Skip to main content Accessibility help
×
Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-23T14:09:18.986Z Has data issue: false hasContentIssue false

Chapter 7 - Intrauterine Growth Restriction

from Section 2 - Pregnancy, Labor, and Delivery Complications Causing Brain Injury

Published online by Cambridge University Press:  13 December 2017

David K. Stevenson
Affiliation:
Stanford University, California
William E. Benitz
Affiliation:
Stanford University, California
Philip Sunshine
Affiliation:
Stanford University, California
Susan R. Hintz
Affiliation:
Stanford University, California
Maurice L. Druzin
Affiliation:
Stanford University, California
Get access

Summary

Image of the first page of this content. For PDF version, please use the ‘Save PDF’ preceeding this image.'
Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2017

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.)

References

Rozance, PJ, Brown, LD, Thorn, SR, et al. Intrauterine growth restriction and the small-for-gestational-age infant. In MacDonald, MG, Seshia, MMK, eds., Avery’s Neonatology: Pathophysiology and Management of the Newborn, 7th edn. Philadelphia: Wolters Kluwer Health, 2015.Google Scholar
Smart, J. Undernutrition, learning and memory: review of experimental studies. In Taylor, TG, Jenkins, NK, eds. Proceedings of XII International Congress of Nutrition. London: John Libbey, 1986: 74.Google Scholar
Cruz-Martínez, R, Figueras, F, Hernandez-Andrade, E, et al. Fetal brain Doppler to predict cesarean delivery for nonreassuring fetal status in term small-for-gestational-age fetuses. Obstet Gynecol 2011; 117: 618–26.CrossRefGoogle ScholarPubMed
Simmons, RA, Gounis, AS, Bangalore, SA, Ogata, ES. Intrauterine growth retardation: fetal glucose transport is diminished in lung but spared in brain. Pediatr Res 1992; 32: 5963.Google Scholar
Poudel, R, McMillen, IC, Dunn, SL, et al. Impact of chronic hypoxemia on blood flow to the brain, heart, and adrenal gland in the late-gestation IUGR sheep fetus. Am J Physiol Regul Integr Comp Physiol 2015; 308: R151–62.CrossRefGoogle Scholar
Castillo-Melendez, M, Yawno, T, Allison, BJ, et al. Cerebrovascular adaptations to chronic hypoxia in the growth restricted lamb. Int J Dev Neurosci 2015; 29:ii.Google Scholar
Toft, PB, Leth, H, Ring, PB, et al. Volumetric analysis of the normal infant brain and in intrauterine growth retardation. Early Hum Dev 1995; 43: 1529.Google Scholar
Østgård, HF, Løhaugen, GC, Bjuland, KJ, et al. Brain morphometry and cognition in young adults born small for gestational age at term. J Pediatr 2014; 165: 921–7.Google Scholar
Lager, S, Powell, TL. Regulation of nutrient transport across the placenta. J Pregnancy 2012; 2012: 179827.Google Scholar
Gaccioli, F, Aye, IL, Roos, S, et al. Expression and functional characterisation of system L amino acid transporters in the human term placenta. Reprod Biol Endocrinol 2015; 9(13):57.Google Scholar
Lepercq, J, Hauguel De Mouzo, SJ. Leptin during pregnancy. Gynecol Obstet Biol Reprod (Paris) 2002; 31: 167–72.Google Scholar
Symonds, ME, Pope, M, Sharkey, D, Budge, H. Adipose tissue and fetal programming. Diabetologia 2012; 55: 1597–606.Google Scholar
Rosario, FJ, Schumacher, MA, Jiang, J, et al. Chronic maternal infusion of full-length adiponectin in pregnant mice down-regulates placental amino acid transporter activity and expression and decreases fetal growth. J Physiol 2012; 15(590): 1495–509.Google Scholar
Limesand, SW, Jensen, J, Hutton, JC, Hay, WW Jr. Diminished beta-cell replication contributes to reduced beta-cell mass in fetal sheep with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol 2005; 288: R1297–305.Google Scholar
