An adverse intrauterine environment: implications for injury and altered development of the brain

Rees, Sandra; Harding, Richard; Walker, David

doi:10.1016/j.ijdevneu.2007.08.020

Cited by 160Neonatal and fetal brain pathologyBirth, Development, and HealthPregnancy and preeclampsia studies

An adverse intrauterine environment: implications for injury and altered development of the brain

Rees, Sandra, Harding, Richard, Walker, David·2008·International Journal of Developmental Neuroscience

DOI 10.1016/j.ijdevneu.2007.08.020

Open this paper in CoChat — free account

Abstract

Abnormal development of the brain during fetal life is now thought to contribute to the aetiology of many functional and behavioural disorders that manifest throughout life. Many factors are likely to underlie such abnormal development including genetic makeup and an adverse intrauterine environment. This review will focus on prenatal hypoxic–ischemic injury and inflammatory/infective insults. A range of experimental models have been used to characterise lesions formed in response to these insults and to determine mechanisms of damage resulting from such events. Relatively brief periods of fetal hypoxia result in neuronal death (cerebellum, hippocampus, and cerebral cortex), white matter damage and reduced growth of neural processes. These effects are more profound at mid than late gestation. Chronic mild placental insufficiency can result in fetal growth restriction and deficits in neural connectivity and myelination. Exposure of the preterm fetus to inflammatory agents causes brain damage particularly in the white matter and this is exacerbated by hypoxia. These studies show that the timing, severity and nature of specific insults are critical in determining the pattern of injury and thus the extent to which neurological function will be affected postnatally. Defining the causes, patterns and mechanisms of brain injury is crucial if we are to develop rational neuroprotective strategies to reduce the burden of altered brain growth and poor functional and behavioural outcomes.

Integrity signals

Registry

Crossref · 10.1016/j.ijdevneu.2007.08.020

Cites

94 of 94 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Abnormal brain development during gestation contributes to many neurological disorders across the lifespan.
“Growing evidence suggests that abnormal development of the brain during gestation contributes to many neurological disorders that are manifested throughout the entire lifespan (Rees et al., 2008).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Rees et al., 2008

