Neonatal and Long-Term Consequences of Fetal Growth Restriction

Marina Colella, Alice Frérot, Aline Rideau Batista Novais, Olivier Baud, Marina Colella, Alice Frérot, Aline Rideau Batista Novais, Olivier Baud

Abstract

Background: Fetal Growth Restriction (FGR) is one of the most common noxious antenatal conditions in humans, inducing a substantial proportion of preterm delivery and leading to a significant increase in perinatal mortality, neurological handicaps and chronic diseases in adulthood. This review summarizes the current knowledge about the postnatal consequences of FGR, with a particular emphasis on the long-term consequences on respiratory, cardiovascular and neurological structures and functions.

Result and conclusion: FGR represents a global health challenge, and efforts are urgently needed to improve our understanding of the critical factors leading to FGR and subsequent insults to the developing organs.

Keywords: FGR; diseases; long-term handicap; maternal malnutrition; neonatal brain injury; perinatal mortality..

Copyright© Bentham Science Publishers; For any queries, please email at epub@benthamscience.net.

References

    1. Jarvis S., Glinianaia S.V., Torrioli M-G., et al. Cerebral palsy and intrauterine growth in single births: European collaborative study. Lancet. 2003;362(9390):1106–1111.
    1. Gordijn S.J., Beune I.M., Ganzevoort W. Building consensus and standards in fetal growth restriction studies. Best Pract. Res. Clin. Obstet. Gynaecol. 2018;49:117–126.
    1. Lausman A., Kingdom J., Gagnon R., et al. Intrauterine growth restriction: screening, diagnosis, and management. J. Obstet. Gynaecol. Can. 2013;35(8):741–748.
    1. de Onis M., Blössner M., Villar J. Levels and patterns of intrauterine growth retardation in developing countries. Eur. J. Clin. Nutr. 1998;52(Suppl. 1):S5–S15.
    1. Frøen J.F., Gardosi J.O., Thurmann A., Francis A., Stray-Pedersen B. Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet. Gynecol. Scand. 2004;83(9):801–807.
    1. Zeitlin J., Szamotulska K., Drewniak N., et al. Preterm birth time trends in Europe: A study of 19 countries. BJOG. 2013;120(11):1356–1365.
    1. Katz J., Lee A.C., Kozuki N., et al. Mortality risk in preterm and small-for-gestational-age infants in low-income and middle-income countries: A pooled country analysis. Lancet. 2013;382(9890):417–425.
    1. Ergaz Z., Avgil M., Ornoy A. Intrauterine growth restriction-etiology and consequences: What do we know about the human situation and experimental animal models? Reprod. Toxicol. 2005;20(3):301–322.
    1. Marzouk A., Filipovic-Pierucci A., Baud O., et al. Prenatal and post-natal cost of small for gestational age infants: A national study. BMC Health Serv. Res. 2017;17(1):221.
    1. Burri P.H. Structural aspects of postnatal lung development - alveolar formation and growth. Biol. Neonate. 2006;89(4):313–322.
    1. Dezateux C., Lum S., Hoo A-F., Hawdon J., Costeloe K., Stocks J. Low birth weight for gestation and airway function in infancy: exploring the fetal origins hypothesis. Thorax. 2004;59(1):60–66.
    1. Bose C., Van Marter L.J., Laughon M., et al. Fetal growth restriction and chronic lung disease among infants born before the 28th week of gestation. Pediatrics. 2009;124(3):e450–e458.
    1. Eriksson L., Haglund B., Odlind V., Altman M., Ewald U., Kieler H. Perinatal conditions related to growth restriction and inflammation are associated with an increased risk of bronchopulmonary dysplasia. Acta Paediatr. 2015;104(3):259–263.
    1. Zeitlin J., El Ayoubi M., Jarreau P-H., et al. Impact of fetal growth restriction on mortality and morbidity in a very preterm birth cohort. J. Pediatr. 2010;157(5):733–739.
    1. Greenough A., Yuksel B., Cheeseman P. Effect of in utero growth retardation on lung function at follow-up of prematurely born infants. Eur. Respir. J. 2004;24(5):731–733.
