutherland, H. G., Martin, D. I. and Whitelaw, E. (1999). Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet., 23, 314–18.CrossRefGoogle ScholarPubMed
Napoli, C., Witztum, J. L., Calara, F., Nigris, F. and Palinski, W. (2000). Maternal hypercholesterolemia enhances atherogenesis in normocholesterolemic rabbits, which is inhibited by antioxidant or lipid-lowering intervention during pregnancy: an experimental model of atherogenic mechanisms in human fetuses. Circ. Res., 87, 946–52.CrossRefGoogle ScholarPubMed
Nishina, H., Green, L. R., McGarrigle, H. H., Noakes, D. E., Poston, L. and Hanson, M. A. (2003). Effect of nutritional restriction in early pregnancy on isolated femoral artery function in mid-gestation fetal sheep. J. Physiol., 553, 637–47.CrossRefGoogle ScholarPubMed
Norman, J. F., and LeVeen, R. F. (2001). Maternal atherogenic diet in swine is protective against early atherosclerosis development in offspring consuming an atherogenic diet post-natally. Atherosclerosis, 157, 41–7.CrossRefGoogle ScholarPubMed
Norman, M. and Martin, H. (2003). Preterm birth attenuates association between low birthweight and endothelial dysfunction. Circulation, 108, 996–1001.CrossRefGoogle ScholarPubMed
Owens, G. K., Kumar, M. S. and Wamhoff, B. R. (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev., 84, 767–801.CrossRefGoogle ScholarPubMed
Ozaki, T., Nishina, H., Hanson, M. A. and Poston, L. (2001). Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J. Physiol., 530, 141–52.CrossRefGoogle ScholarPubMed
Palinski, W., Armiento, D' F. P., Witztum, J. L.et al. (2001). Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ. Res., 89, 991–6.CrossRefGoogle ScholarPubMed
Panza, J. A., Casino, P. R., Kilcoyne, C. M. and Quyyumi, A. A. (1993). Role of endothelium-derived nitric oxide in the abnormal endothelium-dependent vascular relaxation of patients with essential hypertension. Circulation, 87, 1468–74.CrossRefGoogle ScholarPubMed
Phillips, D. I. and Barker, D. J. P. (1997). Association between low birthweight and high resting pulse in adult life: is the sympathetic nervous system involved in programming the insulin resistance syndrome. Diabet. Med., 14, 673–7.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Rakyan, V. K., Chong, S., Champ, M. E.et al. (2003). Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission. Proc. Nat. Acad. Sci. USA, 100, 2538–43.CrossRefGoogle Scholar
Rees, W. D., Hay, S. M., Brown, D. S., Antipatis, C. and Palmer, R. M. (2000). Maternal protein deficiency causes hypermethylation of DNA in the livers of rat fetuses. J. Nutr., 130, 1821–6.CrossRefGoogle ScholarPubMed
Resnick, O. and Morgane, P. J. (1983). Animal models for small-for-gestational-age (SGA) neonates and infants-at-risk (IAR). Brain Res., 312, 221–5.CrossRefGoogle Scholar
Rosso, P. and Kava, R. (1980). Effects of food restriction on cardiac ouput and blood flow to the uterus and placenta in the pregnant rat. J. Nutr., 110, 2350–4.CrossRefGoogle ScholarPubMed
Rosso, P. and Streeter, M. R. (1979). Effects of food or protein restriction on plasma volume expansion in pregnant rats. J. Nutr., 109, 1887–92.CrossRefGoogle ScholarPubMed
Ruijtenbeek, K., Noble, F. A., Janssen, G. M.et al. (2000). Chronic hypoxia stimulates periarterial sympathetic nerve development in chicken embryo. Circulation, 102, 2892–7.CrossRefGoogle ScholarPubMed
Ruijtenbeek, K., Kessels, L. C., De, Mey, J. G. and Blanco, C. E. (2003). Chronic moderate hypoxia and protein malnutrition both induce growth retardation, but have distinct effects on arterial endothelium-dependent reactivity in the chicken embryo. Pediatr. Res., 53, 573–9.CrossRefGoogle ScholarPubMed
Sattar, N., McConnachie, A., Reilly, O' D.et al. (2004). Inverse association between birth weight and C-reactive protein concentrations in the MIDSPAN Family Study. Arterioscler. Thromb. Vasc. Biol., 24, 583–7.CrossRefGoogle ScholarPubMed
Sherman, R. C. and Langley-Evans, S. C. (2000). Antihypertensive treatment in early postnatal life modulates prenatal dietary influences upon blood pressure in the rat. Clin. Sci., 98, 269–75.CrossRefGoogle ScholarPubMed
Siemelink, M., Verhoef, A., Dormans, J. A., Span, P. N. and Piersma, A. H. (2002). Dietary fatty acid composition during pregnancy and lactation in the rat programs growth and glucose metabolism in the offspring. Diabetologia, 45, 1397–403.Google ScholarPubMed