Neurology of the newborn.
Volpe, J. J. (1981) · PubMed · Cited by 2,859 · see citing works
Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial
Gluckman, P. D., Wyatt, J. S., Azzopardi, D., Ballard, R., Edwards, A. D., Ferriero, D. M., Polin, R. A., Robertson, C. M., Thoresen, M., Whitelaw, A., et al. (2005) · The Lancet · doi:10.1016/s0140-6736(05)17946-x · Cited by 2,270 · see citing works
The influence of immaturity on hypoxic‐ischemic brain damage in the rat
Rice, J. E., Vannucci, R. C., & Brierley, J. B. (1981) · Annals of Neurology · doi:10.1002/ana.410090206 · Cited by 2,142 · see citing works
Cerebral Palsy
Miller, F. (2005) · Cited by 2,011 · see citing works
The neuropathology of schizophrenia
Harrison, P. J. (1999) · Brain · doi:10.1093/brain/122.4.593 · Cited by 1,677 · see citing works
CEREBRAL VENTRICULAR SIZE AND COGNITIVE IMPAIRMENT IN CHRONIC SCHIZOPHRENIA
Johnstone, E., Frith, C., Crow, T. J., Husband, J., & Kreel, L. (1976) · The Lancet · doi:10.1016/s0140-6736(76)90890-4 · Cited by 1,253 · see citing works
Neuropharmacology of quinolinic and kynurenic acids.
Stone, T. W. (1993) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)00441-7 · Cited by 949 · see citing works
Antecedents of Cerebral Palsy
Nelson, K. B., & Ellenberg, J. H. (1986) · New England Journal of Medicine · doi:10.1056/nejm198607103150202 · Cited by 945 · see citing works
Maternal Intrauterine Infection, Cytokines, and Brain Damage in the Preterm Newborn
Dammann, O., & Leviton, A. (1997) · Pediatric Research · doi:10.1203/00006450-199707000-00001 · Cited by 886 · see citing works
Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy
Yoon, B. H., Jun, J. K., Romero, R. J., Park, K. H., Gómez, R., Choi, J., & Kim, I.-O. (1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70432-0 · Cited by 756 · see citing works
Outcomes of children of extremely low birthweight and gestational age in the 1990's.
Hack, M., & Fanaroff, A. (1999) · Early Human Development · doi:10.1016/s0378-3782(98)00052-8 · Cited by 731 · see citing works
A template for defining a causal relation between acute intrapartum events and cerebral palsy: international consensus statement
MacLennan, A. (1999) · BMJ · doi:10.1136/bmj.319.7216.1054 · Cited by 731 · see citing works
Periventricular Leukomalacia of Infancy
Banker, B. Q. (1962) · Archives of Neurology · doi:10.1001/archneur.1962.04210050022004 · Cited by 718 · see citing works
Origin and timing of brain lesions in term infants with neonatal encephalopathy
Cowan, F. M., Rutherford, M., Groenendaal, F., Eken, P., Mercuri, E. M., Bydder, G. M., Meiners, L. C., Dubowitz, L. M. S., & de Vries, L. S. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12658-x · Cited by 604 · see citing works
Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion
Back, S. A., Gan, X., Li, Y., Rosenberg, P. A., & Volpe, J. J. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06241.1998 · Cited by 586 · see citing works
Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia
Yoon, B. H., Romero, R., Yang, S. H., Jun, J. K., Kim, I.-O., Choi, J.-H., & Syn, H. C. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70585-9 · Cited by 584 · see citing works
NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury
Salter, M. G., & Fern, R. F. (2005) · Nature · doi:10.1038/nature04301 · Cited by 556 · see citing works
Cerebral Palsy
Kuban, K., & Leviton, A. E. (1994) · New England Journal of Medicine · doi:10.1056/nejm199401203300308 · Cited by 503 · see citing works
Nitrosative and Oxidative Injury to Premyelinating Oligodendrocytes in Periventricular Leukomalacia
Haynes, R. L., Folkerth, R. D., Keefe, R. J., Sung, I., Swzeda, L. I., Rosenberg, P. A., Volpe, J. J., & Kinney, H. C. (2003) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/62.5.441 · Cited by 454 · see citing works
Human macrophages convert l -tryptophan into the neurotoxin quinolinic acid
Heyes, M. P., Saito, K., & Markey, S. P. (1992) · Biochemical Journal · doi:10.1042/bj2830633 · Cited by 448 · see citing works
Bacterial endotoxin sensitizes the immature brain to hypoxic–ischaemic injury
Eklind, S., Mallard, C. E., Leverin, A., Gilland, E., Blomgren, K., Mattsby‐Baltzer, I., & Hagberg, H. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01474.x · Cited by 423 · see citing works
White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term.
Inder, T. E., Anderson, N. J., Spencer, C., Wells, S., & Volpe, J. J. (2003) · PubMed Central · Cited by 378 · see citing works
Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term
