The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome

Journal of Physiology

Volumn 594, Issue 4, 2016, Pages 807-823

  Miller, Suzanne L ^a   Huppi, Petra S ^b   Mallard, Carina ^c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ASTROCYTOSIS; BRAIN BLOOD FLOW; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN SIZE; BRAIN VENTRICLE DILATATION; COGNITIVE DEFECT; DETERIORATION; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; DISEASE SEVERITY; FETUS HYPOXIA; FRACTIONAL ANISOTROPY; GESTATIONAL AGE; GRAY MATTER; HEART OUTPUT; HUMAN; HYPOGLYCEMIA; INTELLIGENCE QUOTIENT; INTRAUTERINE GROWTH RETARDATION; MIDDLE CEREBRAL ARTERY; NONHUMAN; PLACENTA INSUFFICIENCY; PREECLAMPSIA; PREMATURE LABOR; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SMALL FOR DATE INFANT; ANIMAL; BRAIN; FEMALE; GROWTH, DEVELOPMENT AND AGING; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY;

ANIMALS; BRAIN; FEMALE; FETAL GROWTH RETARDATION; HUMANS; PREGNANCY;

EID: 84958113084     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271402     Document Type: Review

References (139)

1. Akalin-Sel T, Nicolaides KH, Peacock J & Campbell S (1994). Doppler dynamics and their complex interrelation with fetal oxygen pressure, carbon dioxide pressure, and pH in growth-retarded fetuses. Obstet Gynecol 84, 439-444.
2. Alexander G (1964). Studies on the placenta of the sheep (Ovis aries L.). Effect of surgical reduction in the number of caruncles. J Reprod Fertil 7, 307-322.
3. Antonow-Schlorke I, Schwab M, Cox LA, Li C, Stuchlik K, Witte OW, Nathanielsz PW & McDonald TJ (2011). Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proc Natl Acad Sci USA 108, 3011-3016.
4. Back SA & Rosenberg PA (2014). Pathophysiology of glia in perinatal white matter injury. Glia 62, 1790-1815.
5. Baschat AA (2011). Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol 37, 501-514.
6. Baschat AA (2014). Neurodevelopment after fetal growth restriction. Fetal Diagn Ther 36, 136-142.
7. Basilious A, Yager J & Fehlings MG (2015). Neurological outcomes of animal models of uterine artery ligation and relevance to human intrauterine growth restriction: a systematic review. Dev Med Child Neurol 57, 420-430.
8. Batalle D, Eixarch E, Figueras F, Munoz-Moreno E, Bargallo N, Illa M, Acosta-Rojas R, Amat-Roldan I & Gratacos E (2012). Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome. Neuroimage 60, 1352-1366.
9. Batalle D, Munoz-Moreno E, Arbat-Plana A, Illa M, Figueras F, Eixarch E & Gratacos E (2014). Long-term reorganization of structural brain networks in a rabbit model of intrauterine growth restriction. Neuroimage 100, 24-38.
10. Bergvall N, Iliadou A, Tuvemo T & Cnattingius S (2006). Birth characteristics and risk of low intellectual performance in early adulthood: are the associations confounded by socioeconomic factors in adolescence or familial effects? Pediatrics 117, 714-721.
11. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A & Golan A (2000). Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 182, 198-206.
12. Bisignano M & Rees S (1988). The effects of intrauterine growth retardation on synaptogenesis and mitochondrial formation in the cerebral and cerebellar cortices of fetal sheep. Int J Dev Neurosci 6, 453-460.
13. Blair E (2000). Paediatric implications of IUGR with special reference to cerebral palsy. In: Intrauterine Growth Restriction Aetiology and Management, ed. Kingdom J & Baker P, pp 351-366. Springer, London.
14. Blair EM & Nelson KB (2014). Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks' gestation. Am J Obstet Gynecol 212, 520.e1-520.e7.
