Tracking regional brain growth up to age 13 in children born term and very preterm

Serial regional brain growth from the newborn period to adolescence has not been described. Here, we measured regional brain growth in 216 very preterm (VP) and 45 full-term (FT) children. Brain MRI was performed at term-equivalent age, 7 and 13 years in 82 regions. Brain volumes increased between term-equivalent and 7 years, with faster growth in the FT than VP group. Perinatal brain abnormality was associated with less increase in brain volume between term-equivalent and 7 years in the VP group. Between 7 and 13 years, volumes were relatively stable, with some subcortical and cortical regions increasing while others reduced. Notably, VP infants continued to lag, with overall brain size generally less than that of FT peers at 13 years. Parieto–frontal growth, mainly between 7 and 13 years in FT children, was associated with higher intelligence at 13 years. This study improves understanding of typical and atypical regional brain growth. In this longitudinal study, the authors tracked the course of brain development from birth to adolescence (age 13 years) and examined the effects of very preterm birth. Very preterm children showed slower brain growth from age 0 (term equivalent) to age 7.

[1]  Gehan Roberts,et al.  Rates of early intervention services in very preterm children with developmental disabilities at age 2 years , 2008, Journal of paediatrics and child health.

[2]  Andrew Zalesky,et al.  Structural connectivity relates to perinatal factors and functional impairment at 7years in children born very preterm , 2016, NeuroImage.

[3]  Alan Connelly,et al.  Contribution of Brain Size to IQ and Educational Underperformance in Extremely Preterm Adolescents , 2013, PloS one.

[4]  Daniel A. Hackman,et al.  Socioeconomic Status and the Developing Brain , 2022 .

[5]  L. D. de Vries,et al.  Brain tissue volumes in preterm infants: prematurity, perinatal risk factors and neurodevelopmental outcome: A systematic review , 2012, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[6]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[7]  Deanne K. Thompson,et al.  Examination of the Pattern of Growth of Cerebral Tissue Volumes From Hospital Discharge to Early Childhood in Very Preterm Infants. , 2016, JAMA pediatrics.

[8]  Christopher N Martyn,et al.  The Influence of Head Growth in Fetal Life, Infancy, and Childhood on Intelligence at the Ages of 4 and 8 Years , 2006, Pediatrics.

[9]  John H. Gilmore,et al.  Imaging structural and functional brain development in early childhood , 2018, Nature Reviews Neuroscience.

[10]  T J Cole,et al.  British 1990 growth reference centiles for weight, height, body mass index and head circumference fitted by maximum penalized likelihood. , 1998, Statistics in medicine.

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

[12]  Live Eikenes,et al.  Cortical trajectories during adolescence in preterm born teenagers with very low birthweight , 2016, Cortex.

[13]  J. Rapoport,et al.  Structural MRI of Pediatric Brain Development: What Have We Learned and Where Are We Going? , 2010, Neuron.

[14]  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.

[15]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[16]  Margot J. Taylor,et al.  Neuroanatomical consequences of very preterm birth in middle childhood , 2012, Brain Structure and Function.

[17]  N. Makris,et al.  Regional infant brain development: an MRI-based morphometric analysis in 3 to 13 month olds. , 2013, Cerebral cortex.

[18]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[19]  Koenraad Van Leemput,et al.  A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI , 2015, NeuroImage.

[20]  Karen F. Berman,et al.  Regional Variations in Brain Gyrification Are Associated with General Cognitive Ability in Humans , 2016, Current Biology.

[21]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

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

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

[24]  Chiara Nosarti,et al.  Alterations in cortical thickness development in preterm-born individuals: Implications for high-order cognitive functions , 2015, NeuroImage.

[25]  Chris Adamson,et al.  A new neonatal cortical and subcortical brain atlas: the Melbourne Children's Regional Infant Brain (M-CRIB) atlas , 2017, NeuroImage.

[26]  Hiroyuki Kidokoro,et al.  Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different neonatal intensive care unit environments. , 2014, The Journal of pediatrics.

[27]  L. Papile,et al.  Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. , 1978, The Journal of pediatrics.

[28]  F. Gilles,et al.  Gyral development of the human brain , 1977, Transactions of the American Neurological Association.

[29]  J. Oosterlaan,et al.  Cognitive Outcomes of Children Born Extremely or Very Preterm Since the 1990s and Associated Risk Factors: A Meta-analysis and Meta-regression , 2018, JAMA pediatrics.

[30]  J. Skranes,et al.  Trajectories of brain development in school-age children born preterm with very low birth weight , 2018, Scientific Reports.

[31]  Y. Benjamini,et al.  Controlling the false discovery rate in behavior genetics research , 2001, Behavioural Brain Research.

[32]  Z. Pavlova,et al.  Two‐Year Outcome of Infants Weighing 600 Grams or Less at Birth and Born 1994 Through 1998 , 2003, Obstetrics and gynecology.

[33]  S. Back.  Cerebral white and gray matter injury in newborns: new insights into pathophysiology and management. , 2014, Clinics in perinatology.

[34]  Michael C. Stevens,et al.  Adolescent maturation of the relationship between cortical gyrification and cognitive ability , 2017, NeuroImage.

[35]  Huibert D. Mansvelder,et al.  Genes, Cells and Brain Areas of Intelligence , 2019, Front. Hum. Neurosci..

[36]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[37]  D. Kennedy,et al.  The human brain age 7-11 years: a volumetric analysis based on magnetic resonance images. , 1996, Cerebral cortex.

[38]  M. Viergever,et al.  Robustness of Automated Methods for Brain Volume Measurements across Different MRI Field Strengths , 2016, PloS one.

[39]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[40]  W R Shankle,et al.  Developmental patterns in the cytoarchitecture of the human cerebral cortex from birth to 6 years examined by correspondence analysis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Simon K. Warfield,et al.  Simultaneous Truth and Performance Level Estimation Through Fusion of Probabilistic Segmentations , 2013, IEEE Transactions on Medical Imaging.

[42]  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.

[43]  Megha Sharda,et al.  Imaging Brain Development: Benefiting from Individual Variability , 2015, Journal of experimental neuroscience.

[44]  Deanne K. Thompson,et al.  Longitudinal Preterm Cerebellar Volume: Perinatal and Neurodevelopmental Outcome Associations , 2018, Cerebellum.

[45]  Norbert Schuff,et al.  Bayesian segmentation of brainstem structures in MRI , 2015, NeuroImage.

[46]  Jian Chen,et al.  Early life predictors of brain development at term-equivalent age in infants born across the gestational age spectrum , 2019, NeuroImage.

[47]  Paul M. Thompson,et al.  Volumetric grey matter alterations in adolescents and adults born very preterm suggest accelerated brain maturation , 2017, NeuroImage.

[48]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.

[49]  Simon K. Warfield,et al.  Changes in neonatal regional brain volume associated with preterm birth and perinatal factors , 2019, NeuroImage.

[50]  Olaf Sporns,et al.  Children's intellectual ability is associated with structural network integrity , 2016, NeuroImage.

[51]  Martin Voracek,et al.  Meta-analysis of associations between human brain volume and intelligence differences: How strong are they and what do they mean? , 2015, Neuroscience & Biobehavioral Reviews.

[52]  G. Ball,et al.  Exploring the multiple-hit hypothesis of preterm white matter damage using diffusion MRI , 2017, NeuroImage: Clinical.

[53]  Rebecca C. Knickmeyer,et al.  A Structural MRI Study of Human Brain Development from Birth to 2 Years , 2008, The Journal of Neuroscience.

[54]  M. Mallar Chakravarty,et al.  Normative brain size variation and brain shape diversity in humans , 2018, Science.

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

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

[57]  Heidi Furre Østgård,et al.  Fetal Growth, Cognitive Function, and Brain Volumes in Childhood and Adolescence , 2015, Obstetrics and gynecology.

[58]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[59]  Lillian G. Matthews,et al.  Brain growth in the NICU: critical periods of tissue-specific expansion , 2018, Pediatric Research.

[60]  Chiara Nosarti,et al.  Preterm birth and structural brain alterations in early adulthood , 2014, NeuroImage: Clinical.

[61]  J. Neil,et al.  New MR Imaging Assessment Tool to Define Brain Abnormalities in Very Preterm Infants at Term , 2013, American Journal of Neuroradiology.

[62]  Frederik Barkhof,et al.  Global and Regional Differences in Brain Anatomy of Young Children Born Small for Gestational Age , 2011, PloS one.

[63]  R. Haier,et al.  The Parieto-Frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence , 2007, Behavioral and Brain Sciences.