Simpson, S. J., Batley, R. and Raubenheimer, D. (2003). Geometric analysis of macronutrient intake in humans: the power of protein?Appetite 41, 123–40.CrossRefGoogle ScholarPubMed
Singhal, A. and Lucas, A. (2004). Early origins of cardiovascular disease: is there a unifying hypothesis?Lancet, 363, 1642–5.CrossRefGoogle Scholar
Singhal, A., Cole, T. J., Fewtrell, M. and Lucas, A. (2004a). Breastmilk feeding and lipoprotein profile in adolescents born preterm: follow-up of a prospective randomised study. Lancet, 15, 1571–8.CrossRefGoogle Scholar
Singhal, A., Cole, T. J. and Fewtrell, M., Deanfield, J. and Lucas, A. (2004b). Is slower early growth beneficial for long term cardiovascular health?Circulation, 109, 1108–13.CrossRefGoogle Scholar
Szmitko, P. E., Wang, C. H., Weisel, R. D.et al. (2003a). New markers of inflammation and endothelial cell activation. Circulation, 108, 1917–23.CrossRefGoogle Scholar
Szmitko, P. E., Wang, C. H., Weisel, R. D., Jeffries, G. A., Anderson, T. J. and Verma, S. (2003b). Biomarkers of vascular disease linking inflammation to endothelial activation. Circulation, 108, 2041–48.CrossRefGoogle Scholar
Taylor, P. D., McConnell, J., Khan, I. Y.et al. (2004a). Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R134–9.CrossRefGoogle Scholar
Taylor, P. D., Khan, I. Y., Hanson, M. A. and Poston, L. (2004b). Impaired EDHF-mediated vasodilatation in adult offspring of rats exposed to a fat-rich diet in pregnancy. J. Physiol., 558, 943–51.CrossRefGoogle Scholar
Te Velde, S. J., Ferreira, I., Twisk, J. W., Stehouwer, C. D., Mechelen, W. and Kemper, H. C. (2004). Birthweight and arterial stiffness and blood pressure in adulthood: results from the Amsterdam Growth and Health Longitudinal Study. Int. J. Epidemiol., 33, 154–61.CrossRefGoogle ScholarPubMed
Tonkiss, J., Trzcinska, M., Galler, J. R., Ruiz-Opazo, N. and Herrera, V. L. (1998). Prenatal malnutrition-induced changes in blood pressure: dissociation of stress and nonstress responses using radiotelemetry. Hypertension, 32, 108–14.CrossRefGoogle ScholarPubMed
Torrens, C., Brawley, L., Dance, C. S, Itoh, S., Poston, L. and Hanson, M. A. (2002). First evidence for transgenerational vascular programming in the rat protein restriction model. J. Physiol., 543P, 41P.Google Scholar
Torrens, C., Brawley, L., Barker, A. C., Itoh, S., Poston, L. and Hanson, M. A. (2003). Maternal protein restriction in the rat impairs resistance artery but not conduit artery function in pregnant offspring. J. Physiol., 547, 77–84.CrossRefGoogle Scholar
Vickers, M. H., Breier, B. H., Cutfield, W. S., Hofman, P. L. and Gluckman, P. D. (2000). Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am. J. Physiol. Endocrinol. Metab., 279, E83–7.CrossRefGoogle ScholarPubMed
Wadsworth, R. M. (1990). Calcium and vascular reactivity in aging and hypertension. J. Hypertens., 8, 975–83.CrossRefGoogle ScholarPubMed
Walker, B. R., McConnachie, A., Noon, J. P., Webb, D. J. and Watt, G. C. (1998). Contribution of parental blood pressures to association between low birth weight and adult high blood pressure: cross sectional study. BMJ, 316, 834–7.CrossRefGoogle ScholarPubMed
Waterland, R. A. and Jirtle, R. L. (2004). Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition, 20, 63–8.CrossRefGoogle ScholarPubMed
Woodall, S. M., Johnston, B. M., Breier, B. H. and Gluckman, P. D. (1996). Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr. Res., 40, 438–43.CrossRefGoogle ScholarPubMed
Woods, L. L., Ingelfinger, J. R., Nyengaard, J. R. and Rasch, R. (2001). Maternal protein restriction suppresses the newborn renin–angiotensin system and programs adult hypertension in rats. Pediatr. Res., 49, 460–7.CrossRefGoogle ScholarPubMed
Young, J. B., Kaufman, L. N., Saville, M. E. and Landsberg, L. (1985). Increased sympathetic nervous system activity in rats fed a low-protein diet. Am. J. Physiol., 248, R627–37.Google ScholarPubMed
Yu, H. I., Sheu, W. H., Lai, C. J., Lee, W. J. and Chen, Y. T. (2001). Endothelial dysfunction in type 2 diabetes mellitus subjects with peripheral artery disease. Int. J. Cardiol., 78, 19–25.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×