15. Brown JD & Vannucci RC (1978). Cerebral oxidative metabolism during intrauterine growth retardation. Biol Neonate 34, 170-173.
16. Businelli C, de Wit C, Visser GH & Pistorius LR (2015). Ultrasound evaluation of cortical brain development in fetuses with intrauterine growth restriction. J Matern Fetal Neonatal Med 28, 1302-1307.
17. Castillo-Melendez M, Yawno T, Allison BJ, Jenkin G, Wallace EM & Miller SL (2015). Cerebrovascular adaptations to chronic hypoxia in the growth restricted lamb. Int J Dev Neurosci 45, 55-65.
18. Cetin I & Alvino G (2009). Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta 30(Suppl A), S77-S82.
19. Chase HP, Welch NN, Dabiere CS, Vasan NS & Butterfield LJ (1972). Alterations in human brain biochemistry following intrauterine growth retardation. Pediatrics 50, 403-411.
20. Chauhan SP & Magann EF (2006). Screening for fetal growth restriction. Clin Obstet Gynecol 49, 284-294.
21. Chiang MC, Barysheva M, Shattuck DW, Lee AD, Madsen SK, Avedissian C, Klunder AD, Toga AW, McMahon KL, de Zubicaray GI, Wright MJ, Srivastava A, Balov N & Thompson PM (2009). Genetics of brain fiber architecture and intellectual performance. J Neurosci 29, 2212-2224.
22. Clapp JF 3rd, McLaughlin MK, Gellis J, Hemphill C & Catalano PM (1984). Regional distribution of cerebral blood flow in experimental intrauterine growth retardation. Am J Obstet Gynecol 150, 843-846.
23. Costantine MM, Weiner SJ, Rouse DJ, Hirtz DG, Varner MW, Spong CY, Mercer BM, Iams JD, Wapner RJ, Sorokin Y, Thorp JM Jr, Ramin SM, O'Sullivan MJ, Peaceman AM, Simhan HN; Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Maternal-Fetal Medicine Units Network (2011). Umbilical cord blood biomarkers of neurologic injury and the risk of cerebral palsy or infant death. Int J Dev Neurosci 29, 917-922.
24. Cottrell EC, Holmes MC, Livingstone DE, Kenyon CJ & Seckl JR (2012). Reconciling the nutritional and glucocorticoid hypotheses of fetal programming. FASEB J 26, 1866-1874.
25. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, Oros D & Gratacos E (2011). Fetal brain Doppler to predict cesarean delivery for nonreassuring fetal status in term small-for-gestational-age fetuses. Obstet Gynecol 117, 618-626.
26. Cruz-Martinez R, Figueras F, Oros D, Padilla N, Meler E, Hernandez-Andrade E & Gratacos E (2009). Cerebral blood perfusion and neurobehavioral performance in full-term small-for-gestational-age fetuses. Am J Obstet Gynecol 201, 474.e1-474.e7.
27. Damodaram MS, Story L, Eixarch E, Patkee P, Patel A, Kumar S & Rutherford M (2012). Foetal volumetry using magnetic resonance imaging in intrauterine growth restriction. Early Hum Dev 88(Suppl 1), S35-S40.
28. de Onis M, Blossner M & Villar J (1998). Levels and patterns of intrauterine growth retardation in developing countries. Eur J Clin Nutr 52(Suppl 1), S5-S15.
29. Delcour M, Russier M, Amin M, Baud O, Paban V, Barbe MF & Coq JO (2012). Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behav Brain Res 232, 233-244.
30. Dieni S & Rees S (2003). Dendritic morphology is altered in hippocampal neurons following prenatal compromise. J Neurobiol 55, 41-52.
31. Dobbing J & Sands J (1979). Comparative aspects of the brain growth spurt. Early Hum Dev 3, 79-83.
32. Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF & Huppi PS (2008). Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131, 2028-2041.