Rozance, PJ, Anderson, M, Martinez, M, et al. Placental insufficiency decreases pancreatic vascularity and disrupts hepatocyte growth factor signaling in the pancreatic islet endothelial cell in fetal sheep. Diabetes 2015; 64: 555–64.CrossRefGoogle ScholarPubMed
Andrews, SE, Brown, LD, Thorn, SR, et al. Increased adrenergic signaling is responsible for decreased glucose-stimulated insulin secretion in the chronically hyperinsulinemic ovine fetus. Endocrinology 2015; 156: 367–76.Google Scholar
Fowden, Al. The insulin-like growth factors and feto-placental growth. Placenta 2003; 24(8–9): 803–12.Google Scholar
Ye, P, Carson, J, D’Ercole, AJ. In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J Neurosci 1995; 15: 7344.Google Scholar
Abuzzahab, MJ, Schneider, A, Goddard, A, et al. Intrauterine Growth Retardation (IUGR) Study Group. IFG-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med 2003; 349(23): 2211–22.Google Scholar
Baumann, MU, Schneider, H, Malek, A, et al. Regulation of human trophoblast GLUT1 glucose transporter by insulin-like growth factor I (IGF-I). PLoS One 2014; 9(8):e106037.Google Scholar
Sferruzzi-Perri, AN, Vaughan, OR, Forhead, AJ, Fowden, AL. Hormonal and nutritional drivers of intrauterine growth. Curr Opin Clin Nutr Metab Care 2013; 16: 298309.Google Scholar
Gressens, P, Hill, JM, Paindaveine, B, et al. Severe microcephaly induced by blockade of vasoactive intestinal peptide function in the primitive neuroepithelium of the mouse. J Clin Invest 1994; 94: 2020–7.Google Scholar
Nicolaides, KH, Economides, DL, Soothill, PW. Blood gases, pH, and lactate in appropriate- and small-for-gestational-age fetuses. Am J Obstet Gynecol 1989; 161: 9961001.Google Scholar
Scholl, TO, Hediger, ML, Schall, JI, et al. Maternal growth during pregnancy and the competition for nutrients. Am J Clin Nutr 1994; 60: 183–8.Google Scholar
Klein, JO, Baker, CJ, Remington, JS, et al. Current concepts of infection of the fetus and newborn infants. In Remington, JS, Klein, JO, Wilson, CB, Baker, CJ, eds., Infectious Diseases of the Fetus and Newborn Infant, 6th edn. Philadelphia: Elsevier Saunders, 2006: 125.Google Scholar
Kleigman, RM. Intrauterine growth restriction. In Fanaroff, AA, Martin, RJ, Walsh, MC, eds., Neonatal-Perinatal Medicine: Diseases of the Fetus and Infant, 5th edn. Philadelphia: Mosby Elsevier, 2006: 221306.Google Scholar
Ananth, CV, Friedman, AM. Ischemic placental disease and risks of perinatal mortality and morbidity and neurodevelopmental outcomes. Semin Perinatol 2014; 38: 151–8.Google Scholar
Roos, S, Powell, TL, Jansson, T. Placental mTOR links maternal nutrient availability to fetal growth. Biochem Soc Trans 2009; 37: 295–8.Google Scholar
Lumey, LH. Decreased birth weights in infants after maternal in utero exposure to the Dutch famine of 1944–1945. Paediatr Perinat Epidemiol 1992; 6: 240–53.Google Scholar
Catalano, PM, McIntyre, HD, Cruickshank, JK, et al. HAPO Study Cooperative Research Group. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care 2012; 35: 780–6.Google Scholar
Hernandez, TL, Van Pelt, RE, Anderson, MA, et al. A higher-complex carbohydrate diet in gestational diabetes mellitus achieves glucose targets and lowers postprandial lipids: a randomized crossover study. Diabetes Care 2014; 37: 1254–62.CrossRefGoogle ScholarPubMed
Crume, TL, Shapiro, AL, Brinton, JT, et al. Maternal fuels and metabolic measures during pregnancy and neonatal body composition: the healthy start study. J Clin Endocrinol Metab 2015; 100: 1672–80.Google Scholar