    1. Pike K.C., Crozier S.R., Lucas J.S.A., et al. Patterns of fetal and infant growth are related to atopy and wheezing disorders at age 3 years. Thorax. 2010;65(12):1099–1106.
    1. Morsing E., Gustafsson P., Brodszki J. Lung function in children born after foetal growth restriction and very preterm birth. Acta Paediatr. 2012;101(1):48–54.
    1. Ronkainen E., Dunder T., Kaukola T., Marttila R., Hallman M. Intrauterine growth restriction predicts lower lung function at school age in children born very preterm. Arch. Dis. Child. Fetal Neonatal Ed. 2016;101(5):F412–F417.
    1. Kotecha S.J., Watkins W.J., Henderson A.J., Kotecha S. The effect of birth weight on lung spirometry in white, school-aged children and adolescents born at term: A longitudinal population based observational cohort study. J. Pediatr. 2015;166(5):1163–1167.
    1. Gortner L. Intrauterine growth restriction and risk for arterial hypertension: A causal relationship? J. Perinat. Med. 2007;35(5):361–365.
    1. Chen C-M., Wang L-F., Su B. Effects of maternal undernutrition during late gestation on the lung surfactant system and morphometry in rats. Pediatr. Res. 2004;56(3):329–335.
    1. Maritz G.S., Cock M.L., Louey S., Suzuki K., Harding R. Fetal growth restriction has long-term effects on postnatal lung structure in sheep. Pediatr. Res. 2004;55(2):287–295.
    1. Karadag A., Sakurai R., Wang Y., et al. Effect of maternal food restriction on fetal rat lung lipid differentiation program. Pediatr. Pulmonol. 2009;44(7):635–644.
    1. Maritz G.S., Cock M.L., Louey S., Joyce B.J., Albuquerque C.A., Harding R. Effects of fetal growth restriction on lung development before and after birth: A morphometric analysis. Pediatr. Pulmonol. 2001;32(3):201–210.
    1. Joss-Moore L.A., Albertine K.H., Lane R.H. Epigenetics and the developmental origins of lung disease. Mol. Genet. Metab. 2011;104(1-2):61–66.
    1. Rehan V.K., Sakurai R., Li Y., et al. Effects of maternal food restriction on offspring lung extracellular matrix deposition and long term pulmonary function in an experimental rat model. Pediatr. Pulmonol. 2012;47(2):162–171.
    1. O’Brien E.A., Barnes V., Zhao L., et al. Uteroplacental insufficiency decreases p53 serine-15 phosphorylation in term IUGR rat lungs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007;293(1):R314–R322.
    1. Rozance P.J., Seedorf G.J., Brown A., et al. Intrauterine growth restriction decreases pulmonary alveolar and vessel growth and causes pulmonary artery endothelial cell dysfunction in vitro in fetal sheep. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011;301(6):L860–L871.
    1. Joyce B.J., Louey S., Davey M.G., Cock M.L., Hooper S.B., Harding R. Compromised respiratory function in postnatal lambs after placental insufficiency and intrauterine growth restriction. Pediatr. Res. 2001;50(5):641–649.
    1. Joss-Moore L.A., Wang Y., Baack M.L., et al. IUGR decreases PPARγ and SETD8 Expression in neonatal rat lung and these effects are ameliorated by maternal DHA supplementation. Early Hum. Dev. 2010;86(12):785–791.
    1. Cromi A., Ghezzi F., Raffaelli R., Bergamini V., Siesto G., Bolis P. Ultrasonographic measurement of thymus size in IUGR fetuses: A marker of the fetal immunoendocrine response to malnutrition. Ultrasound Obstet. Gynecol. 2009;33(4):421–426.
    1. Briana D.D., Baka S., Boutsikou M., et al. Soluble fas antigen and soluble fas ligand in intrauterine growth restriction. Neonatology. 2010;97(1):31–35.
    1. Pallotto E.K., Kilbride H.W. Perinatal outcome and later implications of intrauterine growth restriction. Clin. Obstet. Gynecol. 2006;49(2):257–269.
    1. Tröger B., Göpel W., Faust K., et al. Risk for late-onset blood-culture proven sepsis in very-low-birth weight infants born small for gestational age: A large multicenter study from the German Neonatal Network. Pediatr. Infect. Dis. J. 2014;33(3):238–243.