Allin, M. P. G., Matsumoto, H., Santhouse, A. M., Nosarti, C., AlAsady, M. H. S., STEWART, A. L., Rifkin, L., & Murray, R. M. (2001) · Brain · doi:10.1093/brain/124.1.60 · Cited by 363 · see citing works
Neonatal excitotoxic hippocampal damage in rats causes post-pubertal changes in prepulse inhibition of startle and its disruption by apomorphine
Lipska, B. K., Weinberger, D. R., Swerdlow, N. R., Geyer, M. A., BRAFF, D. L., & Jaskiw, G. E. (1995) · Psychopharmacology · doi:10.1007/bf02246439 · Cited by 356 · see citing works
Hippocampal Volume and Everyday Memory in Children of Very Low Birth Weight
Isaacs, E., Lucas, A., Chong, W. K., Wood, S. J., Johnson, C. L., Marshall, C., Vargha‐Khadem, F., & Gadian, D. G. (2000) · Pediatric Research · doi:10.1203/00006450-200006000-00006 · Cited by 336 · see citing works
Erythropoietin as an antiapoptotic, tissue-protective cytokine
Ghezzi, P., & Brines, M. (2004) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401450 · Cited by 327 · see citing works
Rapid Ischemic Cell Death in Immature Oligodendrocytes: A Fatal Glutamate Release Feedback Loop
Fern, R. F., & Möller, T. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00034.2000 · Cited by 321 · see citing works
Potentially asphyxiating conditions and spastic cerebral palsy in infants of normal birth weight
Nelson, K. B., & Grether, J. K. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70387-4 · Cited by 300 · see citing works
Human microglia convert l -tryptophan into the neurotoxin quinolinic acid
Heyes, M. P., Achim, C. L., Wiley, C. A., Major, E. O., Saito, K., & Markey, S. P. (1996) · Biochemical Journal · doi:10.1042/bj3200595 · Cited by 260 · see citing works
White Matter Injury after Repeated Endotoxin Exposure in the Preterm Ovine Fetus
Duncan, J. R., Cock, M. L., Scheerlinck, J. Y., Westcott, K. T., McLean, C., Harding, R., & Rees, S. M. (2002) · Pediatric Research · doi:10.1203/00006450-200212000-00021 · Cited by 229 · see citing works
Self-citation
Outcome after ischemia in the developing sheep brain: An electroencephalographic and histological study
Williams, C. E., Gunn, A. J., Mallard, C. E., et al. (1992) · Annals of Neurology · doi:10.1002/ana.410310104 · Cited by 224 · see citing works
White Matter Injury Following Systemic Endotoxemia or Asphyxia in the Fetal Sheep
Mallard, C. E., Welin, A.-K., Peebles, D., Hagberg, H., & Kjellmer, I. (2003) · Neurochemical Research · doi:10.1023/a:1022368915400 · Cited by 222 · see citing works
Preterm Fetal Hypoxia-Ischemia Causes Hypertonia and Motor Deficits in the Neonatal Rabbit: A Model for Human Cerebral Palsy?
Derrick, M., Luo, N. L., Bregman, J. C., Jilling, T., Ji, X., Fisher, K., Gladson, C. L., Beardsley, D. J., MURDOCH, G. H., Back, S. A., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2816-03.2004 · Cited by 221 · see citing works
Micronutrients and Intrauterine Infection, Preterm Birth and the Fetal Inflammatory Response Syndrome
Romero, R. J., Chaiworapongsa, T., & Espinoza, J. (2003) · Journal of Nutrition · doi:10.1093/jn/133.5.1668s · Cited by 219 · see citing works
Impaired Trophic Interactions Between the Cerebellum and the Cerebrum Among Preterm Infants
Limperopoulos, C., Soul, J. S., Haidar, H., Hüppi, P. S., Bassan, H., Warfield, S. K., Robertson, R. L., Moore, M., Akins, P., Volpe, J. J., et al. (2005) · PEDIATRICS · doi:10.1542/peds.2004-2282 · Cited by 217 · see citing works
Spatial Heterogeneity in Oligodendrocyte Lineage Maturation and Not Cerebral Blood Flow Predicts Fetal Ovine Periventricular White Matter Injury
Riddle, A., Luo, N. L., Manese, M., Beardsley, D. J., Green, L., Rorvik, D. A., Kelly, K. A., Barlow, C. H., Kelly, J. J., Hohimer, A. R., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5200-05.2006 · Cited by 186 · see citing works
Insulin-like growth factor-1 is a potent neuronal rescue agent after hypoxic-ischemic injury in fetal lambs.
Johnston, B. M., Mallard, C. E., Williams, C. E., & Gluckman, P. D. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118416 · Cited by 181 · see citing works
Neonatal Cytokines and Cerebral Palsy in Very Preterm Infants
Nelson, K. B., Grether, J. K., Dambrosia, J. M., Walsh, E. M., Kohler, S. J., Satyanarayana, G., Nelson, P. G., Dickens, B. F., & Phillips, T. M. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000056802.22454.ab · Cited by 173 · see citing works
Effects of Chronic Placental Insufficiency on Brain Development in Fetal Sheep
Mallard, C. E., Rees, S. M., Stringer, M., et al. (1998) · Pediatric Research · doi:10.1203/00006450-199802000-00018 · Cited by 168 · see citing works
Self-citation
Origins of Cerebral Palsy