Ota, E, Mori, R, Middleton, P, et al. Zinc supplementation for improving pregnancy and infant outcome. Cochrane Database Syst Rev 2015; 2(2):CD000230.Google Scholar
Butterworth, RF. Maternal thiamine deficiency: still a problem in some world communities. Am J Clin Nutr 2001; 74: 712–13.Google Scholar
Conti, J, Abraham, S, Taylor, A. Eating behavior and pregnancy outcome. J Psychosom Res 1998; 44: 465–77.Google Scholar
Many, A, Fattal, A, Leitner, Y, et al. Neurodevelopmental and cognitive assessment of children born growth restricted to mothers with and without preeclampsia. Hypertens Pregnancy 2003; 22: 25–9.Google Scholar
Manuck, T, Branch, DW, Lai, Y, et al. Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Antiphospholipid antibodies and pregnancy outcomes in women heterozygous for factor V Leiden. J Reprod Immunol 2010; 85: 180–5.Google Scholar
Triche, EW, Hossain, N. Environmental factors implicated in the causation of diverse pregnancy outcome. Semin Perinatol 2007; 31: 240–2.Google Scholar
Blatt, K, Moore, E, Chen, A, et al. Association of reported trimester-specific smoking cessation with fetal growth restriction. Obstet Gynecol 2015; 125: 1452–9.Google Scholar
Kallen, K. Maternal smoking during pregnancy and infant head circumference at birth. Early Hum Dev 2000; 58: 197204.CrossRefGoogle ScholarPubMed
Carter, RC, Jacobson, JL, Sokol, RJ, et al. Fetal alcohol-related growth restriction from birth through young adulthood and moderating effects of maternal prepregnancy weight. Alcohol Clin Exp Res 2013; 37: 452–62.CrossRefGoogle ScholarPubMed
Little, BB, Snell, LM. Brain growth among fetuses exposed to cocaine in utero: asymmetrical growth retardation. Obstet Gynecol 1991; 77: 361–4.Google Scholar
Frank, DA, Bauchner, H, Parker, S, et al. Neonatal body proportionality and body composition after in utero exposure to cocaine and marijuana. J Pediatr 1990; 117: 622–6.Google Scholar
Christian, MS, Brent, RL. Teratogen update: evaluation of the reproductive and developmental risks of caffeine. Teratology 2001; 64: 5178.Google Scholar
Giussani, DA, Salinas, CE, Villena, M. The role of oxygen in prenatal growth: studies in the chick embryo. J Physiol 2007; 585: 911–17.Google Scholar
Milley, JR. Ovine fetal leucine kinetics and protein metabolism during decreased oxygen availability. Am J Physiol 1998; 274:e618–26.Google Scholar
Illsley, NP, Caniggia, I, Zamudio, S. Placental metabolic reprogramming: do changes in the mix of energy-generating substrates modulate fetal growth? Int J Dev Biol 2010; 54: 409–19.Google Scholar
Soria, R, Julian, CG, Vargas, E, et al. Graduated effects of high-altitude hypoxia and highland ancestry on birth size. Pediatr Res 2013; 74: 633–8.Google Scholar
Wilson, MJ, Lopez, M, Vargas, M, et al. Greater uterine artery blood flow during pregnancy in multigenerational (Andean) than shorter-term (European) high-altitude residents. Am J Physiol Regul Integr Comp Physiol 2007; 293: R1313–24.Google Scholar
Bennett, A, Sain, SR, Vargas, E, Moore, LG. The effect of heavy maternal workload on fetal growth retardation and preterm delivery: a study among southern Thai women. J Occup Environ Med 1998; 40: 1013–21.Google Scholar
Tuntiseranee, P, Geater, A, Chongsuvivatwong, V, Kor-anantakul, O. The effect of heavy maternal workload on fetal growth retardation and preterm delivery: a study among southern Thai women. J Occup Environ Med 1998; 40: 1013–21.Google Scholar
Koos, BJ, Longo, LD. Mercury toxicity in the pregnant woman, fetus, and newborn infant: a review. Am J Obstet Gynecol 1976; 126: 390409.Google Scholar