    1. Longo S., Borghesi A., Tzialla C., Stronati M. IUGR and infections. Early Hum. Dev. 2014;90(Suppl. 1):S42–S44.
    1. Tröger B., Müller T., Faust K., et al. Intrauterine growth restriction and the innate immune system in preterm infants of ≤32 weeks gestation. Neonatology. 2013;103(3):199–204.
    1. Manerikar S.S., Malaviya A.N., Singh M.B., Rajgopalan P., Kumar R. Immune status and BCG vaccination in newborns with intra-uterine growth retardation. Clin. Exp. Immunol. 1976;26(1):173–175.
    1. Contreras Y.M., Yu X., Hale M.A., et al. Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats. Pediatr. Res. 2011;70(2):123–129.
    1. Mukhopadhyay D., Weaver L., Tobin R., et al. Intrauterine growth restriction and prematurity influence regulatory T cell development in newborns. J. Pediatr. Surg. 2014;49(5):727–732.
    1. Lang U., Baker R.S., Khoury J., Clark K.E. Effects of chronic reduction in uterine blood flow on fetal and placental growth in the sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000;279(1):R53–R59.
    1. March M.I., Gupta M., Modest A.M., et al. Maternal risk factors for neonatal necrotizing enterocolitis. J Matern Neonatal Med. 2015;28:1285–1290.
    1. Amu S., Hahn-Zoric M., Malik A., et al. Cytokines in the placenta of Pakistani newborns with and without intrauterine growth retardation. Pediatr. Res. 2006;59(2):254–258.
    1. Hahn-Zoric M., Hagberg H., Kjellmer I., Ellis J., Wennergren M., Hanson L.Å. Aberrations in placental cytokine mRNA related to intrauterine growth retardation. Pediatr. Res. 2002;51(2):201–206.
    1. Lin Y., Wang J., Wang X., Wu W., Lai C. T cells development Is different between thymus from normal and intrauterine growth restricted pig fetus at different gestational stage. Asian-Australas. J. Anim. Sci. 2013;26(3):343–348.
    1. Zhong X., Li W., Huang X., et al. Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation. Cell Stress Chaperones. 2012;17(4):495–505.
    1. Tosun M., Celik H., Avci B., Yavuz E., Alper T., Malatyalioğlu E. Maternal and umbilical serum levels of interleukin-6, interleukin-8, and tumor necrosis factor-alpha in normal pregnancies and in pregnancies complicated by preeclampsia. J. Matern. Fetal Neonatal Med. 2010;23(8):880–886.
    1. Krajewski P., Sieroszewski P., Karowicz-Bilinska A., et al. Assessment of interleukin-6, interleukin-8 and interleukin-18 count in the serum of IUGR newborns. J. Matern. Fetal Neonatal Med. 2014;27(11):1142–1145.
    1. McElrath T.F., Allred E.N., Van Marter L., Fichorova R.N., Leviton A. Perinatal systemic inflammatory responses of growth-restricted preterm newborns. Acta Paediatr. 2013;102(10):e439–e442.
    1. Neta G.I., von Ehrenstein O.S., Goldman L.R., et al. Umbilical cord serum cytokine levels and risks of small-for-gestational-age and preterm birth. Am. J. Epidemiol. 2010;171(8):859–867.
    1. Marlow N., Morris T., Brocklehurst P., et al. A randomised trial of granulocyte-macrophage colony-stimulating factor for neonatal sepsis: childhood outcomes at 5 years. Arch. Dis. Child. Fetal Neonatal Ed. 2015;100(4):F320–F326.
    1. Barker D.J. Adult consequences of fetal growth restriction. Clin. Obstet. Gynecol. 2006;49(2):270–283.
    1. McMillen I.C., Robinson J.S. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 2005;85(2):571–633.
    1. Bateson P., Barker D., Clutton-Brock T., et al. Developmental plasticity and human health. Nature. 2004;430(6998):419–421.
    1. Pike K.C., Hanson M.A., Godfrey K.M. Developmental mismatch: Consequences for later cardiorespiratory health. BJOG. 2008;115(2):149–157.
    1. Banister C.E., Koestler D.C., Maccani M.A., Padbury J.F., Houseman E.A., Marsit C.J. Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics. 2011;6(7):920–927.
    1. Sebert S., Sharkey D., Budge H., Symonds M.E. The early programming of metabolic health: Is epigenetic setting the missing link? Am. J. Clin. Nutr. 2011;94(6) Suppl.:1953S–1958S.
    1. Heindel J.J., Balbus J., Birnbaum L., et al. Developmental origins of health and disease: Integrating environmental influences. Endocrinology. 2015;156(10):3416–3421.
    1. Yuen R.K., Peñaherrera M.S., von Dadelszen P., McFadden D.E., Robinson W.P. DNA methylation profiling of human placentas reveals promoter hypomethylation of multiple genes in early-onset preeclampsia. Eur. J. Hum. Genet. 2010;18(9):1006–1012.
    1. Park J.H., Stoffers D.A., Nicholls R.D., Simmons R.A. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J. Clin. Invest. 2008;118(6):2316–2324.
    1. Xu Y.P., Liang L., Wang X-M. The levels of Pdx1/insulin, Cacna1c and Cacna1d, and β-cell mass in a rat model of intrauterine undernutrition. J. Matern. Fetal Neonatal Med. 2011;24(3):437–443.
    1. Lambertini L., Lee T-L., Chan W-Y., et al. Differential methylation of imprinted genes in growth-restricted placentas. Reprod. Sci. 2011;18(11):1111–1117.
    1. Chelbi S.T., Doridot L., Mondon F., et al. Combination of promoter hypomethylation and PDX1 overexpression leads to TBX15 decrease in vascular IUGR placentas. Epigenetics. 2011;6(2):247–255.
    1. Johansson S., Iliadou A., Bergvall N., Tuvemo T., Norman M., Cnattingius S. Risk of high blood pressure among young men increases with the degree of immaturity at birth. Circulation. 2005;112(22):3430–3436.
    1. Brodszki J., Länne T., Marsál K., Ley D. Impaired vascular growth in late adolescence after intrauterine growth restriction. Circulation. 2005;111(20):2623–2628.
    1. Skilton M.R., Evans N., Griffiths K.A., Harmer J.A., Celermajer D.S. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet. 2005;365(9469):1484–1486.
    1. Martyn C.N., Gale C.R., Jespersen S., Sherriff S.B. Impaired fetal growth and atherosclerosis of carotid and peripheral arteries. Lancet. 1998;352(9123):173–178.
    1. Zanardo V., Visentin S., Trevisanuto D., Bertin M., Cavallin F., Cosmi E. Fetal aortic wall thickness: a marker of hypertension in IUGR children? Hypertens. Res. 2013;36(5):440–443.
    1. Crispi F., Bijnens B., Figueras F., et al. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation. 2010;121(22):2427–2436.
    1. Menendez-Castro C., Fahlbusch F., Cordasic N., et al. Early and late postnatal myocardial and vascular changes in a protein restriction rat model of intrauterine growth restriction. PLoS One. 2011;6(5):e20369.
    1. Oliveira V., de Souza L.V., Fernandes T., et al. Intrauterine growth restriction-induced deleterious adaptations in endothelial progenitor cells: Possible mechanism to impair endothelial function. J. Dev. Orig. Health Dis. 2017;8(6):665–673.
    1. Wlodek M.E., Westcott K., Siebel A.L., Owens J.A., Moritz K.M. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008;74(2):187–195.
    1. Rakow A., Johansson S., Legnevall L., et al. Renal volume and function in school-age children born preterm or small for gestational age. Pediatr. Nephrol. 2008;23(8):1309–1315.
    1. Bacchetta J., Harambat J., Dubourg L., et al. Both extrauterine and intrauterine growth restriction impair renal function in children born very preterm. Kidney Int. 2009;76(4):445–452.
    1. Rees S., Harding R., Walker D. An adverse intrauterine environment: implications for injury and altered development of the brain. Int. J. Dev. Neurosci. 2008;26(1):3–11.
    1. Miller S.L., Huppi P.S., Mallard C. The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome. J. Physiol. 2016;594(4):807–823.
    1. Korzeniewski S.J., Allred E.N., Joseph R.M., et al. Neurodevelopment at Age 10 Years of Children Born <28 Weeks With Fetal Growth Restriction. Pediatrics. 2017;140(5):140.
    1. Freire G., Shevell M., Oskoui M. Cerebral palsy: Phenotypes and risk factors in term singletons born small for gestational age. Eur. J. Paediatr. Neurol. 2015;19(2):218–225.
    1. Murray E., Fernandes M., Fazel M., Kennedy S.H., Villar J., Stein A. Differential effect of intrauterine growth restriction on childhood neurodevelopment: A systematic review. BJOG. 2015;122(8):1062–1072.
    1. Blair E.M., Nelson K.B. Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks’ gestation. Am. J. Obstet. Gynecol. 2015;212(4):520.e1–520.e7.
    1. Guellec I., Lapillonne A., Marret S., et al. Effect of Intra- and Extrauterine Growth on Long-Term Neurologic Outcomes of Very Preterm Infants. J. Pediatr. 2016;175:93–99.e1.
    1. Jacobsson B., Ahlin K., Francis A., Hagberg G., Hagberg H., Gardosi J. Cerebral palsy and restricted growth status at birth: Population-based case-control study. BJOG. 2008;115(10):1250–1255.
    1. Bickle Graz M., Tolsa J-F., Fischer Fumeaux C.J. Being small for gestational age: Does it matter for the neurodevelopment of premature infants? A cohort study. PLoS One. 2015;10(5):e0125769.
    1. Edmonds C.J., Isaacs E.B., Cole T.J., et al. The effect of intrauterine growth on verbal IQ scores in childhood: A study of monozygotic twins. Pediatrics. 2010;126(5):e1095–e1101.
    1. Baschat A.A. Neurodevelopment after fetal growth restriction. Fetal Diagn. Ther. 2014;36(2):136–142.
    1. Olivier P., Baud O., Evrard P., Gressens P., Verney C. Prenatal ischemia and white matter damage in rats. J. Neuropathol. Exp. Neurol. 2005;64(11):998–1006.
    1. Olivier P., Baud O., Bouslama M., Evrard P., Gressens P., Verney C. Moderate growth restriction: Deleterious and protective effects on white matter damage. Neurobiol. Dis. 2007;26(1):253–263.
    1. Reid M.V., Murray K.A., Marsh E.D., Golden J.A., Simmons R.A., Grinspan J.B. Delayed myelination in an intrauterine growth retardation model is mediated by oxidative stress upregulating bone morphogenetic protein 4. J. Neuropathol. Exp. Neurol. 2012;71(7):640–653.
    1. Tolsa C.B., Zimine S., Warfield S.K., et al. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr. Res. 2004;56(1):132–138.
    1. Zhao M., Dai H., Deng Y., Zhao L. SGA as a risk factor for cerebral palsy in moderate to late preterm infants: A system review and meta-analysis. Sci. Rep. 2016;6:38853.
    1. Rees S., Harding R., Walker D. The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int. J. Dev. Neurosci. 2011;29(6):551–563.
    1. Poudel R., McMillen I.C., Dunn S.L., Zhang S., Morrison J.L. 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(3):R151–R162.
    1. Figueras F., Cruz-Martinez R., Sanz-Cortes M., et al. Neurobehavioral outcomes in preterm, growth-restricted infants with and without prenatal advanced signs of brain-sparing. Ultrasound Obstet. Gynecol. 2011;38(3):288–294.
    1. 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(3):288.e1–288.e5.
    1. Mone F., McConnell B., Thompson A., et al. Fetal umbilical artery Doppler pulsatility index and childhood neurocognitive outcome at 12 years. BMJ Open. 2016;6(6):e008916.
    1. Hernandez-Andrade E., Figueroa-Diesel H., Jansson T., Rangel-Nava H., Gratacos E. Changes in regional fetal cerebral blood flow perfusion in relation to hemodynamic deterioration in severely growth-restricted fetuses. Ultrasound Obstet. Gynecol. 2008;32(1):71–76.
    1. Esteban F.J., Padilla N., Sanz-Cortés M., et al. Fractal-dimension analysis detects cerebral changes in preterm infants with and without intrauterine growth restriction. Neuroimage. 2010;53(4):1225–1232.
    1. Padilla N., Falcón C., Sanz-Cortés M., et al. Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: A magnetic resonance imaging study. Brain Res. 2011;1382:98–108.
    1. Dubois J., Benders M., Borradori-Tolsa C., et al. Primary cortical folding in the human newborn: An early marker of later functional development. Brain. 2008;131(Pt 8):2028–2041.
    1. Samuelsen G.B., Pakkenberg B., Bogdanović N., et al. Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants. Am. J. Obstet. Gynecol. 2007;197(1):56.e1–56.e7.
    1. Mazur M., Miller R.H., Robinson S. Postnatal erythropoietin treatment mitigates neural cell loss after systemic prenatal hypoxic-ischemic injury. J. Neurosurg. Pediatr. 2010;6(3):206–221.
    1. Guo R., Hou W., Dong Y., Yu Z., Stites J., Weiner C.P. Brain injury caused by chronic fetal hypoxemia is mediated by inflammatory cascade activation. Reprod. Sci. 2010;17(6):540–548.
    1. Tolcos M., Bateman E., O’Dowd R., et al. Intrauterine growth restriction affects the maturation of myelin. Exp. Neurol. 2011;232(1):53–65.
    1. Pham H., Duy A.P., Pansiot J., et al. Impact of inhaled nitric oxide on white matter damage in growth-restricted neonatal rats. Pediatr. Res. 2015;77(4):563–569.
    1. Mallard C., Loeliger M., Copolov D., Rees S. Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience. 2000;100(2):327–333.
    1. Miller S.L., Yawno T., Alers N.O., et al. Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction. J. Pineal Res. 2014;56(3):283–294.
    1. Fung C., Ke X., Brown A.S., Yu X., McKnight R.A., Lane R.H. Uteroplacental insufficiency alters rat hippocampal cellular phenotype in conjunction with ErbB receptor expression. Pediatr. Res. 2012;72(1):2–9.
    1. Isaacs E.B., Lucas A., Chong W.K., et al. Hippocampal volume and everyday memory in children of very low birth weight. Pediatr. Res. 2000;47(6):713–720.
    1. Illa M., Eixarch E., Batalle D., et al. Long-term functional outcomes and correlation with regional brain connectivity by MRI diffusion tractography metrics in a near-term rabbit model of intrauterine growth restriction. PLoS One. 2013;8(10):e76453.
    1. Rideau BNA, Pham H. Transcriptomic regulations in oligodendroglial and microglial cells related to brain damage following fetal growth restriction. Glia. 2016;64(12):2306–2320.
    1. Batalle D., Eixarch E., Figueras F., et al. Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome. Neuroimage. 2012;60(2):1352–1366.
    1. Padilla N., Fransson P., Donaire A., et al. Intrinsic functional connectivity in preterm infants with fetal growth restriction evaluated at 12 months Corrected Age. Cereb. Cortex. 2017;27(10):4750–4758.
    1. Baud O., Daire J-L., Dalmaz Y., et al. Gestational hypoxia induces white matter damage in neonatal rats: A new model of periventricular leukomalacia. Brain Pathol. 2004;14(1):1–10.
    1. Favrais G., van de Looij Y., Fleiss B., et al. Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 2011;70(4):550–565.
    1. Leviton A., Fichorova R.N., O’Shea T.M., et al. Two-hit model of brain damage in the very preterm newborn: Small for gestational age and postnatal systemic inflammation. Pediatr. Res. 2013;73(3):362–370.
    1. Campbell L.R., Pang Y., Ojeda N.B., Zheng B., Rhodes P.G., Alexander B.T. Intracerebral lipopolysaccharide induces neuroinflammatory change and augmented brain injury in growth-restricted neonatal rats. Pediatr. Res. 2012;71(6):645–652.
    1. Fleiss B., Gressens P. Tertiary mechanisms of brain damage: A new hope for treatment of cerebral palsy? Lancet Neurol. 2012;11(6):556–566.
    1. Leviton A., Dammann O. Brain damage markers in children. Neurobiological and clinical aspects. Acta Paediatr. 2002;91(1):9–13.
    1. Gazzolo D., Visser G.H., Lituania M., et al. S100B protein cord blood levels and development of fetal behavioral states: A study in normal and small-for-dates fetuses. J. Matern. Fetal Neonatal Med. 2002;11(6):378–384.

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