33. Edmonds CJ, Isaacs EB, Cole TJ, Rogers MH, Lanigan J, Singhal A, Birbara T, Gringras P, Denton J & Lucas A (2010). The effect of intrauterine growth on verbal IQ scores in childhood: a study of monozygotic twins. Pediatrics 126, e1095-e1101.
34. Eixarch E, Batalle D, Illa M, Munoz-Moreno E, Arbat-Plana A, Amat-Roldan I, Figueras F & Gratacos E (2012). Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PLoS One 7, e31497.
35. Eixarch E, Meler E, Iraola A, Illa M, Crispi F, Hernandez-Andrade E, Gratacos E & Figueras F (2008). Neurodevelopmental outcome in 2-year-old infants who were small-for-gestational age term fetuses with cerebral blood flow redistribution. Ultrasound Obstet Gynecol 32, 894-899.
36. Emmanouilides GC, Townsend DE & Bauer RA (1968). Effects of single umbilical artery ligation in the lamb fetus. Pediatrics 42, 919-927.
37. Esteban FJ, Padilla N, Sanz-Cortes M, de Miras JR, Bargallo N, Villoslada P & Gratacos E (2010). Fractal-dimension analysis detects cerebral changes in preterm infants with and without intrauterine growth restriction. Neuroimage 53, 1225-1232.
38. Fang S (2005). Management of preterm infants with intrauterine growth restriction. Early Hum Dev 81, 889-900.
39. Figueras F & Gardosi J (2011). Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 204, 288-300.
40. Figueras F & Gratacos E (2014). Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther 36, 86-98.
41. Figueroa-Diesel H, Hernandez-Andrade E, Acosta-Rojas R, Cabero L & Gratacos E (2007). Doppler changes in the main fetal brain arteries at different stages of hemodynamic adaptation in severe intrauterine growth restriction. Ultrasound Obstet Gynecol 30, 297-302.
42. Fischi-Gomez E, Vasung L, Meskaldji DE, Lazeyras F, Borradori-Tolsa C, Hagmann P, Barisnikov K, Thiran JP & Huppi PS (2014). Structural brain connectivity in school-age preterm infants provides evidence for impaired networks relevant for higher order cognitive skills and social cognition. Cerebral cortex 25, 2793-2805.
43. Fung C, Ke X, Brown AS, Yu X, McKnight RA & Lane RH (2012). Uteroplacental insufficiency alters rat hippocampal cellular phenotype in conjunction with ErbB receptor expression. Pediatr Res 72, 2-9.
44. Gagnon R (2003). Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol 110, S99-S107.
45. Gagnon R, Challis J, Johnston L & Fraher L (1994). Fetal endocrine responses to chronic placental embolization in the late-gestation ovine fetus. Am J Obstet Gynecol 170, 929-938.
46. Gale CR, O'Callaghan FJ, Bredow M & Martyn CN (2006). The influence of head growth in fetal life, infancy, and childhood on intelligence at the ages of 4 and 8 years. Pediatrics 118, 1486-1492.
47. Gazzolo D, Marinoni E, di Iorio R, Lituania M, Bruschettini PL & Michetti F (2002). Circulating S100β protein is increased in intrauterine growth-retarded fetuses. Pediatr Res 51, 215-219.
48. Gazzolo D, Marinoni E, Di Iorio R, Lituania M, Marras M, Bruschettini M, Bruschettini P, Frulio R, Michetti F, Petraglia F & Florio P (2006). High maternal blood S100B concentrations in pregnancies complicated by intrauterine growth restriction and intraventricular hemorrhage. Clin Chem 52, 819-826.
49. Geva R, Eshel R, Leitner Y, Fattal-Valevski A & Harel S (2006a). Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res 1117, 186-194.
50. Geva R, Eshel R, Leitner Y, Valevski AF & Harel S (2006b). Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics 118, 91-100.
51. Gilbert WM & Danielsen B (2003). Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol 188, 1596-1599; discussion 1599-1601.
52. Gotlieb SJ, Biasini FJ & Bray NW (1988). Visual recognition memory in IUGR and normal birth-weight infants. Infant Behav Dev 11, 223-228.
53. Guellec I, Lapillonne A, Renolleau S, Charlaluk ML, Roze JC, Marret S, Vieux R, Monique K, Ancel PY & Group ES (2011). Neurologic outcomes at school age in very preterm infants born with severe or mild growth restriction. Pediatrics 127, e883-e891.
54. Hadders-Algra M & Touwen B (1990). Body measurements, neurological and behavioural development in six-year-old children born preterm and/or small-for-gestational-age. Early Hum Dev 22, 1-13.
55. Harel S, Tomer A, Barak Y, Binderman I & Yavin E (1985). The cephalization index: a screening device for brain maturity and vulnerability in normal and intrauterine growth retarded newborns. Brain Dev 7, 580-584.
56. Hernandez-Andrade E, Serralde JA & Cruz-Martinez R (2012). Can anomalies of fetal brain circulation be useful in the management of growth restricted fetuses? Prenat Diagn 32, 103-112.
57. Herrera EA, Macchiavello R, Montt C, Ebensperger G, Diaz M, Ramirez S, Parer JT, Seron-Ferre M, Reyes RV & Llanos AJ (2014). Melatonin improves cerebrovascular function and decreases oxidative stress in chronically hypoxic lambs. J Pineal Res 57, 33-42.
58. Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA & Volpe JJ (1998). Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44, 584-590.
59. Illa M, Eixarch E, Batalle D, Arbat-Plana A, Munoz-Moreno E, Figueras F & Gratacos E (2013). 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 8, e76453.
60. Kamitomo M, Alonso JG, Okai T, Longo LD & Gilbert RD (1993). Effects of long-term, high-altitude hypoxemia on ovine fetal cardiac output and blood flow distribution. Am J Obstet Gynecol 169, 701-707.
61. Kingdom J & Smith G (2000). Diagnosis and management of IUGR. In: Intrauterine Growth Restriction Aetiology and Management, ed. Kingdom J & Baker P, pp. 257-273. Springer, London.
62. Kok JH, den Ouden AL, Verloove-Vanhorick SP & Brand R (1998). Outcome of very preterm small for gestational age infants: the first nine years of life. Br J Obstet Gynaecol 105, 162-168.
63. Lackman F, Capewell V, Richardson B, daSilva O & Gagnon R (2001). The risks of spontaneous preterm delivery and perinatal mortality in relation to size at birth according to fetal versus neonatal growth standards. Am J Obstet Gynecol 184, 946-953.
64. Lafeber HN, Rolph TP & Jones CT (1984). Studies on the growth of the fetal guinea pig. The effects of ligation of the uterine artery on organ growth and development. J Dev Physiol 6, 441-459.
65. Leitner Y, Fattal-Valevski A, Geva R, Eshel R, Toledano-Alhadef H, Rotstein M, Bassan H, Radianu B, Bitchonsky O, Jaffa AJ & Harel S (2007). Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol 22, 580-587.
66. Liu J, Liu L & Chen H (2011). Antenatal taurine supplementation for improving brain ultrastructure in fetal rats with intrauterine growth restriction. Neuroscience 181, 265-270.
67. Lodygensky GA, Seghier ML, Warfield SK, Tolsa CB, Sizonenko S, Lazeyras F & Huppi PS (2008). Intrauterine growth restriction affects the preterm infant's hippocampus. Pediatr Res 63, 438-443.
68. Loftin RW, Habli M, Snyder CC, Cormier CM, Lewis DF & Defranco EA (2010). Late preterm birth. Rev Obstet Gynecol 3, 10-19.
69. Louey S, Cock ML, Stevenson KM & Harding R (2000). Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep. Pediatr Res 48, 808-814.