Albu, AR, Horhoianu, IA, Dumitrascu, MC, Horhoianu, V. Growth assessment in diagnosis of fetal growth restriction. J Med Life 2014; 5(7): 150–4.Google Scholar
Grivell, RM, Wong, L, Bhatia, V. Regimens of fetal surveillance for impaired fetal growth. Cochrane Database Syst Rev 2012; 6:CD007113.Google Scholar
Businelli, C, de Wit, C, Visser, GH, Pistorius, LR. Ultrasound evaluation of cortical brain development in fetuses with intrauterine growth restriction. J Matern Fetal Neonatal Med 2014; 10: 16.Google Scholar
Hershkovitz, R, Kingdom, JC, Geary, M, Rodeck, CH. Fetal cerebral blood flow redistribution in late gestation: identification of compromise in small fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2000; 15: 209–12.CrossRefGoogle ScholarPubMed
Flood, K, Unterscheider, J, Daly, S, et al. The role of brain sparing in the prediction of adverse outcomes in intrauterine growth restriction: results of the multicenter PORTO Study. Am J Obstet Gynecol 2014; 211(288):e15.Google Scholar
Cruz-Martinez, R, Tenorio, V, Padilla, N, et al. Risk of neonatal brain ultrasound abnormalities in intrauterine growth restricted fetuses born between 28 and 34 weeks: relationship with gestational age at birth and fetal Doppler. Ultrasound Obstet Gynecol 2015; 46:389–90.Google Scholar
Girardi, G. MRI-based methods to detect placental and fetal brain abnormalities in utero. J Reprod Immunol 2015; 2:pii: S01650378(15)00094–7.Google Scholar
Marconi, AM, Ronzoni, S, Vailati, S, et al. Neonatal morbidity and mortality in intrauterine growth restricted (IUGR) pregnancies is predicated upon prenatal diagnosis of clinical severity. Reprod Sci 2009; 16: 373–9.Google Scholar
Marconi, AM, Paolini, CL, Zerbe, G, Battaglia, FC. Lactacidemia in intrauterine growth restricted (IUGR) pregnancies: relationship to clinical severity, oxygenation and placental weight. Pediatr Res 2006; 59: 570–4.CrossRefGoogle ScholarPubMed
Regnault, TR, de Vrijer, B, Galan, HL, et al. Development and mechanisms of fetal hypoxia in severe fetal growth restriction. Placenta 2007; 28: 714–23.Google Scholar
Salihagić-Kadić, A, Medić, M, Jugović, D, et al. Fetal cerebrovascular response to chronic hypoxia: implications for the prevention of brain damage. J Matern Fetal Neonatal Med 2006; 19: 387–96.Google Scholar
Figueras, F, Eixarch, E, Meler, E, et al. Small-for-gestational-age fetuses with normal umbilical artery Doppler have suboptimal perinatal and neurodevelopmental outcome. Eur J Obstet Gynecol Reprod Biol 2008; 136: 34–8.Google Scholar
Bendapudi, P, Rao, GG, Greenough, A. Diagnosis and management of persistent pulmonary hypertension of the newborn. Paediatr Respir Rev. 2015; 16: 157–61.Google Scholar
Harris, DL, Weston, PJ, Harding, JE. Incidence of neonatal hypoglycemia in babies identified as at risk. J Pediatr 2012; 161: 787–91.Google Scholar
Hawdon, JM, Aynsley-Green, A, Ward Platt, MP. Neonatal blood glucose concentrations: metabolic effects of intravenous glucagon and intragastric medium chain triglyceride. Arch Dis Child 1993; 68: 255–61.Google Scholar
Limesand, SW, Rozance, PJ, Smith, D, Hay, WW Jr. Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction. Am J Physiol Endocrinol Metab 2007; 293: E1716–25.Google Scholar
van Kempen, AA, Ackermans, MT, Endert, E, et al. Glucose production in response to glucagon is comparable in preterm AGA and SGA infants. Clin Nutr 2005; 24: 727–36.Google Scholar
Arya, VB, Flanagan, SE, Kumaran, A, et al. Clinical and molecular characterization of hyperinsulinaemic hypoglycaemia in infants born small-for-gestational age. Arch Dis Child Fetal Neonatal Ed 2013; 98: F356–8.CrossRefGoogle ScholarPubMed
Macko, AR, Yates, DT, Chen, X, et al. Elevated plasma norepinephrine inhibits insulin secretion, but adrenergic blockade reveals enhanced β-cell responsiveness in an ovine model of placental insufficiency at 0.7 of gestation. J Dev Orig Health Dis 2013; 4: 402–10.Google Scholar
Gatford, KL, Simmons, RA. Prenatal programming of insulin secretion in intrauterine growth restriction. Clin Obstet Gynecol 2013; 56: 520–8.Google Scholar
Law, TL, Korte, JE, Katikaneni, LD, et al. Ultrasound assessment of intrauterine growth restriction: relationship to neonatal body composition. Am J Obstet Gynecol 2011; 205(255):e16.Google Scholar
Thorn, SR, Regnault, TRH, Brown, LD, et al. Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces hepatic and skeletal muscle mRNA translation initiation and nutrient sensing. Endocrinology 2009; 150: 3021–30.Google Scholar
Thorn, SR, Brown, LD, Rozance, PJ, et al. Increased hepatic glucose production in fetal sheep with intrauterine growth restriction is not suppressed by insulin. Diabetes 2013; 62: 6573.Google Scholar
Jain, A, Agarwal, R, Sankar, MJ, et al. Hypocalcemia in the newborn. Ind J Pediatr 2010; 77: 1123–8.Google Scholar
Bauer, J, Masin, M, Brodner, K. Resting energy expenditure and metabolic parameters in small for gestational age moderately preterm infants. Horm Res Paediatr 2011; 76: 202–7.Google Scholar
Glasser, I, Sutten, N, Schmeling, M, Machan, JT. A comprehensive study of umbilical cord blood cell developmental changes and reference ranges by gestation, gender and mode of delivery. J Perinatol 2015; 35: 469–75.Google Scholar
Basha, S, Surendran, N, Pichichero, M. Immune responses in neonates. Exp Rev Clin Immunol 2014; 10: 1171–84.Google Scholar
Kempley, S, Gupta, N, Linsell, L, et al. Feeding infants below 29 weeks’ gestation with abnormal antenatal Doppler: analysis from a randomised trial. Arch Dis Child Fetal Neonatal Ed. 2014; 99: F611.Google Scholar
Abdelmaaboud, M, Mohammed, A. Early versus late minimal enteral feeding in weeks preterm growth-restricted neonates with abnormal antenatal Doppler studies. J Matern Fetal Neonatal Med 2012 (epub ahead of print).Google Scholar
Leaf, A, Dorling, J, Kempley, S, et al. Abnormal Doppler Enteral Prescription Trial Collaborative Group. Early or delayed enteral feeding for preterm growth-restricted infants: a randomized trial. Pediatrics 2012; 129: e1260–8.Google Scholar
Pettigrew, AG, Edwards, DA, Henderson-Smart, DJ. The influence of intra-uterine growth retardation on brainstem development of preterm infants. Dev Med Child Neurol 1985; 27: 467–72.Google Scholar
Stanley, OH, Fleming, PJ, Morgan, MH. Development of visual evoked potentials following intrauterine growth retardation. Early Hum Dev 1991; 27: 7991.CrossRefGoogle ScholarPubMed
Scherjon, S, Briët, J, Oosting, H, Kok, J. The discrepancy between maturation of visual-evoked potentials and cognitive outcome at five years in very preterm infants with and without hemodynamic signs of fetal brain-sparing. Pediatrics 2000; 105: 385–91.Google Scholar
Nijhuis, IJ, ten Hof, J, Nijhuis, JG, et al. Temporal organization of fetal behavior from 24-weeks gestation onwards in normal and complicated pregnancies. Dev Psychobiol 1999; 34: 257–68.Google Scholar
Leventhal, JM, Berg, A, Egerter, SA. Is intrauterine growth retardation a risk factor for child abuse? Pediatrics 1987; 79: 515–19.Google Scholar
Watt, J. Interaction and development in the first year. II. The effects of intrauterine growth retardation. Early Hum Dev 1986; 13: 211–23.Google Scholar
