Brain Volumes in Adolescents With Very Low Birth Weight: Effects on Brain Structure and Associations With Neuropsychological Outcomes

The aims of this study were to examine abnormalities in brain structure in adolescents and young adults with very low birth weight (VLBW, <1,500 g) and associations of these abnormalities with neuropsychological outcomes. The sample of 108 participants from 14 to 19 years of age included 37 participants with <750 g birth weight, 35 with 750–1,499 g birth weight, and 36 normal birth weight (NBW) controls. One or both of the VLBW groups had smaller brain volumes, larger lateral ventricles, and a small surface area of the corpus callosum than the NBW controls. Group differences in white matter (WM) structures, subcortical gray matter (GM), and the cerebellum were found even when controlling for whole brain volume (WBV), and were most pronounced in the <750 g group. WM reductions in the two VLBW groups relative to NBW controls were associated with more pervasive cognitive deficits than were reductions in subcortical GM. Associations of cognitive outcomes with structural abnormalities remained when controlling for WBV or neonatal risks. The results are consistent with previous findings of residual brain abnormalities in adolescents and young adults with VLBW and provide new information on their cognitive correlates.

[1]  G. Aylward,et al.  Neurodevelopmental Outcomes of Infants Born Prematurely , 2005, Journal of developmental and behavioral pediatrics : JDBP.

[2]  H. Levin.  A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary , 1993 .

[3]  Serena J Counsell,et al.  Severity of perinatal illness and cerebral cortical growth in preterm infants , 2009, Acta paediatrica.

[4]  T. Bohan,et al.  Effects of intraventricular hemorrhage and hydrocephalus on the long‐term neurobehavioral development of preterm very‐low‐birthweight infants , 1997, Developmental medicine and child neurology.

[5]  Simon K Warfield,et al.  Neonate hippocampal volumes: Prematurity, perinatal predictors, and 2‐year outcome , 2008, Annals of neurology.

[6]  R. Kikinis,et al.  Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. , 2001, Pediatrics.

[7]  Núria Bargalló,et al.  Correlations of thalamic reductions with verbal fluency impairment in those born prematurely , 2006, Neuroreport.

[8]  A. Fanaroff,et al.  Object working memory deficits predicted by early brain injury and development in the preterm infant , 2007 .

[9]  Steven P. Miller,et al.  Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. , 2005, The Journal of pediatrics.

[10]  Chiara Nosarti,et al.  Corpus callosum size and very preterm birth: relationship to neuropsychological outcome. , 2004, Brain : a journal of neurology.

[11]  Jason W. Osborne,et al.  Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. , 2005 .

[12]  N. Bargalló,et al.  Patterns of cerebral white matter damage and cognitive impairment in adolescents born very preterm , 2008, International Journal of Developmental Neuroscience.

[13]  R. Fields,et al.  White matter in learning, cognition and psychiatric disorders , 2008, Trends in Neurosciences.

[14]  Alan C. Evans,et al.  Intellectual ability and cortical development in children and adolescents , 2006, Nature.

[15]  A. Dale,et al.  Cerebral cortex thickness in 15-year-old adolescents with low birth weight measured by an automated MRI-based method. , 2005, Brain : a journal of neurology.

[16]  L. Doyle,et al.  Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. , 2003, JAMA.

[17]  Simon K Warfield,et al.  Early Alteration of Structural and Functional Brain Development in Premature Infants Born with Intrauterine Growth Restriction , 2004, Pediatric Research.

[18]  O. Pryds,et al.  Brain lesions in preterms: origin, consequences and compensation , 1999, Acta paediatrica.

[19]  M. Allin,et al.  Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. , 2001, Brain : a journal of neurology.

[20]  B. Vohr,et al.  Neurodevelopmental outcome of the premature infant. , 2009, Pediatric clinics of North America.

[21]  E. Courchesne,et al.  Regional size reduction in the human corpus callosum following pre- and perinatal brain injury. , 2000, Cerebral cortex.

[22]  R Todd Constable,et al.  Longitudinal Brain Volume Changes in Preterm and Term Control Subjects During Late Childhood and Adolescence , 2009, Pediatrics.

[23]  P. Lachenbruch.  Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[24]  Jim Stevenson,et al.  Executive functions in school-age children born very prematurely. , 2007, Early human development.

[25]  P. Filipek,et al.  Long-term neuropsychological outcomes of very low birth weight: Associations with early risks for periventricular brain insults , 2004, Journal of the International Neuropsychological Society.

[26]  D. Kennedy,et al.  The young adult human brain: an MRI-based morphometric analysis. , 1994, Cerebral cortex.

[27]  P. Khong,et al.  White Matter Volume and Anisotropy in Preterm Children: A Pilot Study of Neurocognitive Correlates , 2007, Pediatric Research.

[28]  Judith D. Singer,et al.  Using SAS PROC MIXED to Fit Multilevel Models, Hierarchical Models, and Individual Growth Models , 1998 .

[29]  김의영,et al.  한국인 신경인지기능 평가를 위한 Cambridge Neuropsychological Test Automated Battery(CANTAB)의 신뢰성 평가 , 2012 .

[30]  Joseph Hajnal,et al.  Natural History of Brain Lesions in Extremely Preterm Infants Studied With Serial Magnetic Resonance Imaging From Birth and Neurodevelopmental Assessment , 2006, Pediatrics.

[31]  S. Blakemore,et al.  Development of the adolescent brain: implications for executive function and social cognition. , 2006 .

[32]  B. Vohr,et al.  Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. , 2008, The Journal of pediatrics.

[33]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[34]  O. Spreen,et al.  A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary , 1991 .

[35]  B. J. Casey,et al.  Imaging the developing brain: what have we learned about cognitive development? , 2005, Trends in Cognitive Sciences.

[36]  J. Giedd,et al.  Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging , 2006, Neuroscience & Biobehavioral Reviews.

[37]  Jon Skranes,et al.  White matter abnormalities and executive function in children with very low birth weight , 2009, Neuroreport.

[38]  P. Renshaw,et al.  Volumetric MRI analysis comparing subjects having attention-deficit hyperactivity disorder with normal controls , 1997, Neurology.

[39]  Chiara Nosarti,et al.  Adolescents who were born very preterm have decreased brain volumes. , 2002, Brain : a journal of neurology.

[40]  R. Kikinis,et al.  Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term , 1999, Annals of neurology.

[41]  H. Taylor,et al.  Mathematics deficiencies in children with very low birth weight or very preterm birth. , 2009, Developmental disabilities research reviews.

[42]  Catherine Limperopoulos,et al.  Does Cerebellar Injury in Premature Infants Contribute to the High Prevalence of Long-term Cognitive, Learning, and Behavioral Disability in Survivors? , 2007, Pediatrics.

[43]  Chiara Nosarti,et al.  Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. , 2008, Brain : a journal of neurology.

[44]  C. Junqué,et al.  Corpus callosum and prefrontal functions in adolescents with history of very preterm birth , 2008, Neuropsychologia.

[45]  L J Abernethy,et al.  Quantitative magnetic resonance imaging of the brain in survivors of very low birth weight , 2002, Archives of disease in childhood.

[46]  Christopher J. Cannistraci,et al.  Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. , 2000, JAMA.

[47]  Chiara Nosarti,et al.  Growth of the corpus callosum in adolescents born preterm. , 2007, Archives of pediatrics & adolescent medicine.

[48]  R. Cooke,et al.  Caudate and Hippocampal Volumes, Intelligence, and Motor Impairment in 7-Year-Old Children Who Were Born Preterm , 2004, Pediatric Research.

[49]  D. Ffytche,et al.  The functional significance of perinatal corpus callosum damage: an fMRI study in young adults. , 2002, Brain : a journal of neurology.

[50]  Hong Wang,et al.  Abnormal Cerebral Structure Is Present at Term in Premature Infants , 2005, Pediatrics.

[51]  Núria Bargalló,et al.  White matter volume and concentration reductions in adolescents with history of very preterm birth: A voxel-based morphometry study , 2006, NeuroImage.

[52]  P. Hüppi,et al.  Lung Disease and Brain Development , 2006, Neonatology.

[53]  David J Larkman,et al.  Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. , 2003, Pediatrics.

[54]  Chiara Nosarti,et al.  Neural substrates of visual paired associates in young adults with a history of very preterm birth: Alterations in fronto-parieto-occipital networks and caudate nucleus , 2009, NeuroImage.

[55]  H. Taylor,et al.  Standardization of the contingency naming test (CNT) for school-aged children: a measure of reactive flexibility , 2000 .

[56]  Allan L Reiss,et al.  Sex differences in cerebral volumes of 8-year-olds born preterm. , 2004, The Journal of pediatrics.

[57]  C. Schatschneider,et al.  School-age outcomes in children with birth weights under 750 g. , 1995, The New England journal of medicine.

[58]  D G Gadian,et al.  Calculation difficulties in children of very low birthweight: a neural correlate. , 2001, Brain : a journal of neurology.

[59]  Jaap Oosterlaan,et al.  Executive Function in Very Preterm Children at Early School Age , 2009, Journal of abnormal child psychology.

[60]  Joshua I. Breier,et al.  Neocortical reorganization in spina bifida , 2008, NeuroImage.

[61]  B. Casey.  Disruption of inhibitory control in developmental disorders: A mechanistic model of implicated frontostriatal circuitry. , 2001 .

[62]  Chiara Nosarti,et al.  Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. , 2008, Brain : a journal of neurology.

[63]  A. B. Hollingshead,et al.  Four factor index of social status , 1975 .

[64]  H. Forssberg,et al.  Preterm Children Have Disturbances of White Matter at 11 Years of Age as Shown by Diffusion Tensor Imaging , 2003, Pediatric Research.

[65]  Deanne K. Thompson,et al.  Perinatal risk factors altering regional brain structure in the preterm infant. , 2006, Brain : a journal of neurology.

[66]  J. Volpe.  Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances , 2009, The Lancet Neurology.

[67]  T. Inder,et al.  Defining the nature of the cerebral abnormalities in the premature infant: a qualitative magnetic resonance imaging study. , 2003, Jornal de Pediatria.

[68]  S. F. Witelson.  Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[69]  F. McLean,et al.  Intrauterine growth of live-born Caucasian infants at sea level: standards obtained from measurements in 7 dimensions of infants born between 25 and 44 weeks of gestation. , 1969, The Journal of pediatrics.

[70]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[71]  M. Gappa,et al.  Lung and brain damage in preterm newborns, and their association with gestational age, prematurity subgroup, infection/inflammation and long term outcome , 2005, BJOG : an international journal of obstetrics and gynaecology.

[72]  B. J. Casey,et al.  Structural and functional brain development and its relation to cognitive development , 2000, Biological Psychology.

[73]  J. Volpe.  Neurology of the Newborn , 1959, Major problems in clinical pediatrics.

[74]  Maxwell P. Henderson,et al.  Effects of very low birthweight on brain structure in adulthood. , 2004, Developmental medicine and child neurology.

[75]  F. Lazeyras,et al.  Structural and Functional Brain Development After Hydrocortisone Treatment for Neonatal Chronic Lung Disease , 2005, Pediatrics.

[76]  E. Melhem,et al.  Periventricular leukomalacia: relationship between lateral ventricular volume on brain MR images and severity of cognitive and motor impairment. , 2000, Radiology.

[77]  B. Vohr,et al.  Volumetric analysis of regional cerebral development in preterm children. , 2004, Pediatric neurology.

[78]  N. Minich,et al.  Middle-school-age outcomes in children with very low birthweight. , 2000, Child development.

[79]  M. Luciana.  Practitioner review: computerized assessment of neuropsychological function in children: clinical and research applications of the Cambridge Neuropsychological Testing Automated Battery (CANTAB). , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[80]  Chiara Nosarti,et al.  Brain volumes in adult survivors of very low birth weight: a sibling-controlled study. , 2004, Pediatrics.

[81]  F. Cowan,et al.  Reduced development of cerebral cortex in extremely preterm infants , 2000, The Lancet.

[82]  J. Sattler.  Assessment of Children , 1992 .

[83]  Deanne K. Thompson,et al.  Preterm infant hippocampal volumes correlate with later working memory deficits. , 2008, Brain : a journal of neurology.

[84]  Terrie E Inder,et al.  Defining the nature of the cerebral abnormalities in the premature infant: a qualitative magnetic resonance imaging study. , 2003, The Journal of pediatrics.

[85]  Richard L Robertson,et al.  Late Gestation Cerebellar Growth Is Rapid and Impeded by Premature Birth , 2005, Pediatrics.

[86]  J. Allsop,et al.  Quantification of Deep Gray Matter in Preterm Infants at Term-Equivalent Age Using Manual Volumetry of 3-Tesla Magnetic Resonance Images , 2007, Pediatrics.

[87]  Chiara Nosarti,et al.  Impaired executive functioning in young adults born very preterm , 2007, Journal of the International Neuropsychological Society.

[88]  Jane Holmes Bernstein,et al.  Developmental Test of Visual-Motor Integration , 2010, Encyclopedia of Autism Spectrum Disorders.

[89]  M. Mishkin,et al.  Developmental amnesia associated with early hypoxic-ischaemic injury. , 2000, Brain : a journal of neurology.

[90]  Comprehensive Assessment of Spoken Language (casl) , 2022 .

[91]  Peter Mariën,et al.  Cerebellar neurocognition: Insights into the bottom of the brain , 2008, Clinical Neurology and Neurosurgery.

[92]  Judy Reilly,et al.  Cognitive development following early brain injury: evidence for neural adaptation , 2005, Trends in Cognitive Sciences.

[93]  A. Dale,et al.  Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. , 2007, Brain : a journal of neurology.

[94]  Alan Lucas,et al.  Hippocampal Volume and Everyday Memory in Children of Very Low Birth Weight , 2000, Pediatric Research.

[95]  A. Anderson,et al.  Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. , 2003, Pediatrics.

[96]  K C Schneider,et al.  The Etiology and Outcome of Cerebral Ventriculomegaly at Term in Very Low Birth Weight Preterm Infants , 1999, Pediatrics.

[97]  A. Kaufman,et al.  Short Forms of the K-ABC Mental Processing and Achievement Scales at Ages 4 to 12½ Years for Clinical and Screening Purposes , 1988 .

[98]  R. Gardner.  The objective diagnosis of minimal brain dysfunction , 1979 .

[99]  Richard L Robertson,et al.  Impaired Trophic Interactions Between the Cerebellum and the Cerebrum Among Preterm Infants , 2005, Pediatrics.

[100]  H. Kinney,et al.  Late Oligodendrocyte Progenitors Coincide with the Developmental Window of Vulnerability for Human Perinatal White Matter Injury , 2001, The Journal of Neuroscience.