Neuroimaging and neurodevelopmental outcomes in preterm infants.

Imaging of the preterm infant brain has advanced dramatically beyond the earliest era of transillumination. Computed tomography (CT), a crucial innovation during the early 1970s, allowed noninvasive visualization of intracerebral lesions, particularly hemorrhage. The capability to document brain injury in the preterm infant led to better clarification of links to developmental outcomes. With the development of cranial ultrasound (CUS), and more recently, magnetic resonance imaging (MRI), CT is used rarely for imaging the brain of preterm infants. Despite extensive experience with neonatal neuroimaging, significant questions still remain. Substantial controversies exist pertaining to when and how neuroimaging should be performed and how images should be interpreted.

[1]  J. Volpe Brain injury in the premature infant. Neuropathology, clinical aspects, pathogenesis, and prevention. , 1997, Clinics in perinatology.

[2]  J. Volpe,et al.  Neurobiology of Periventricular Leukomalacia in the Premature Infant , 2001, Pediatric Research.

[3]  P. Grant,et al.  Practice parameter: Neuroimaging of the neonate , 2002 .

[4]  Mary A. Rutherford,et al.  MRI of the Neonatal Brain , 2001 .

[5]  J. Rozé,et al.  Limitations of ultrasonography for diagnosing white matter damage in preterm infants , 2003, Archives of disease in childhood. Fetal and neonatal edition.

[6]  J. Bodensteiner,et al.  Cerebellar Injury in the Extremely Premature Infant: Newly Recognized but Relatively Common Outcome , 2005, Journal of child neurology.

[7]  L. D. de Vries,et al.  Ultrasound abnormalities preceding cerebral palsy in high-risk preterm infants. , 2004, The Journal of pediatrics.

[8]  Steven P. Miller,et al.  Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. , 2003, AJNR. American journal of neuroradiology.

[9]  B. Vohr,et al.  Neurodevelopmental Outcomes of Extremely Low Birth Weight Infants <32 Weeks’ Gestation Between 1993 and 1998 , 2005, Pediatrics.

[10]  Rebecca D Folkerth,et al.  Axonal development in the cerebral white matter of the human fetus and infant , 2005, The Journal of comparative neurology.

[11]  Gérard Bréart,et al.  Cerebral Palsy Among Very Preterm Children in Relation to Gestational Age and Neonatal Ultrasound Abnormalities: The EPIPAGE Cohort Study , 2006, Pediatrics.

[12]  P. Barnes Neuroimaging and the Timing of Fetal and Neonatal Brain Injury , 2001, Journal of Perinatology.

[13]  F. R. Zadik FRACTURE OF THE FEMORAL NECK. , 1964, Lancet.

[14]  G. Enríquez,et al.  Posterior fontanelle sonography: an acoustic window into the neonatal brain. , 2004, AJNR. American journal of neuroradiology.

[15]  C. Cans Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers , 2000, Developmental medicine and child 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]  J. Volpe Encephalopathy of Prematurity Includes Neuronal Abnormalities , 2005, Pediatrics.

[18]  L. D. de Vries,et al.  Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. , 1999, Neuropediatrics.

[19]  J. Dubois,et al.  Diffusion tensor imaging of brain development. , 2006, Seminars in fetal & neonatal medicine.

[20]  A J Barkovich,et al.  MR imaging of the neonatal brain. , 2006, Neuroimaging clinics of North America.

[21]  M. Platt Surveillance of cerebral palsy in Europe. A European collaboration of cerebral palsy surveys and registers. , 2000 .

[22]  L. D. de Vries,et al.  Unilateral parenchymal haemorrhagic infarction in the preterm infant. , 2001, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[23]  D. Wilson‐Costello,et al.  Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. , 2006, The Journal of pediatrics.

[24]  Mark Schluchter,et al.  Poor Predictive Validity of the Bayley Scales of Infant Development for Cognitive Function of Extremely Low Birth Weight Children at School Age , 2005, Pediatrics.

[25]  J. Volpe Cerebral white matter injury of the premature infant-more common than you think. , 2003, Pediatrics.

[26]  J. Pinto-Martin,et al.  Relation of cranial ultrasound abnormalities in low‐birthweight infants to motor or cognitive performance at ages 2, 6, and 9 years , 1999, Developmental medicine and child neurology.

[27]  F. Cowan,et al.  Should cranial MRI screening of preterm infants become routine? , 2007, Nature Clinical Practice Neurology.

[28]  F. Cowan,et al.  Comparison of Findings on Cranial Ultrasound and Magnetic Resonance Imaging in Preterm Infants , 2001, Pediatrics.

[29]  B. Vohr,et al.  Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. , 2004, JAMA.

[30]  B. Vohr,et al.  Changes in Neurodevelopmental Outcomes at 18 to 22 Months' Corrected Age Among Infants of Less Than 25 Weeks' Gestational Age Born in 1993–1999 , 2005, Pediatrics.

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

[32]  J. Valk,et al.  Early MR features of hypoxic-ischemic brain injury in neonates with periventricular densities on sonograms. , 2000, AJNR. American journal of neuroradiology.

[33]  C. Limperopoulos,et al.  Disorders of cerebellar growth and development , 2006, Current opinion in pediatrics.

[34]  B. Vohr,et al.  School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial. , 2003, Pediatrics.

[35]  P. Grant,et al.  Practice parameter: Neuroimaging of the neonate: Report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society , 2002, Neurology.

[36]  J. Volpe,et al.  Cerebellar Hemorrhage in the Preterm Infant: Ultrasonographic Findings and Risk Factors , 2005, Pediatrics.

[37]  Kuniyoshi Kuno,et al.  Quantitative evaluation of thalami and basal ganglia in infants with periventricular leukomalacia , 2001, Developmental medicine and child neurology.

[38]  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.

[39]  L. Vainionpää,et al.  Magnetic resonance imaging at term and neuromotor outcome in preterm infants , 2000, Acta paediatrica.

[40]  L. Cornette,et al.  Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. , 2001, Clinical radiology.

[41]  M. Moseley,et al.  Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. , 2003, AJNR. American journal of neuroradiology.

[42]  Michael D. Ernst,et al.  Ultrasound diagnosis and neurodevelopmental outcome of localised and extensive cystic periventricular leucomalacia , 2001, Archives of disease in childhood. Fetal and neonatal edition.

[43]  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.

[44]  S. Back,et al.  Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. , 2006, Mental retardation and developmental disabilities research reviews.

[45]  M. Schluchter,et al.  Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g: 1992-1995. , 2000, Archives of pediatrics & adolescent medicine.

[46]  N. Gelman,et al.  Uncomplicated Intraventricular Hemorrhage Is Followed by Reduced Cortical Volume at Near-Term Age , 2004, Pediatrics.

[47]  L. Doyle,et al.  Neurodevelopmental sequelae of intraventricular haemorrhage at 8 years of age in a regional cohort of ELBW/very preterm infants. , 2005, Early human development.

[48]  Donald N. Di Salvo,et al.  A New View of the Neonatal Brain: Clinical Utility of Supplemental Neurologic US Imaging Windows , 2001 .

[49]  J. Perlman,et al.  Surveillance protocol for the detection of intracranial abnormalities in premature neonates. , 2000, Archives of pediatrics & adolescent medicine.

[50]  J. Bodensteiner,et al.  Frequency and Nature of Cerebellar Injury in the Extremely Premature Survivor with Cerebral Palsy , 2005, Journal of child neurology.

[51]  A. Sandler Neurodevelopment and predictors of outcomes of children with birth weights of less that 1000 g , 2001 .

[52]  A. Mildner,et al.  Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes , 2007, Nature Genetics.

[53]  Abhik Das,et al.  Interobserver reliability and accuracy of cranial ultrasound scanning interpretation in premature infants. , 2007, The Journal of pediatrics.

[54]  G. Wezel-Meijler,et al.  Hyperechogenicity of the thalamus and basal ganglia in very preterm infants: radiological findings and short-term neurological outcome. , 2004, Neuropediatrics.

[55]  C. Shatz,et al.  Selective Vulnerability of Subplate Neurons after Early Neonatal Hypoxia-Ischemia , 2003, The Journal of Neuroscience.

[56]  N. Marlow,et al.  Neurologic and developmental disability at six years of age after extremely preterm birth. , 2005, The New England journal of medicine.

[57]  J. Saul,et al.  Fluctuating Pressure-Passivity Is Common in the Cerebral Circulation of Sick Premature Infants , 2007, Pediatric Research.

[58]  S. Roth,et al.  Neurodevelopmental outcome of preterm infants with ventricular dilatation with and without associated haemorrhage , 2006, Developmental Medicine & Child Neurology.

[59]  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.

[60]  A. Hart,et al.  Predictive Value of Neonatal MRI with Respect to Late MRI Findings and Clinical Outcome. A Study in Infants with Periventricular Densities on Neonatal Ultrasound , 2005, Neuropediatrics.

[61]  P. VandenBerg,et al.  Neurologic and Developmental Disability at Six Years of Age After Extremely Preterm Birth , 2005 .

[62]  T. O'Shea,et al.  RELIABILITY OF INTERPRETATION OF CRANIAL ULTRASOUND EXAMINATIONS OF VERY LOW‐BIRTHWEIGHT NEONATES , 1993, Developmental medicine and child neurology.

[63]  E. Reynolds,et al.  ULTRASOUND DETECTION OF BRAIN DAMAGE IN PRETERM INFANTS , 1979, The Lancet.

[64]  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.

[65]  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.

[66]  K. Nave,et al.  Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination , 2003, Nature Genetics.

[67]  N Marlow,et al.  The EPICure study: associations and antecedents of neurological and developmental disability at 30 months of age following extremely preterm birth , 2005, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[68]  L. D. de Vries,et al.  Parenchymal brain injury in the preterm infant: comparison of cranial ultrasound, MRI and neurodevelopmental outcome. , 2001, Neuropediatrics.

[69]  R. Lasky,et al.  Intraobserver and interobserver reliability in assessment of neonatal cranial ultrasounds. , 1991, Early human development.

[70]  J. Perlman,et al.  Linear hyperechogenicity within the basal ganglia and thalamus of preterm infants. , 2000, Pediatric neurology.

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

[72]  C. Verney,et al.  Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection , 2003, Neuroscience.

[73]  B. Vohr,et al.  Neurodevelopmental and Growth Outcomes of Extremely Low Birth Weight Infants After Necrotizing Enterocolitis , 2005, Pediatrics.

[74]  D. Vigneron,et al.  Magnetic resonance imaging compatible neonate incubator , 2002 .

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

[76]  A. Barkovich,et al.  Profound asphyxia in the premature infant: imaging findings. , 1995, AJNR. American journal of neuroradiology.

[77]  Patrick D Barnes,et al.  Neonatal Brain Magnetic Resonance Imaging Before Discharge Is Better Than Serial Cranial Ultrasound in Predicting Cerebral Palsy in Very Low Birth Weight Preterm Infants , 2004, Pediatrics.

[78]  L. Papile,et al.  Fluctuating Pressure-Passivity Is Common in the Cerebral Circulation of Sick Premature Infants , 2008 .

[79]  T. Inder,et al.  White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. , 2003, AJNR. American journal of neuroradiology.

[80]  E Kazam,et al.  White matter disorders of prematurity: association with intraventricular hemorrhage and ventriculomegaly. The Developmental Epidemiology Network. , 1999, The Journal of pediatrics.

[81]  M. Schluchter,et al.  Consequences and Risks of <1000-g Birth Weight for Neuropsychological Skills, Achievement, and Adaptive Functioning , 2006, Journal of developmental and behavioral pediatrics : JDBP.

[82]  Namasivayam Ambalavanan,et al.  Prediction of Neurologic Morbidity in Extremely Low Birth Weight Infants , 2000, Journal of Perinatology.

[83]  Daniel Rueckert,et al.  Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry , 2006, NeuroImage.

[84]  J. Pinto-Martin,et al.  Neonatal cranial ultrasound abnormalities in low birth weight infants: relation to cognitive outcomes at six years of age. , 1996, Pediatrics.

[85]  L. Kuhns,et al.  Real-time sonography of the brain through the anterior fontanelle. , 1981, AJR. American journal of roentgenology.

[86]  R. Arthur Magnetic resonance imaging in preterm infants , 2006, Pediatric Radiology.

[87]  Marvin D Nelson,et al.  MR imaging of newborns by using an MR-compatible incubator with integrated radiofrequency coils: initial experience. , 2004, Radiology.

[88]  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.

[89]  P. Grant,et al.  Practice parameter: Neuroimaging of the neonate: Report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society , 2002 .

[90]  B. Popko Myelin: not just a conduit for conduction , 2003, Nature Genetics.

[91]  D. D. Di Salvo A new view of the neonatal brain: clinical utility of supplemental neurologic US imaging windows. , 2001, Radiographics : a review publication of the Radiological Society of North America, Inc.

[92]  T. Inder,et al.  Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. , 2006, The New England journal of medicine.

[93]  R. Goldstein,et al.  Sonographic visualization of neonatal posterior fossa abnormalities through the posterolateral fontanelle. , 2000, AJR. American journal of roentgenology.

[94]  Deanne K. Thompson,et al.  Reduction in Cerebellar Volumes in Preterm Infants: Relationship to White Matter Injury and Neurodevelopment at Two Years of Age , 2006, Pediatric Research.

[95]  G. Sébire,et al.  Cytokine immunoreactivity in cortical and subcortical neurons in periventricular leukomalacia: are cytokines implicated in neuronal dysfunction in cerebral palsy? , 2003, Acta Neuropathologica.

[96]  A. Leviton,et al.  Characteristics of cranial ultrasound white‐matter echolucencies that predict disability: a review , 1999, Developmental medicine and child neurology.

[97]  S. Shankaran,et al.  Adverse Neurodevelopmental Outcomes Among Extremely Low Birth Weight Infants With a Normal Head Ultrasound: Prevalence and Antecedents , 2005, Pediatrics.

[98]  S. Wallenstein,et al.  Interobserver variability in neonatal cranial ultrasonography. , 1988, Paediatric and perinatal epidemiology.

[99]  G. Dawson,et al.  Practice parameter: Screening and diagnosis of autism , 2000, Neurology.

[100]  L. D. de Vries,et al.  Using cerebral ultrasound effectively in the newborn infant. , 2006, Early human development.

[101]  Yoshiaki Sato,et al.  Magnetic Resonance Imaging Regional T1 Abnormalities at Term Accurately Predict Motor Outcome in Preterm Infants , 2007, Pediatrics.

[102]  C. Barnewolt,et al.  Use of the mastoid fontanelle for improved sonographic visualization of the neonatal midbrain and posterior fossa. , 1997, AJR. American journal of roentgenology.

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

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