70. Low JA, Handley-Derry MH, Burke SO, Peters RD, Pater EA, Killen HL & Derrick EJ (1992). Association of intrauterine fetal growth retardation and learning deficits at age 9 to 11 years. Am J Obstet Gynecol 167, 1499-1505.
71. McIntyre S, Taitz D, Keogh J, Goldsmith S, Badawi N & Blair E (2013). A systematic review of risk factors for cerebral palsy in children born at term in developed countries. Dev Med Child Neurol 55, 499-508.
72. McMillen IC, Adams MB, Ross JT, Coulter CL, Simonetta G, Owens JA, Robinson JS & Edwards LJ (2001). Fetal growth restriction: adaptations and consequences. Reproduction 122, 195-204.
73. Malhotra A, Yahya Z, Sasi A, Jenkin G, Ditchfield M, Polglase GR & Miller SL (2015). Does fetal growth restriction lead to increased brain injury as detected by neonatal cranial ultrasound in premature infants? J Paediatr Child Health 51, 1103-1108.
74. Mallard C, Loeliger M, Copolov D & Rees S (2000). Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience 100, 327-333.
75. Mallard EC, Rees S, Stringer M, Cock ML & Harding R (1998). Effects of chronic placental insufficiency on brain development in fetal sheep. Pediatr Res 43, 262-270.
76. Manjarrez-Gutierrez G, Gonzalez-Ramirez M, Boyzo-Montes de Oca A & Hernandez-Rodriguez J (2010). Dihydropteridine reductase activity in the brainstem of intrauterine growth-restricted rats. Int J Dev Neurosci 28, 621-624.
77. Marlow N (2000). Paediatric implications-neonatal complications. In Intrauterine Growth Restriction Aetiology and Management, ed. Kingdom J & Baker P, pp. 337-349. Springer, London.
78. Marsoosi V, Bahadori F, Esfahani F & Ghasemi-Rad M (2012). The role of Doppler indices in predicting intra ventricular hemorrhage and perinatal mortality in fetal growth restriction. Med Ultrason 14, 125-132.
79. Miller SL, Supramaniam VG, Jenkin G, Walker DW & Wallace EM (2009). Cardiovascular responses to maternal betamethasone administration in the intrauterine growth-restricted ovine fetus. Am J Obstet Gynecol 201, 613.e1-613.e8.
80. Miller SL & Wallace EM (2013). Effect of antenatal steroids on haemodynamics in the normally grown and growth restricted fetus. Curr Pediatr Rev 9, 67-74.
81. Miller SL, Yawno T, Alers NO, Castillo-Melendez M, Supramaniam VG, Vanzyl N, Sabaretnam T, Loose JM, Drummond GR, Walker DW, Jenkin G & Wallace EM (2014). Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction. J Pineal Res 56, 283-294.
82. Morrison JL (2008). Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol 35, 730-743.
83. Morsing E, Asard M, Ley D, Stjernqvist K & Marsal K (2011). Cognitive function after intrauterine growth restriction and very preterm birth. Pediatrics 127, e874-e882.
84. Nitsos I & Rees S (1990). The effects of intrauterine growth retardation on the development of neuroglia in fetal guinea pigs. An immunohistochemical and an ultrastructural study. Int J Dev Neurosci 8, 233-244.
85. Olivier P, Baud O, Bouslama M, Evrard P, Gressens P & Verney C (2007). Moderate growth restriction: deleterious and protective effects on white matter damage. Neurobiol Dis 26, 253-263.
86. Olivier P, Baud O, Evrard P, Gressens P & Verney C (2005). Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 64, 998-1006.
87. Oros D, Figueras F, Cruz-Martinez R, Padilla N, Meler E, Hernandez-Andrade E & Gratacos E (2010). Middle versus anterior cerebral artery Doppler for the prediction of perinatal outcome and neonatal neurobehavior in term small-for-gestational-age fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 35, 456-461.