Naeye, R. L. (1989) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1989.02150220044018 · Cited by 167 · see citing works
Long‐term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism
Harris, L. W., Sharp, T., Gartlon, J. E., Jones, D. N. C., & Harrison, P. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02902.x · Cited by 162 · see citing works
N‐acetylcysteine reduces lipopolysaccharide‐sensitized hypoxic‐ischemic brain injury
Wang, X., Svedin, P., Nie, C., Lapatto, R., Zhu, C., Gustavsson, M., Sandberg, M., Karlsson, J., Romero, R. J., Hagberg, H., et al. (2007) · Annals of Neurology · doi:10.1002/ana.21066 · Cited by 161 · see citing works
Melatonin Provides Neuroprotection in the Late-Gestation Fetal Sheep Brain in Response to Umbilical Cord Occlusion
Miller, S., Yan, E. B., Castillo-Meléndez, M., Jenkin, G., & Walker, D. W. (2005) · Developmental Neuroscience · doi:10.1159/000085993 · Cited by 149 · see citing works
Self-citation
Visual deficits in children born at less than 32 weeks' gestation with and without major ocular pathology and cerebral damage.
Dowdeswell, H. J., Slater, A. M., Broomhall, J., et al. (1995) · British Journal of Ophthalmology · doi:10.1136/bjo.79.5.447 · Cited by 135 · see citing works
The Correlation of Prenatal Brain Damage with Placental Pathology
Grafe, M. R. (1994) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199407000-00013 · Cited by 134 · see citing works
Immunohistochemical expression of tumor necrosis factor α in neonatal leukomalacia
Deguchi, K., Mizuguchi, M., & Takashima, S. (1996) · Pediatric Neurology · doi:10.1016/0887-8994(95)00223-5 · Cited by 125 · see citing works
The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation
Rees, S. M., Stringer, M., Just, Y., Hooper, S. B., & Harding, R. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)81787-7 · Cited by 123 · see citing works
Self-citation
Hypoxic regulation of the fetal cerebral circulation
Pearce, W. J. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00990.2005 · Cited by 123 · see citing works
Ventriculomegaly and reduced hippocampal volume following intrauterine growth-restriction: implications for the aetiology of schizophrenia
Mallard, C. E., Rehn, A., Rees, S. M., Tolcos, M., & Copolov, D. (1999) · Schizophrenia Research · doi:10.1016/s0920-9964(99)00041-9 · Cited by 120 · see citing works
Self-citation
Regional Cerebral Blood Flow after Hemorrhagic Hypotension in the Preterm, Near-Term, and Newborn Lamb
Szymonowicz, W., WALKER, A. M., YU, V. Y. H., et al. (1990) · Pediatric Research · doi:10.1203/00006450-199010000-00012 · Cited by 118 · see citing works
A Model of Cerebral Palsy From Fetal Hypoxia-Ischemia
Derrick, M., Drobyshevsky, A., Ji, X., & Tan, S. (2007) · Stroke · doi:10.1161/01.str.0000251445.94697.64 · Cited by 118 · see citing works
Topical Review: Role of Instrumented Fetal Sheep Preparations in Defining the Pathogenesis of Human Periventricular White-Matter Injury
Back, S. A., Riddle, A., & Hohimer, A. R. (2006) · Journal of Child Neurology · doi:10.1177/08830738060210070101 · Cited by 115 · see citing works
Brief Update on Animal Models of Hypoxic-Ischemic Encephalopathy and Neonatal Stroke
Northington, F. J. (2006) · ILAR Journal · doi:10.1093/ilar.47.1.32 · Cited by 107 · see citing works
Hypoxia—Ischemia Preferentially Triggers Glutamate Depletion from Oligodendroglia and Axons in Perinatal Cerebral White Matter
Back, S. A., Craig, A., Kayton, R. J., Luo, N. L., Meshul, C. K., Allcock, N., & Fern, R. F. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600344 · Cited by 105 · see citing works
Circulatory responses to prolonged hypoxemia in fetal sheep
Bocking, A. D., Gagnon, R., White, S. E., Homan, J., Milne, K. M., & Richardson, B. S. (1988) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(88)90567-4 · Cited by 104 · see citing works
Chronic Exposure to Intra-Amniotic Lipopolysaccharide Affects the Ovine Fetal Brain
Nitsos, I., Rees, S. M., Duncan, J., Kramer, B. W. W., Harding, R., Newnham, J. P., & Moss, T. J. M. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2006.02.011 · Cited by 99 · see citing works
Self-citation
Prolonged Reductions in Placental Blood Flow and Cerebral Oxygen Delivery in Preterm Fetal Sheep Exposed to Endotoxin: Possible Factors in Whitge Matter Injury After Acute Infection
Dalitz, P., Harding, R., Rees, S. M., & Cock, M. L. (2003) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(03)00090-x · Cited by 96 · see citing works
Self-citation
An animal model of chronic placental insufficiency: Relevance to neurodevelopmental disorders including schizophrenia