Pallotto, EK, Killbride, HW. Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol 2006; 49: 257–69.Google Scholar
Ortibus, E, Lopriore, E, Deprest, J, et al. The pregnancy and long-term neurodevelopmental outcome of monochorionic diamniotic twin gestations: a multicenter prospective cohort study from the first trimester onward. Am J Obstet Gynecol 2009; 200(494):e18.Google Scholar
von Beckerath, AK, Kollmann, M, Rotky-Fast, C, et al. Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. Am J Obstet Gynecol 2013; 208(130):e16.Google Scholar
Levine, TA, Grunau, RE, McAuliffe, FM, et al. Early childhood neurodevelopment after intrauterine growth restriction: a systematic review. Pediatrics 2015; 135: 126–41.Google Scholar
Wang, Y, Fu, W, Liu, J. Neurodevelopment in children with intrauterine growth restriction: adverse effects and interventions. J Matern Fetal Neonatal Med 2015; 23: 19.Google Scholar
Murray, E, Fernandes, M, Fazel, M, et al. Differential effect of intrauterine growth restriction on childhood neurodevelopment: a systematic review. BJOG 2015; 122: 1062–72.Google Scholar
Casey, PH. Growth of low birth weight preterm children. Semin Perinatol 2008; 32: 20–7.Google Scholar
Rogne, T, Engstrøm, AA, Jacobsen, GW, et al. Fetal growth, cognitive function, and brain volumes in childhood and adolescence. Obstet Gynecol 2015; 125: 673–82.Google Scholar
McIntyre, S, Blair, E, Badawi, N, et al. Antecedents of cerebral palsy and perinatal death in term and late preterm singletons. Obstet Gynecol 2013; 122: 869–77.Google Scholar
Hack, M. Effects of intrauterine growth retardation on mental performance and behavior outcomes during adolescence and adulthood. Eur J Clin Nutr 1998; 52: S6570.Google Scholar
Yerushalmy-Feler, A, Marom, R, Peylan, T, et al. Electroencephalographic characteristics in preterm infants born with intrauterine growth restriction. J Pediatr 2014; 164: 756–61.Google Scholar
Simić Klarić, A, Kolundžić, Z, Galić, S. Language development inpreschool children born after asymmetrical intrautering growth retardation. Eur J Paediatr Neurol 2012; 16: 132–7.Google Scholar
Ortigosa Rocha, C, Bittar, RE, Zugaib, M. Neonatal outcomes of late-preterm birth associated or not with intrauterine growth restriction. Obstet Gynecol Int 2010; 2010: 231842.Google Scholar
Fattal-Valevski, A, Leitner, Y, Kutai, M, et al. Neurodevelopmental outcome in children with intrauterine growth retardation: a 3-year follow-up. J Child Neurol 1999; 14: 724–7.CrossRefGoogle ScholarPubMed
De Jesus, LC, Pappas, A, Shankaran, S, et al. Eunice Kennedy Shriver National Institute of Health and Human Development Neonatal Research Network. Outcomes of small for gestational age infants born at <27 weeks’ gestation. J Pediatr 2013; 163(55–60):e13.Google Scholar
Guellec, I, Lapillonne, A, Renolleau, S, et al. Neurologic outcomes at school age in very preterm infants born with severe or mild growth restriction. Pediatrics 2011; 127: e883–91.Google Scholar
Aucott, SW, Donohue, PK, Northington, FJ. Increased morbidity in severe early intrauterine growth restriction. J Perinatol 2004; 24: 435–40.CrossRefGoogle ScholarPubMed
Christian, P. Fetal growth restriction and preterm as determinants of child growth in the first two years and potential interventions. Nestle Nutr Inst Workshop Ser 2014; 78: 8191.Google Scholar
Baker, J, Workman, M, Bedrick, E, et al. Brains versus brawn: an empirical test of Barker’s brain sparing model. Am J Hum Biol 2010; 22: 206–15.Google Scholar
Basilious, A, Yager, J, Fehlings, MG. Neurological outcomes of animal models of uterine artery ligation and relevance to human intrauterine growth restriction: a systematic review. Dev Med Child Neurol 2015; 57: 420–30.Google Scholar
Piorkowska, K, Thompson, J, Nygard, K, et al. Synaptic development and neuronal myelination are altered with growth restriction in fetal guinea pigs. Dev Neurosci 2014; 36: 465–76.Google Scholar
Hack, M, Breslau, N, Weissman, B, et al. Effect of very low birth weight and subnormal head size on cognitive abilities at school age. N Engl J Med 1991; 325: 231–7.Google Scholar
Lundgren, EM, Tuvemo, T. Effects of being born small for gestational age on long-term intellectual performance. Best Pract Res Clin Endocrinol Metab. 2008; 22: 477–88.Google Scholar
Paz, I, Seidman, DS, Danon, YL, et al. Are children born small for gestational age at increased risk of short stature? Am J Dis Child 1993; 147: 337–9.Google Scholar
Bergvall, N, Iliadou, A, Johansson, S, et al. Risks for low intellectual performance related to being born small for gestational age are modified by gestational age. Pediatrics 2006; 117: e460–7.Google Scholar
Monset-Couchard, M, de Bethmann, O. Catch-up growth in 166 small-forgestational age premature infants weighing less than 1,000 g at birth. Biol Neonate 2000; 78: 161–7.CrossRefGoogle Scholar
de Bie, HM, de Ruiter, MB, Ouwendijk, M, et al. Using fMRI to investigate memory in young children born small for gestational age. PLoS One 2015; 1(10):e0129721.Google Scholar
Spinillo, A, Gardella, B, Preti, E, et al. Rates of neonatal death and cerebral palsy associated with fetal growth restriction among very low birth weight infants: a temporal analysis. BJOG 2006; 113: 775–80.Google Scholar
MacLennan, AH, Thompson, SC, Gecz, J. Cerebral palsy: causes, pathways, and the role of genetic variants. Am J Obstet Gynecol 2015; 213: 779–88.Google Scholar
Blair, EM, Nelson, KB. Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks’ gestation. Am J Obstet Gynecol 2015; 212(520):e17.Google Scholar
O’Callaghan, ME, MacLennan, AH, Gibson, CS, et al. Epidemiologic associations with cerebral palsy. Obstet Gynecol 2011; 118: 576–82.Google ScholarPubMed
Spence, D, Alderdice, FA, Stewart, MC, et al. Does intrauterine growth restriction affect quality of life in adulthood? Arch Dis Child 2007; 92: 700–3.Google Scholar
Geva, R, Eshel, R, Leitner, Y, et al. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics 2006; 118: 91100.CrossRefGoogle ScholarPubMed
Bergvall, N, Iliadou, A, Tuvemo, T, Cnattingius, S. Birth characteristics and risk of low intellectual performance in early adulthood: are the associations confounded by socioeconomic factors in adolescence or familial effects? Pediatrics 2006; 117: 714–21.CrossRefGoogle ScholarPubMed
Leonard, H, Nassar, N, Bourke, J, et al. Relation between intrauterine growth and subsequent intellectual disability in a ten-year population cohort of children in Western Australia. Am J Epidemiol 2008; 167: 103–11.Google Scholar
Leitner, Y, Fattal-Valevski, A, Geva, R, et al. Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol 2007; 22: 580–7.Google Scholar
Barker, DJ, Gluckman, PD, Godfrey, KM, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet 1993; 341: 938–41.Google Scholar
Gortner, L. Intrauterine growth restriction and risk for arterial hypertension: a causal relationship? J Perinat Med 2007; 35: 361–5.Google Scholar
Ong, TP, Ozanne, SE. Developmental programming of type 2 diabetes: early nutrition and epigenetic mechanisms. Curr Opin Clin Nutr Metab Care 2015; 18: 354–60.Google Scholar
Duque-Guimarães, DE, Ozanne, SE. Nutritional programming of insulin resistance: causes and consequences. Trends Endocrinol Metab 2013; 245: 525–35.Google Scholar
Forsén, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med 2000; 133: 176–82.Google Scholar
Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008; 359: 6173.Google Scholar
Sayer, AA, Syddall, H, Martin, H, et al. The developmental origins of sarcopenia. J Nutr Health Aging 2008; 12: 427–32.Google Scholar
Koklu, E, Ozturk, MA, Kurtoglu, S, et al. Aortic intima-media thickness, serum IGF-I, IGFBP-3, and leptin levels in intrauterine growth-restricted newborns of healthy mothers. Pediatr Res 2007; 62: 704–9.Google Scholar
Skilton, MR, Evans, N, Griffiths, KA, et al. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet 2005; 365: 1484–6.Google Scholar
Bloomfield, FH, Oliver, MH, Harding, JE. The late effects of fetal growth patterns. Arch Dis Child Fetal Neonatal Ed 2006; 91: F299304.Google Scholar
Barker, DJ, Eriksson, JG, Forsen, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 2002; 31: 1235–9.Google Scholar
Bujold, E, Roberge, S, Lacasse, Y, et al. Prevention of preeclampsia and intrauterine growth restriction with aspirin started in early pregnancy: a meta-analysis. Obstet Gynecol 2010; 116: 402–14.Google Scholar
Satterfield, MC, Bazer, FW, Spencer, TE, Wu, G. Sildenafil citrate treatment enhances amino acid availability in the conceptus and fetal growth in an ovine model of intrauterine growth restriction. J Nutr 2010; 140: 251–8.Google Scholar
de Boo, HA, Eremia, SC, Bloomfield, FH, et al. Treatment of intrautere growth restriction with maternal growth hormone supplementation in sheep. Am J Obstet Gynecol 2008; 199(599):e19.Google Scholar
Rozance, PJ, Limesand, SW, Barry, JS, et al. Glucose replacement to euglycemia causes hypoxia, acidosis, and decreased insulin secretion in fetal sheep with intrauterine growth restriction. Pediatr Res 2009; 65: 72–8.Google Scholar
Rush, D, Stein, Z, Susser, M. A randomized controlled trial of prenatal nutritional supplementation in New York City. Pediatrics 1980; 65: 683–97.Google Scholar
Ceesay, SM, Prentice, AM, Cole, TJ, et al. Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial. BMJ 1997; 315: 786–90.Google Scholar
Gulmezoglu, AM, Hofmeyr, GJ. Maternal nutrient supplementation for suspected impaired fetal growth. Cochrane Database Syst Rev 2000; 2: CD000148.Google Scholar
Catalano, PM, Thomas, AJ, Huston, LP, Fung, CM. Effect of maternal metabolism on fetal growth and body composition. Diabetes Care. 1998; 21(Suppl. 2):B8590.Google Scholar
Fernandez-Twinn, DS, Ozanne, SE. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav 2006; 88: 234–43.Google Scholar
Gulmezoglu, AM, Hofmeyr, GJ. Plasma volume expansion for suspected impaired fetal growth. Cochrane Database Syst Rev 2000; 2: CD000167.Google Scholar
Gulmezoglu, AM, Hofmeyr, GJ. Bed rest in hospital for suspected impaired fetal growth. Cochrane Database Syst Rev 2000; 2: CD000034.Google Scholar
Kinzler, WL, Kaminsky, L. Fetal growth restriction and subsequent pregnancy risks. Semin Perinatol 2007; 31: 126–34.Google Scholar
Brenner, B, Aharon, A. Thrombophilia and adverse pregnancy outcome. Clin Perinatol 2007; 34: 527–41.Google Scholar
Brown, LD, Green, AS, Limesand, SW, Rozance, PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci (Schol Ed) 2011; 3: 428–44.Google Scholar
Dusick, AM, Poindexter, BB, Ehrenkranz, RA, Lemons, JA. Growth failure in the preterm infant: can we catch up? Semin Perinatol 2003; 27: 302–10.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org 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
×