88. Ortigosa Rocha C, Bittar RE & Zugaib M (2010). Neonatal outcomes of late-preterm birth associated or not with intrauterine growth restriction. Obstet Gynecol Int 2010, 231842.
89. Oyama K, Padbury J, Chappell B, Martinez A, Stein H & Humme J (1992). Single umbilical artery ligation-induced fetal growth retardation: effect on postnatal adaptation. Am J Physiol Endocrinol Metab 263, E575-E583.
90. Padilla N, Falcon C, Sanz-Cortes M, Figueras F, Bargallo N, Crispi F, Eixarch E, Arranz A, Botet F & Gratacos E (2011). Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: a magnetic resonance imaging study. Brain Res 1382, 98-108.
91. Padilla N, Junque C, Figueras F, Sanz-Cortes M, Bargallo N, Arranz A, Donaire A, Figueras J & Gratacos E (2014). Differential vulnerability of gray matter and white matter to intrauterine growth restriction in preterm infants at 12 months corrected age. Brain Res 1545, 1-11.
92. Padilla N, Perapoch J, Carrascosa A, Acosta-Rojas R, Botet F & Gratacos E (2010). Twelve-month neurodevelopmental outcome in preterm infants with and without intrauterine growth restriction. Acta Paediatr 99, 1498-1503.
93. Parkinson CE, Wallis S & Harvey D (1981). School achievement and behaviour of children who were small-for-dates at birth. Dev Med Child Neurol 23, 41-50.
94. Pearce W (2006). Hypoxic regulation of the fetal cerebral circulation. J Appl Physiol 100, 731-738.
95. Pham H, Duy AP, Pansiot J, Bollen B, Gallego J, Charriaut-Marlangue C & Baud O (2015). Impact of inhaled nitric oxide on white matter damage in growth-restricted neonatal rats. Pediatr Res 77, 563-569.
96. Pollack RN & Divon MY (1992). Intrauterine growth retardation: definition, classification, and etiology. Clin Obstet Gynecol 35, 99-107.
97. Poudel R, McMillen IC, Dunn SL, Zhang S & Morrison JL (2015). 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 308, R151-R162.
98. Procianoy RS, Garcia-Prats JA, Adams JM, Silvers A & Rudolph AJ (1980). Hyaline membrane disease and intraventricular haemorrhage in small for gestational age infants. Arch Dis Child 55, 502-505.
99. Pryor J, Silva PA & Brooke M (1995). Growth, development and behaviour in adolescents born small-for-gestational-age. J Paediatr Child Health 31, 403-407.
100. Ramenghi LA, Martinelli A, De Carli A, Brusati V, Mandia L, Fumagalli M, Triulzi F, Mosca F & Cetin I (2011). Cerebral maturation in IUGR and appropriate for gestational age preterm babies. Reprod Sci 18, 469-475.
101. Raznahan A, Greenstein D, Lee NR, Clasen LS & Giedd JN (2012). Prenatal growth in humans and postnatal brain maturation into late adolescence. Proc Natl Acad Sci USA 109, 11366-11371.
102. Rees S, Bocking AD & Harding R (1988). Structure of the fetal sheep brain in experimental growth retardation. J Dev Physiol 10, 211-225.
103. Rees S, Mallard C, Breen S, Stringer M, Cock M & Harding R (1998). Fetal brain injury following prolonged hypoxemia and placental insufficiency: a review. Comp Biochem Physiol A Mol Integr Physiol 119, 653-660.
104. Rehn AE, Van Den Buuse M, Copolov D, Briscoe T, Lambert G & Rees S (2004). An animal model of chronic placental insufficiency: relevance to neurodevelopmental disorders including schizophrenia. Neuroscience 129, 381-391.
105. Reid MV, Murray KA, Marsh ED, Golden JA, Simmons RA & Grinspan JB (2012). Delayed myelination in an intrauterine growth retardation model is mediated by oxidative stress upregulating bone morphogenetic protein 4. J Neuropathol Exp Neurol 71, 640-653.
106. Represa A, Chanez C, Flexor MA & Ben-Ari Y (1989). Development of the cholinergic system in control and intra-uterine growth retarded rat brain. Brain Res Dev Brain Res 47, 71-79.
107. Resnik R (2002). Intrauterine growth restriction. Obstet Gynecol 99, 490-496.
108. Robinson JS, Kingston EJ, Jones CT & Thorburn GD (1979). Studies on experimental growth retardation in sheep. The effect of removal of a endometrial caruncles on fetal size and metabolism. J Dev Physiol 1, 379-398.
109. Rossi A, Romanello I, Forzano L, Fachechi G & Marchesoni D (2011). Evaluation of fetal cerebral blood flow perfusion using power Doppler ultrasound angiography (3D-PDA) in growth-restricted fetuses. Facts Views Vis Obgyn 3, 175-180.
110. Roza SJ, Steegers EA, Verburg BO, Jaddoe VW, Moll HA, Hofman A, Verhulst FC & Tiemeier H (2008). What is spared by fetal brain-sparing? Fetal circulatory redistribution and behavioral problems in the general population. Am J Epidemiol 168, 1145-1152.
111. Samuelsen GB, Pakkenberg B, Bogdanovic N, Gundersen HJ, Larsen JF, Graem N & Laursen H (2007). Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants. Am J Obstet Gynecol 197, 56.e1-56.e7.
112. Scherjon S, Briet J, Oosting H & Kok J (2000). 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 105, 385-391.
113. Scherjon SA, Oosting H, Smolders-DeHaas H, Zondervan HA & Kok JH (1998). Neurodevelopmental outcome at three years of age after fetal 'brain-sparing'. Early Hum Dev 52, 67-79.
114. Schreuder AM, McDonnell M, Gaffney G, Johnson A & Hope PL (2002). Outcome at school age following antenatal detection of absent or reversed end diastolic flow velocity in the umbilical artery. Arch Dis Child Fetal Neonatal Ed 86, F108-114.
115. Somm E, Larvaron P, van de Looij Y, Toulotte A, Chatagner A, Faure M, Metairon S, Mansourian R, Raymond F, Gruetter R, Wang B, Sizonenko SV & Huppi PS (2014). Protective effects of maternal nutritional supplementation with lactoferrin on growth and brain metabolism. Pediatr Res 75, 51-61.
116. Somm E, Vauthay DM, Guerardel A, Toulotte A, Cettour-Rose P, Klee P, Meda P, Aubert ML, Huppi PS & Schwitzgebel VM (2012). Early metabolic defects in dexamethasone-exposed and undernourished intrauterine growth restricted rats. PLoS One 7, e50131.
117. Soo PS, Hiscock J, Botting KJ, Roberts CT, Davey AK & Morrison JL (2012). Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod Toxicol 33, 374-381.
118. Soothill PW, Ajayi RA, Campbell S, Ross EM & Nicolaides KH (1995). Fetal oxygenation at cordocentesis, maternal smoking and childhood neuro-development. Eur J Obstet Gynecol Reprod Biol 59, 21-24.
119. Soothill PW, Nicolaides KH & Campbell S (1987). Prenatal asphyxia, hyperlacticaemia, hypoglycaemia, and erythroblastosis in growth retarded fetuses. Br Med J (Clin Res Ed) 294, 1051-1053.
120. Spinillo A, Montanari L, Roccio M, Zanchi S, Tzialla C & Stronati M (2009). Prognostic significance of the interaction between abnormal umbilical and middle cerebral artery Doppler velocimetry in pregnancies complicated by fetal growth restriction. Acta Obstet Gynecol Scand 88, 159-166.
121. Story L, Damodaram MS, Supramaniam V, Allsop JM, McGuinness A, Patel A, Wylezinska M, Kumar S & Rutherford MA (2013). Myo-inositol metabolism in appropriately grown and growth-restricted fetuses: a proton magnetic resonance spectroscopy study. Eur J Obstet Gynecol Reprod Biol 170, 77-81.
122. Streimish IG, Ehrenkranz RA, Allred EN, O'Shea TM, Kuban KC, Paneth N & Leviton A; ELGAN Study Investigators (2012). Birth weight- and fetal weight-growth restriction: impact on neurodevelopment. Early Hum Dev 88, 765-771.
123. Sung IK, Vohr B & Oh W (1993). Growth and neurodevelopmental outcome of very low birth weight infants with intrauterine growth retardation: comparison with control subjects matched by birth weight and gestational age. J Pediatr 123, 618-624.
124. Supramaniam VG, Jenkin G, Loose J, Wallace EM & Miller SL (2006). Chronic fetal hypoxia increases activin A concentrations in the late-pregnant sheep. BJOG 113, 102-109.
125. Swanson AM & David AL (2015). Animal models of fetal growth restriction: Considerations for translational medicine. Placenta 36, 623-630.
126. Tashima L, Nakata M, Anno K, Sugino N & Kato H (2001). Prenatal influence of ischemia-hypoxia-induced intrauterine growth retardation on brain development and behavioral activity in rats. Biol Neonate 80, 81-87.
127. Thordstein M & Hedner T (1992). Cerebral and adrenal monoamine metabolism in the growth-retarded rat fetus under normoxia and hypoxia. Pediatr Res 31, 131-137.
128. Tolcos M, Bateman E, O'Dowd R, Markwick R, Vrijsen K, Rehn A & Rees S (2011). Intrauterine growth restriction affects the maturation of myelin. Exp Neurol 232, 53-65.
129. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, Lazeyras F, Hanquinet S, Pfizenmaier M & Huppi PS (2004). Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res 56, 132-138.
130. Uysal A, Oktem G, Yilmaz O, Uslu S, Aktug H & Yurtseven ME (2008). Quantitative immunohistochemical analysis of nitric oxide synthases and apoptosis regulator proteins in the fetal rat brain following maternal uterine artery ligation. Int J Neurosci 118, 891-901.
131. van de Looij Y, Dean JM, Gunn AJ, Huppi PS & Sizonenko SV (2015). Advanced magnetic resonance spectroscopy and imaging techniques applied to brain development and animal models of perinatal injury. Int J Dev Neurosci 45, 29-38.
132. van Marthens E, Harel S & Zamenshof S (1975). Experimental intrauterine growth retardation. Biol Neonate 26, 221-231.
133. van Vliet E, Eixarch E, Illa M, Arbat-Plana A, Gonzalez-Tendero A, Hogberg HT, Zhao L, Hartung T & Gratacos E (2013). Metabolomics reveals metabolic alterations by intrauterine growth restriction in the fetal rabbit brain. PLoS One 8, e64545.
134. van Wassenaer A (2005). Neurodevelopmental consequences of being born SGA. Pediatr Endocrinol Rev 2, 372-377.
135. von Beckerath AK, Kollmann M, Rotky-Fast C, Karpf E, Lang U & Klaritsch P (2013). Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. Am J Obstet Gynecol 208, 130.e1-130.e6.
136. Vossbeck S, de Camargo OK, Grab D, Bode H & Pohlandt F (2001). Neonatal and neurodevelopmental outcome in infants born before 30 weeks of gestation with absent or reversed end-diastolic flow velocities in the umbilical artery. Eur J Pediatr 160, 128-134.
137. Wigglesworth JS (1974). Fetal growth retardation. Animal model: uterine vessel ligation in the pregnant rat. Am J Pathol 77, 347-350.
138. Woodall SM, Breier BH, Johnston BM & Gluckman PD (1996). A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Endocrinol 150, 231-242.
139. Yanney M & Marlow N (2004). Paediatric consequences of fetal growth restriction. Semin Fetal Neonatal Med 9, 411-418.