Rehn, A., van den Buuse, M., Copolov, D., Briscoe, T. A., Lambert, G. W., & Rees, S. M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.047 · Cited by 95 · see citing works
Self-citation
Hypoxemia Near Mid-Gestation Has Long-term Effects on Fetal Brain Development
Rees, S. M., Breen, S. J., Loeliger, M. M., et al. (1999) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199909000-00004 · Cited by 95 · see citing works
Self-citation
Characteristics of cranial ultrasound white‐matter echolucencies that predict disability: a review
Holling, E. E., & Leviton, A. E. (1999) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.1999.tb00567.x · Cited by 91 · see citing works
The effects of intrauterine growth retardation on the development of neuroglia in fetal guinea pigs. An immunohistochemical and an ultrastructural study
Nitsos, I., & Rees, S. M. (1990) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(90)90029-2 · Cited by 88 · see citing works
Self-citation
Cerebrovascular Responses in the Fetal Sheep Brain to Low-Dose Endotoxin
Yan, E. B., Castillo-Meléndez, M., Nicholls, T., Hirst, J. J., & Walker, D. W. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000115681.95957.d4 · Cited by 84 · see citing works
Self-citation
Chronic Endotoxin Exposure Causes Brain Injury in the Ovine Fetus in the Absence of Hypoxemia
Duncan, J., Cock, M. L., Suzuki, K., Scheerlinck, J. Y., Harding, R., & Rees, S. M. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2005.12.003 · Cited by 82 · see citing works
Self-citation
Structure of the fetal sheep brain in experimental growth retardation.
Rees, S. M., Bocking, A. D., & Harding, R. (1988) · PubMed · Cited by 82 · see citing works
Self-citation
Endotoxemia Severely Affects Circulation During Normoxia and Asphyxia in Immature Fetal Sheep
Garnier, Y., Coumans, A. B. C., Berger, R. E., Jensen, A., & Hasaart, T. H. M. (2001) · Journal of the Society for Gynecologic Investigation · doi:10.1177/107155760100800303 · Cited by 72 · see citing works
Adenosine Mediates Decreased Cerebral Metabolic Rate and Increased Cerebral Blood Flow During Acute Moderate Hypoxia in the Near‐Term Fetal Sheep
Blood, A. B., Hunter, C. J., & Power, G. G. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.047928 · Cited by 68 · see citing works
Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep
Loeliger, M. M., Watson, C. S., Reynolds, J. D. H., Penning, D. H., Harding, R., Bocking, A. D., & Rees, S. M. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00756-x · Cited by 68 · see citing works
Self-citation
Hypoxic-Ischemic Brain Injury in the Term Newborn
Rivkin, M. J. (1997) · Clinics in Perinatology · doi:10.1016/s0095-5108(18)30161-1 · Cited by 68 · see citing works
Modest Hypothermia Preserves Cerebral Energy Metabolism during Hypoxia-Ischemia and Correlates with Brain Damage: A 31P Nuclear Magnetic Resonance Study in Unanesthetized Neonatal Rats
Williams, G. D., Dardzinski, B. J., Buckalew, A. R., et al. (1997) · Pediatric Research · doi:10.1203/00006450-199711000-00024 · Cited by 67 · see citing works
Lipid Peroxidation, Caspase-3 Immunoreactivity, and Pyknosis in Late-Gestation Fetal Sheep Brain after Umbilical Cord Occlusion
Castillo-Meléndez, M., Chow, J. A. M., & Walker, D. W. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000115679.86566.c4 · Cited by 66 · see citing works
Self-citation
Identification of kynurenine pathway enzyme mRNAs and metabolites in human placenta: Up-regulation by inflammatory stimuli and with clinical infection
Manuelpillai, U., Ligam, P., Smythe, G. A., Wallace, E. M., Hirst, J. J., & Walker, D. W. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.06.090 · Cited by 65 · see citing works
Self-citation
Relationship between placental histologic features and umbilical cord blood gases in preterm gestations
Salafia, C. M., MINIOR, V. K., López-Zeno, J., et al. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91326-2 · Cited by 62 · see citing works
Novel treatments after experimental brain injury
Johnston, M. V., Trescher, W. H., Ishida, A., et al. (2000) · Seminars in Neonatology · doi:10.1053/siny.1999.0116 · Cited by 60 · see citing works
The effects of intrauterine growth retardation on the development of the Purkinje cell dendritic tree in the cerebellar cortex of fetal sheep: A note on the ontogeny of the Purkinje cell
Rees, S. M., & Harding, R. (1988) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(88)90052-4 · Cited by 58 · see citing works
Self-citation
Neuropathology of the near-term and midgestation ovine fetal brain after sustained in utero hypoxemia
