Abstract
Purpose
Epidemiological and experimental studies demonstrate that intrauterine growth restriction (IUGR) followed by accelerated postnatal growth leads to increased risk of developing cardiac disease in adulthood. The aim of this study was to examine the effect of early life growth restriction on cardiac structure and function in young adult rats.
Methods
IUGR was induced in Wistar Kyoto dams through administration of a low protein diet (LPD; 8.7 % casein) during pregnancy and lactation; controls received a normal protein diet (NPD; 20 % casein). Cardiac function and structure were assessed in female NPD (n = 7) and LPD (n = 7) offspring at 18 weeks of age by echocardiography and pressure–volume techniques, and systolic blood pressure by tail–cuff sphygmomanometry.
Results
LPD offspring remained significantly smaller throughout life compared to controls. There were no differences in the levels of systolic blood pressure, left ventricular cardiac dimensions, heart rate, ejection fraction and fractional shortening of the cardiac muscle between the investigated groups. Aortic peak systolic velocity was significantly reduced in the LPD group (P = 0.02).
Conclusion
Our findings support the idea that the programming of adult cardiovascular disease can be prevented or delayed in IUGR offspring when postnatal growth trajectory resembles that of in utero.
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References
Cosmi E, Fanelli T, Visentin S, Trevisanuto D, Zanardo V (2011) Consequences in infants that were intrauterine growth restricted. Journal of pregnancy 2011: 364381
McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633
Rich-Edwards JW, Stampfer MJ, Manson JE, Rosner B, Hankinson SE et al (1997) Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 315:396–400
Kaijser M, Bonamy AK, Akre O, Cnattingius S, Granath F et al (2008) Perinatal risk factors for ischemic heart disease: disentangling the roles of birth weight and preterm birth. Circulation 117:405–410
Camm EJ, Hansell JA, Kane AD, Herrera EA, Lewis C et al (2010) Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. Am J Obstet Gynecol 203(495):e424–e434
Elmes MJ, Gardner DS, Langley-Evans SC (2007) Fetal exposure to a maternal low-protein diet is associated with altered left ventricular pressure response to ischaemia-reperfusion injury. Br J Nutr 98:93–100
Ozaki T, Nishina H, Hanson MA, Poston L (2001) Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 530:141–152
Bol VV, Delattre AI, Reusens B, Raes M, Remacle C (2009) Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297:R291–R299
Eriksson JG, Forsen T, Tuomilehto J, Winter PD, Osmond C et al (1999) Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ 318:427–431
Hemachandra AH, Howards PP, Furth SL, Klebanoff MA (2007) Birth weight, postnatal growth, and risk for high blood pressure at 7 years of age: results from the Collaborative Perinatal Project. Pediatrics 119:e1264–e1270
Hermann GM, Miller RL, Erkonen GE, Dallas LM, Hsu E et al (2009) Neonatal catch up growth increases diabetes susceptibility but improves behavioral and cardiovascular outcomes of low birth weight male mice. Pediatr Res 66:53–58
Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. Lancet 2:577–580
Rotteveel J, van Weissenbruch MM, Twisk JW, Delemarre-Van de Waal HA (2008) Infant and childhood growth patterns, insulin sensitivity, and blood pressure in prematurely born young adults. Pediatrics 122:313–321
Eriksson JG (2007) Epidemiology, genes and the environment: lessons learned from the Helsinki Birth Cohort Study. J Intern Med 261:418–425
Barker DJ, Osmond C (1988) Low birth weight and hypertension. BMJ 297:134–135
Eriksson JG (2006) Early growth, and coronary heart disease and type 2 diabetes: experiences from the Helsinki Birth Cohort Studies. Int J Obes 30(Suppl 4):S18–S22
Lim K, Armitage JA, Stefanidis A, Oldfield BJ, Black MJ (2011) Intrauterine growth restriction in the absence of postnatal ‘catch-up’ growth leads to improved whole body insulin sensitivity in rat offspring. Pediatr Res 70:339–344
Lim K, Lombardo P, Schneider-Kolsky M, Hilliard LM, Denton KM et al (2011) Induction of hyperglycemia in adult intrauterine growth restricted rats: effects on renal function. Am J Physiol Renal Physiol 301:F299–F294
Zimanyi MA, Bertram JF, Black MJ (2004) Does a nephron deficit in rats predispose to salt-sensitive hypertension? Kidney Blood press Res 27:239–247
Zimanyi MA, Denton KM, Forbes JM, Thallas-Bonke V, Thomas MC et al (2006) A developmental nephron deficit in rats is associated with increased susceptibility to a secondary renal injury due to advanced glycation end-products. Diabetologia 49:801–810
Zohdi V, Jane Black M, Pearson JT (2011) Elevated vascular resistance and afterload reduce the cardiac output response to dobutamine in early growth-restricted rats in adulthood. Br J Nutr 106:1374–1382
Zohdi V, Wood BR, Pearson JT, Bambery KR, Black MJ (2013) Evidence of altered biochemical composition in the hearts of adult intrauterine growth-restricted rats. Eur J Nutr 52:749–758
Lim K, Zimanyi MA, Black MJ (2006) Effect of maternal protein restriction in rats on cardiac fibrosis and capillarization in adulthood. Pediatr Res 60:83–87
Wlodek ME, Westcott KT, O’Dowd R, Serruto A, Wassef L et al (2005) Uteroplacental restriction in the rat impairs fetal growth in association with alterations in placental growth factors including PTHrP. Am J Physiol Regul Integr Comp Physiol 288:R1620–R1627
Cingolani OH, Yang XP, Cavasin MA, Carretero OA (2003) Increased systolic performance with diastolic dysfunction in adult spontaneously hypertensive rats. Hypertension 41:249–254
Brown L, Fenning A, Chan V, Loch D, Wilson K et al (2002) Echocardiographic assessment of cardiac structure and function in rats. Heart Lung Circ 11:167–173
Boersma B, Wit JM (1997) Catch-up growth. Endocr Rev 18:646–661
Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E et al (2010) Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 121:2427–2436
Crispi F, Hernandez-Andrade E, Pelsers MM, Plasencia W, Benavides-Serralde JA et al (2008) Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses. Am J Obstet Gynecol 199(254):e251–e258
Fagerberg B, Bondjers L, Nilsson P (2004) Low birth weight in combination with catch-up growth predicts the occurrence of the metabolic syndrome in men at late middle age: the Atherosclerosis and Insulin Resistance study. J Intern Med 256:254–259
Forsen T, Eriksson J, Tuomilehto J, Reunanen A, Osmond C et al (2000) The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med 133:176–182
Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 320:967–971
Soto N, Bazaes RA, Pena V, Salazar T, Avila A et al (2003) 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. J Clin Endocrinol Metab 88:3645–3650
Lim K, Lombardo P, Schneider-Kolsky M, Black MJ (2012) Intrauterine growth restriction coupled with hyperglycemia: effects on cardiac structure in adult rats. Pediatr Res 72:344–351
Cheema KK, Dent MR, Saini HK, Aroutiounova N, Tappia PS (2005) Prenatal exposure to maternal undernutrition induces adult cardiac dysfunction. Br J Nutr 93:471–477
Acknowledgments
V. Zohdi was supported by an Australian Postgraduate Research Award whilst conducting this study. M. Kett was supported by a National Heart Foundation of Australia Career Development Fellowship (CRO7M3337).
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Zohdi, V., Pearson, J.T., Kett, M.M. et al. When early life growth restriction in rats is followed by attenuated postnatal growth: effects on cardiac function in adulthood. Eur J Nutr 54, 743–750 (2015). https://doi.org/10.1007/s00394-014-0752-6
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DOI: https://doi.org/10.1007/s00394-014-0752-6