Penning, D. H., Grafe, M. R., Hammond, R. R., et al. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(94)70175-x · Cited by 55 · see citing works
Microglial activation, macrophage infiltration, and evidence of cell death in the fetal brain after uteroplacental administration of lipopolysaccharide in sheep in late gestation
Hutton, L. C., Castillo-Meléndez, M., Smythe, G. A., & Walker, D. W. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.06.035 · Cited by 54 · see citing works
Self-citation
Hearing Loss in Low-Birth-Weight Infants
Anagnostakis, D. (1982) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1982.03970430034009 · Cited by 51 · see citing works
Brain damage markers in children. Neurobiological and clinical aspects
Leviton, A. E., & Dammann, O. (2002) · Acta Paediatrica · doi:10.1111/j.1651-2227.2002.tb01630.x · Cited by 49 · see citing works
BDNF and TrkB protein expression is altered in the fetal hippocampus but not cerebellum after chronic prenatal compromise
Dieni, S., & Rees, S. M. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.06.003 · Cited by 44 · see citing works
Self-citation
Developments in Tryptophan and Serotonin Metabolism
Allegri, G., Ragazzi, E., COSTA, C. V. L., et al. (2003) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-0135-0 · Cited by 44 · see citing works
Reverse Operation of the Na+ ‐Ca2+ Exchanger Mediates Ca 2+ Influx during Anoxia in Mammalian CNS White Mattera
Stys, P. K., Waxman, S. G., & Ransom, B. R. (1991) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1991.tb17321.x · Cited by 40 · see citing works
Effects of Exposure to Chronic Placental Insufficiency on the Postnatal Brain and Retina in Sheep
Duncan, J. R., Cock, M. L., Loeliger, M. M., Louey, S., Harding, R., & Rees, S. M. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.11.1131 · Cited by 33 · see citing works
Self-citation
Neuropathology of the near-term and midgestation ovine fetal brain after sustained in utero hypoxemia
Penning, D. H., Grafe, M. R., Hammond, R. R., et al. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(13)90484-1 · Cited by 30 · see citing works
Chronic placental insufficiency has long-term effects on auditory function in the guinea pig
Rehn, A., Loeliger, M. M., Hardie, N. A., Rees, S. M., Dieni, S., & Shepherd, R. K. (2002) · Hearing Research · doi:10.1016/s0378-5955(02)00312-x · Cited by 23 · see citing works
Self-citation
Altered retinal function and structure after chronic placental insufficiency.
Bui, B. V., Rees, S. M., Loeliger, M. M., et al. (2002) · PubMed · Cited by 22 · see citing works
Self-citation
Increased mRNA Expression of Kynurenine Pathway Enzymes in Human Placentae Exposed To Bacterial Endotoxin
Manuelpillai, U., Wallace, E. M., Nicholls, T., et al. (2003) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-0135-0_9 · Cited by 21 · see citing works
Regional changes in kynurenic acid, quinolinic acid, and glial fibrillary acidic protein concentrations in the fetal sheep brain after experimentally induced placental insufficiency
Nicholls, T., Lacey, B., Nitsos, I., Smythe, G. A., & Walker, D. W. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.108862 · Cited by 19 · see citing works
Self-citation
Assessment of learning ability and behaviour in low birthweight lambs following intrauterine growth restriction
Camm, E. J., Gibbs, M. E., Cock, M. L., et al. (2001) · Reproduction Fertility and Development · doi:10.1071/rd99092 · Cited by 16 · see citing works
Kynurenine production and catabolism in fetal sheep with embolized or nonembolized placentas
Nicholls, T., Nitsos, I., Smythe, G. A., & Walker, D. W. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.117969 · Cited by 16 · see citing works
Self-citation
Origins of Cerebral Palsy
Goodlin, R. C. (1990) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1990.02150290012004 · Cited by 15 · see citing works
Effects of Umbilical Cord Occlusion in Late Gestation on the Ovine Fetal Brain and Retina
Duncan, J. R., Camm, E. J., Loeliger, M. M., Cock, M. L., Harding, R., & Rees, S. M. (2004) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2004.03.004 · Cited by 12 · see citing works
Self-citation
Structural Imaging Findings and Macroscopic Pathology
Hopkins, R., & Lewis, S. W. (2000) · doi:10.1093/oso/9780192629074.003.0002 · Cited by 9 · see citing works
Neuropathology and the Neurodevelopmental Model
Akil, M., & Weinberger, D. R. (2000) · doi:10.1093/oso/9780192629074.003.0009 · Cited by 5 · see citing works
Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights substrates of disability
Sperfeld (1999) · Pure Amsterdam UMC · doi:10.1002/1531-8249(199911)46:5 · Cited by 2 · see citing works

Flagged first, then by citations

Sorted by citations

High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children.
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.010 · Cited by 435 · see citing works
The impact of environmental factors in severe psychiatric disorders
Schmitt, A., Malchow, B., Hasan, A., & Falkai, P. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00019 · Cited by 322 · see citing works
Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age
Buss, C., Davis, E. P., Hobel, C. J., & Sandman, C. A. (2011) · Stress · doi:10.3109/10253890.2011.623250 · Cited by 289 · see citing works
The Programming Power of the Placenta
Sferruzzi-Perri, A. N., & Camm, E. J. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00033 · Cited by 223 · see citing works
Role of Prenatal Hypoxia in Brain Development, Cognitive Functions, and Neurodegeneration
Nalivaeva, N. N., Turner, A. J., & Zhuravin, I. A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00825 · Cited by 181 · see citing works
Exploring early human brain development with structural and physiological neuroimaging
Vasung, L., Abaci Turk, E., Ferradal, S. L., Sutin, J., Stout, J. N., Ahtam, B., Lin, P.-Y., & Grant, P. E. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.07.041 · Cited by 177 · see citing works

Neuroprotective effects of the survival promoting peptide Y-P30
Schneeberg, J., Riek‐Burchardt, M., Braun, H., Landgraf, P., Kreutz, M. R., & Reymann, K. G. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.05.029 · Cited by 8 · see citing works
Neuroprotective Properties of Chitosan and Its Derivatives
Pangestuti, R., & Kim, S. (2010) · Marine Drugs · doi:10.3390/md8072117 · Cited by 173 · see citing works
POTENTIAL NEUROPROTECTIVE EFFECTS OF HERBAL COMPOUNDS
Baibado, J. T., & Cheung, H. (2015) · International Journal of Pharmaceutical and Biological Science Archive
P587. Altered Intracerebellar White Matter Fibers in Psychotic Disorders
Shinn, A. K., Zhang, F., Goldenberg, J. E., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.02.824
Postconditioning with repeated mild hypoxia protects neonatal hypoxia-ischemic rats against brain damage and promotes rehabilitation of brain function
Deng, Q., Chang, Y., Cheng, X., et al. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.02.006 · Cited by 15 · see citing works

Authors: Rees, S., Harding, R., & Walker, D.
Affiliations: The University of Melbourne (AU)
Monash University (AU)
Corresponding author: Rees, Sandra
ORCID: Harding, Richard
Venue: International Journal of Developmental Neuroscience
Publisher: Wiley
Published: 2007-09-29
Volume: 26
Issue: 1
Pages: 3-11
ISSN: 0736-5748 (ISSN-L)
1873-474X
DOI: 10.1016/j.ijdevneu.2007.08.020
OpenAlex: W2018648849
Cited by: 160
References: 94
Citations by year: 2026: 5 · 2025: 8 · 2024: 11 · 2023: 8 · 2022: 6 · 2021: 3 · 2020: 5 · 2019: 9 · 2018: 9 · 2017: 5 · 2016: 9 · 2015: 7 · 2014: 13 · 2013: 10 · 2012: 17
FWCI: 1.18
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: International Journal of Developmental Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Health and Medical Research Council
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: fetal brain development, hypoxia-ischemia, fetal hypoxia, placental insufficiency, fetal growth restriction, neuroinflammation, prenatal infection, white matter injury, neuronal cell death, myelination, neuronal connectivity, neuroprotection
MeSH terms: Animals, Brain, Brain Injuries, Critical Period, Psychological, Disease Models, Animal, Female, Humans, Infant, Newborn, Placental Insufficiency, Pregnancy, Fetal Development, Prenatal Injuries

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

An adverse intrauterine environment: implications for injury and altered development of the brain

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks