Extremely Preterm Birth Outcome: A Review of Four Decades of Cognitive Research

Premature birth incidence and survival rates are increasing steadily due to advances in obstetric and neonatal intensive care. Those born at the limits of viability are highly at-risk of adverse neurocognitive function over their lifespan, leading to current controversy regarding aggressive resuscitation efforts for these extremely preterm children. However, data from earlier generation cohorts who were born in substantially different eras of neonatal intensive care cannot be relied on to predict outcome of today’s newborn. Our review by the crucial variable of birth cohort year shows a changing developmental trajectory in which today’s extremely preterm survivor is likely to have fewer severe medical complications, better neurological outcomes, and fewer adverse cognitive late effects. Such data further underscore the importance of concurrently considering medical, familial, socioenvironmental, and neurobiological factors in combination with individual neonatal intensive care center protocols when studying outcomes of the preterm child. This complex, interrelated range of factors directly affects the immature, rapidly developing premature brain. However, ongoing surveillance to detect subsequent delay or impairment and to apply interventional strategies early in the developmental course holds promise for further enhancement of functional outcome.

[1]  S. Levison,et al.  Astrocytes and developmental white matter disorders. , 2006, Mental retardation and developmental disabilities research reviews.

[2]  K. Stjernqvist,et al.  Developmental outcome, child behaviour and mother-child interaction at 3 years of age following Newborn Individualized Developmental Care and Intervention Program (NIDCAP) intervention. , 2000, Early human development.

[3]  P. Grimaud [Cerebral palsy]. , 1972, Pediatrie.

[4]  J. Volpe Encephalopathy of Prematurity Includes Neuronal Abnormalities , 2005, Pediatrics.

[5]  J. Martin,et al.  Births: preliminary data for 2005. , 2006, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[6]  David L. Streiner,et al.  Transition of Extremely Low-Birth-Weight Infants From Adolescence to Young Adulthood: Comparison With Normal Birth-Weight Controls , 2006 .

[7]  A. Fanaroff,et al.  Outcomes of extremely low birth weight infants. , 1996, Pediatrics.

[8]  G. Greisen,et al.  Intellectual Development in a Danish Cohort of Prematurely Born Preschool Children: Specific or General Difficulties? , 2006, Journal of developmental and behavioral pediatrics : JDBP.

[9]  S. le Cessie,et al.  Effects of Individualized Developmental Care in a Randomized Trial of Preterm Infants <32 Weeks , 2009, Pediatrics.

[10]  E. Hille,et al.  School performance at nine years of age in very premature and very low birth weight infants: perinatal risk factors and predictors at five years of age. Collaborative Project on Preterm and Small for Gestational Age (POPS) Infants in The Netherlands. , 1994, The Journal of pediatrics.

[11]  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.

[12]  I. Baron,et al.  Improved Outcomes of Extremely Low Birth Weight Infants , 2007, Pediatrics.

[13]  R. Piecuch,et al.  Outcome of Infants Born at 24‐26 Weeks' Gestation: II. Neurodevelopmental Outcome , 1997, Obstetrics and gynecology.

[14]  Mijna Hadders-Algra,et al.  Ontogeny of the human central nervous system: what is happening when? , 2006, Early human development.

[15]  P. Groneck,et al.  Association of Histologic Chorioamnionitis, Increased Levels of Cord Blood Cytokines, and Intracerebral Hemorrhage in Preterm Neonates , 2003, Neonatology.

[16]  L. M. Daniel,et al.  Eight-year outcome of very-low-birth-weight infants born in KK hospital. , 2003, Annals of the Academy of Medicine, Singapore.

[17]  B. Vohr,et al.  Neurodevelopmental and school performance of very low-birth-weight infants: a seven-year longitudinal study. , 1985, Pediatrics.

[18]  M. Msall,et al.  The spectrum of behavioral outcomes after extreme prematurity: regulatory, attention, social, and adaptive dimensions. , 2008, Seminars in perinatology.

[19]  J. Wyatt,et al.  Neuropsychological outcome at adolescence of very preterm birth and its relation to brain structure. , 2001, Developmental medicine and child neurology.

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

[21]  J. Wit,et al.  Mortality and neurologic, mental, and psychomotor development at 2 years in infants born less than 27 weeks' gestation: the Leiden follow-up project on prematurity. , 2003, Pediatrics.

[22]  D. Streiner,et al.  School difficulties at adolescence in a regional cohort of children who were extremely low birth weight. , 2000, Pediatrics.

[23]  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.

[24]  L. Doyle Changing availability of neonatal intensive care for extremely low birthweight infants in Victoria over two decades , 2004, The Medical journal of Australia.

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

[26]  D. Wolke,et al.  Prognosis of the very low birthweight baby in relation to gender. , 1986, Archives of disease in childhood.

[27]  T. Yeh,et al.  Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. , 2004, The New England journal of medicine.

[28]  Patterns of brain injury in neonates exposed to perinatal sentinel events , 2007 .

[29]  Christopher Schatschneider,et al.  School-Age Outcomes in Children with Birth Weights under 750 g , 1994 .

[30]  J. Evans,et al.  Surfactant era (1990–2002) 2-year outcomes of infants less than 1500 g from a Community Level 3 Neonatal Intensive Care Unit , 2006, Journal of Perinatology.

[31]  B. Caravale,et al.  Cognitive development in low risk preterm infants at 3–4 years of life , 2005, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[32]  Bruce Fischl,et al.  Segmental brain volumes and cognitive and perceptual correlates in 15-year-old adolescents with low birth weight. , 2009, The Journal of pediatrics.

[33]  F. Lefebvre,et al.  OUTCOME AT SCHOOL AGE OF CHILDREN WITH BIRTHWEIGHTS OF 1000 GRAMS OR LESS , 1988, Developmental medicine and child neurology.

[34]  M. Kaminski,et al.  Behavioral Outcome at 3 Years of Age in Very Preterm Infants: The EPIPAGE Study , 2006, Pediatrics.

[35]  David V Glidden,et al.  Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. , 2004, The Journal of pediatrics.

[36]  R. Butler,et al.  Attentional processes and their remediation in children treated for cancer: A literature review and the development of a therapeutic approach , 2002, Journal of the International Neuropsychological Society.

[37]  J. Martin,et al.  Births: preliminary data for 2007. , 2009 .

[38]  C. J. Wang,et al.  Factors influencing the enrollment of eligible extremely-low-birth-weight children in the part C early intervention program. , 2009, Academic pediatrics.

[39]  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.

[40]  P. P. Berg,et al.  Neurologic and Developmental Disability at Six Years of Age After Extremely Preterm Birth , 2006 .

[41]  D. J. Goldstein,et al.  Survival and major neurodevelopmental impairment in extremely low gestational age newborns born 1990–2000: a retrospective cohort study , 2007, BMC pediatrics.

[42]  T. Sutcliffe Neurodevelopmental Outcomes of Extremely Low Birth Weight Infants <32 Weeks' Gestation Between 1993 and 1998 , 2006 .

[43]  B. Vohr,et al.  Lasting Effects of Preterm Birth and Neonatal Brain Hemorrhage at 12 Years of Age , 2009, Pediatrics.

[44]  R. Mulhern,et al.  A multicenter, randomized clinical trial of a cognitive remediation program for childhood survivors of a pediatric malignancy. , 2008, Journal of consulting and clinical psychology.

[45]  Victoria in Outcome at 2 years of children 23–27 weeks' gestation born in Victoria in 1991–92 , 1997, Journal of paediatrics and child health.

[46]  D. Miller,et al.  Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm , 1999, The Lancet.

[47]  Marit Korkman,et al.  Neurodevelopmental Outcome at 5 Years of Age of a National Cohort of Extremely Low Birth Weight Infants Who Were Born in 1996–1997 , 2005, Pediatrics.

[48]  Jed A. Meltzer,et al.  A Functional Magnetic Resonance Imaging Study of the Long-term Influences of Early Indomethacin Exposure on Language Processing in the Brains of Prematurely Born Children , 2006, Pediatrics.

[49]  D. Ferriero Neonatal brain injury. , 2004, The New England journal of medicine.

[50]  Steven P. Miller,et al.  Neonatal Encephalopathy: Association of Cytokines with MR Spectroscopy and Outcome , 2004, Pediatric Research.

[51]  Linda S de Vries,et al.  Functional Outcomes and Participation in Young Adulthood for Very Preterm and Very Low Birth Weight Infants: The Dutch Project on Preterm and Small for Gestational Age Infants at 19 Years of Age , 2007, Pediatrics.

[52]  S. Lindgren,et al.  Long-term neuropsychological outcome of high risk infants with intracranial hemorrhage. , 1992, Journal of pediatric psychology.

[53]  S. Wardle,et al.  Increased survival and deteriorating developmental outcome in 23 to 25 week old gestation infants, 1990–4 compared with 1984–9 , 1998, Archives of disease in childhood. Fetal and neonatal edition.

[54]  K. Stjernqvist,et al.  Ten‐year follow‐up of children born before 29 gestational weeks: health, cognitive development, behaviour and school achievement , 1999, Acta paediatrica.

[55]  Timo Saarela,et al.  No Improvement in Outcome of Nationwide Extremely Low Birth Weight Infant Populations Between 1996–1997 and 1999–2000 , 2007, Pediatrics.

[56]  R. Brand,et al.  Outcome of very preterm small for gestational age infants: the first nine years of life , 1998, British journal of obstetrics and gynaecology.

[57]  V. Fellman,et al.  Inflammation at Birth is Associated With Subnormal Development in Very Preterm Infants , 2008, Pediatric Research.

[58]  Susan Foster-Cohen,et al.  Early delayed language development in very preterm infants: Evidence from the MacArthur-Bates CDI* , 2007, Journal of Child Language.

[59]  M. Nageotte,et al.  Outcomes of extremely low-birth-weight infants between 500 and 750 g. , 2000, American journal of obstetrics and gynecology.

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

[61]  R. E. Hoekstra,et al.  Survival and long-term neurodevelopmental outcome of extremely premature infants born at 23-26 weeks' gestational age at a tertiary center. , 2004, Pediatrics.

[62]  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.

[63]  H. Lagercrantz,et al.  Neonatal individualized care in practice: a Swedish experience. , 2002, Seminars in neonatology : SN.

[64]  J. Dungan,et al.  Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study , 2009 .

[65]  B. Vohr,et al.  Outcome of extremely-low-birth-weight infants at highest risk: Gestational age ≤24 weeks, birth weight ≤750 g, and 1-minute Apgar ≤3 , 2004 .

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

[67]  A. Bhutta,et al.  Abnormal cognition and behavior in preterm neonates linked to smaller brain volumes , 2001, Trends in Neurosciences.

[68]  D. Wolke,et al.  FIVE‐YEAR FOLLOW‐UP STUDY OF EXTREMELY LOW‐BIRTHWEIGHT INFANTS , 1988, Developmental medicine and child neurology.

[69]  D. J. Goldstein,et al.  Follow-up of a Randomized, Placebo-Controlled Trial of Dexamethasone to Decrease the Duration of Ventilator Dependency in Very Low Birth Weight Infants: Neurodevelopmental Outcomes at 4 to 11 Years of Age , 2007, Pediatrics.

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

[71]  L. Wrage,et al.  Growth in the Neonatal Intensive Care Unit Influences Neurodevelopmental and Growth Outcomes of Extremely Low Birth Weight Infants , 2006, Pediatrics.

[72]  P. Szatmari,et al.  Psychiatric disorders at five years among children with birthweights less than 1000g: a regional perspective. , 1990, Developmental medicine and child neurology.

[73]  M. Schluchter,et al.  Improved Neurodevelopmental Outcomes for Extremely Low Birth Weight Infants in 2000–2002 , 2007, Pediatrics.

[74]  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.

[75]  M. Hack,et al.  Attention deficits in children with <750 gm birth weight. , 1998 .

[76]  K. Barrington The adverse neuro-developmental effects of postnatal steroids in the preterm infant: a systematic review of RCTs , 2001, BMC pediatrics.

[77]  M. Borchert,et al.  Neurology of the Newborn, 5th Edition , 2010 .

[78]  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.

[79]  M. New,et al.  Cognitive and motor development of children with and without congenital adrenal hyperplasia after early-prenatal dexamethasone. , 2004, The Journal of clinical endocrinology and metabolism.

[80]  A. Gunn,et al.  Destruction and reconstruction: hypoxia and the developing brain. , 2007, Birth defects research. Part C, Embryo today : reviews.

[81]  P. P. Berg Proactive Management Promotes Outcome in Extremely Preterm Infants: A Population-Based Comparison of Two Perinatal Management Strategies , 2006 .

[82]  J. Bowen,et al.  Educational outcome at 8 years for children who were born extremely prematurely: A controlled study , 2002, Journal of paediatrics and child health.

[83]  Scottish Neonatal Consultants,et al.  Risk adjusted and population based studies of the outcome for high risk infants in Scotland and Australia , 2000, Archives of disease in childhood. Fetal and neonatal edition.

[84]  B. Vohr,et al.  Transition of Extremely Low-Birth-Weight Infants From Adolescence to Young Adulthood: Comparison With Normal Birth-Weight Controls , 2007 .

[85]  T. Inder,et al.  Executive functioning in preschool children born very preterm: Relationship with early white matter pathology , 2007, Journal of the International Neuropsychological Society.

[86]  Catalina J. Hooper,et al.  The development of nonverbal working memory and executive control processes in adolescents. , 2005, Child development.

[87]  G. Little Perinatal care at the threshold of viability , 1996, Pediatrics.

[88]  S. Teplin,et al.  Neurodevelopmental, health, and growth status at age 6 years of children with birth weights less than 1001 grams. , 1991, The Journal of pediatrics.

[89]  K. Evankovich,et al.  Behavioral effects of prematurity. , 1997, Seminars in perinatology.

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

[91]  H. Lagercrantz,et al.  Indications of improved cognitive development at one year of age among infants born very prematurely who received care based on the Newborn Individualized Developmental Care and Assessment Program (NIDCAP). , 2002, Early human development.

[92]  A. Bhutta,et al.  Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. , 2002, JAMA.

[93]  P. Szatmari,et al.  PSYCHIATRIC DISORDERS AT FIVE YEARS AMONG CHILDREN WITH BIRTHWEIGHTS < 1OOOg: A REGIONAL PERSPECTIVE , 1990 .

[94]  W. Engle Age Terminology During the Perinatal Period , 2004, Pediatrics.

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

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

[97]  A. C. Primavesi Neurologic and Developmental Disability after Extremely Preterm Birth , 2000 .

[98]  S. Raz,et al.  Extreme prematurity and neuropsychological outcome in the preschool years , 2009, Journal of the International Neuropsychological Society.

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

[100]  Lynn T Singer,et al.  Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes. , 2003, Pediatrics.

[101]  Bernard Guyer,et al.  Annual Summary of Vital Statistics: 2004 , 2006, Pediatrics.

[102]  Allan L. Reiss,et al.  Increased temporal lobe gyrification in preterm children , 2006, Neuropsychologia.

[103]  J. Martin,et al.  Births: final data for 2003. , 2005, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[104]  K. Allegaert,et al.  The EPIBEL Study: Outcomes to Discharge From Hospital for Extremely Preterm Infants in Belgium , 2004, Pediatrics.

[105]  F. Duffy,et al.  Early experience alters brain function and structure. , 2004, Pediatrics.

[106]  L. B. Dahl,et al.  A Randomized, Controlled Trial of the Effectiveness of an Early-Intervention Program in Reducing Parenting Stress After Preterm Birth , 2006, Pediatrics.

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

[108]  H. Halliday,et al.  Surfactants: past, present and future , 2008, Journal of Perinatology.

[109]  E. Eichenwald,et al.  Management and Outcomes of Very Low Birth Weight , 2009 .

[110]  L. Sirota,et al.  Comparative outcome study between triplet and singleton preterm newborns , 2002, Acta paediatrica.

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

[112]  Carles Falcon,et al.  Decreased Regional Brain Volume and Cognitive Impairment in Preterm Children at Low Risk , 2009, Pediatrics.

[113]  N. Marlow,et al.  Neurodevelopmental Disability Through 11 Years of Age in Children Born Before 26 Weeks of Gestation , 2009, Pediatrics.

[114]  M. Smrkovsky,et al.  Effects of biological and social factors on the cognitive development of very low birth weight children. , 1993, Pediatrics.

[115]  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.

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

[117]  H. Craig,et al.  Performances of Low-Income, African American Preschool and Kindergarten Children on the Peabody Picture Vocabulary Test-Revised , 1992 .

[118]  N. Marlow,et al.  Neurodevelopmental and Respiratory Follow-up Results at 7 Years for Children From the United Kingdom and Ireland Enrolled in a Randomized Trial of Early and Late Postnatal Corticosteroid Treatment, Systemic and Inhaled (the Open Study of Early Corticosteroid Treatment) , 2006, Pediatrics.

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

[120]  B. Vohr,et al.  Center differences and outcomes of extremely low birth weight infants. , 2004, Pediatrics.

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

[122]  M. Johnston,et al.  Plasticity in the developing brain: implications for rehabilitation. , 2009, Developmental disabilities research reviews.

[123]  Sutton,et al.  Population‐based study of infants born at less than 28 weeks’ gestation in New South Wales, Australia, in 1992–3 , 1999 .

[124]  Stefano Vicari,et al.  Spatial working memory deficits in children at ages 3-4 who were low birth weight, preterm infants. , 2004, Neuropsychology.

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

[126]  B. Vohr,et al.  Unimpaired Outcomes for Extremely Low Birth Weight Infants at 18 to 22 Months , 2009, Pediatrics.

[127]  Anne Martin,et al.  Early Intervention in Low Birth Weight Premature Infants: Results at 18 Years of Age for the Infant Health and Development Program , 2006, Pediatrics.

[128]  J. Tyson,et al.  Outcomes for extremely low-birth-weight infants: disappointing news. , 2005, JAMA.

[129]  D. Streiner,et al.  School-age outcomes in children who were extremely low birth weight from four international population-based cohorts. , 2003, Pediatrics.

[130]  B. Vohr,et al.  Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993-1994. , 2000, Pediatrics.

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

[132]  E. Draper,et al.  Health status of a population of infants born before 26 weeks gestation derived from routine data collected between 21 and 27 months post-delivery. , 1999, Early human development.

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

[134]  H. Taylor,et al.  Functional limitations and special health care needs of 10- to 14-year-old children weighing less than 750 grams at birth. , 2000, Pediatrics.

[135]  A. Fanaroff,et al.  Outcomes of extremely-low-birth-weight infants between 1982 and 1988. , 1989, The New England journal of medicine.

[136]  V. Pierrat,et al.  Factors Associated With Neurodevelopmental Outcome at 2 Years After Very Preterm Birth: The Population-Based Nord-Pas-de-Calais EPIPAGE Cohort , 2006, Pediatrics.

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

[138]  M. Lewis,et al.  Early risk, attention, and brain activation in adolescents born preterm. , 2006, Child development.

[139]  Alan R Fleischman,et al.  Surgeon General’s Conference on the Prevention of Preterm Birth , 2009, Obstetrics and gynecology.

[140]  J. Lumley,et al.  The survival of extremely‐low‐birthweight infants in Victoria: 1982–1985 , 1988, The Medical journal of Australia.

[141]  B. Vohr,et al.  Bias in reported neurodevelopmental outcomes among extremely low birth weight survivors. , 2004, Pediatrics.

[142]  L. Mutch,et al.  SCHOOL ATTAINMENT, COGNITIVE ABILITY AND MOTOR FUNCTION IN A TOTAL SCOTTISH VERYLOW‐BIRTHWEIGHT POPULATION AT EIGHT YEARS: A CONTROLLED STUDY , 1995, Developmental medicine and child neurology.

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

[144]  D. Ferriero,et al.  Selective vulnerability in the developing central nervous system. , 2004, Pediatric neurology.

[145]  R. Romero,et al.  Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy , 1997 .

[146]  H. Kilbride,et al.  Preschool outcome of less than 801-gram preterm infants compared with full-term siblings. , 2004, Pediatrics.

[147]  A. Fanaroff,et al.  Outcomes of children of extremely low birthweight and gestational age in the 1990's. , 1999, Early human development.

[148]  J. Volpe,et al.  Pathogenesis of cerebral white matter injury of prematurity , 2007, Archives of Disease in Childhood Fetal and Neonatal Edition.

[149]  I. Singh,et al.  Neuroprotective Interventions: Is It Too Late? , 2009, Journal of child neurology.

[150]  Controversies and Advances in Neonatal Neurology: Introduction , 2009 .

[151]  H. Roeyers,et al.  Outcome at 3 Years of Age in a Population-Based Cohort of Extremely Preterm Infants , 2007, Obstetrics and gynecology.

[152]  T. Inder,et al.  Mechanisms of perinatal brain injury. , 2000, Seminars in neonatology : SN.

[153]  N. Marlow,et al.  Specific language difficulties and school achievement in children born at 25 weeks of gestation or less. , 2008, The Journal of pediatrics.

[154]  N. Svenningsen,et al.  Neurobehavioural development at term of extremely low-birthweight infants (less than 901g). , 1990, Developmental medicine and child neurology.

[155]  B. Peter,et al.  Perinatal care improves the outcome of triplets. , 2002, European journal of obstetrics, gynecology, and reproductive biology.

[156]  J. Stockman Early Death, Morbidity, and Need of Treatment Among Extremely Premature Infants , 2006 .

[157]  Barbara J. Stoll,et al.  Neurodevelopmental Outcome of Extremely Low Birth Weight Infants With Posthemorrhagic Hydrocephalus Requiring Shunt Insertion , 2008, Pediatrics.

[158]  Toshihito Suzuki,et al.  The (CTG)n polymorphism in the NOTCH4 gene is not associated with schizophrenia in Japanese individuals , 2001, BMC psychiatry.

[159]  John E. Desmond,et al.  Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks , 2005, NeuroImage.

[160]  ACOG practice bulletin. Perinatal care at the threshold of viability. Number 38, September 2002. American College of Obstetrics and Gynecology. , 2002, International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics.

[161]  N. Bargalló,et al.  Proton Magnetic Resonance Spectroscopy Reveals Medial Temporal Metabolic Abnormalities in Adolescents With History of Preterm Birth , 2008, Pediatric Research.

[162]  O. Dammann,et al.  Fetal Inflammatory Response and Brain Injury in the Preterm Newborn , 2009, Journal of child neurology.

[163]  R. Nickel,et al.  School performance of children with birth weights of 1,000 g or less. , 1982, American journal of diseases of children.

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

[165]  Monica Luciana,et al.  Working Memory Performance in Typically Developing Children and Adolescents: Behavioral Evidence of Protracted Frontal Lobe Development , 2007, Developmental neuropsychology.

[166]  J. Stockman Intensive Care for Extreme Prematurity — Moving Beyond Gestational Age , 2010 .

[167]  D. J. Goldstein,et al.  Survival and developmental disability in infants with birth weights of 501 to 800 grams, born between 1979 and 1994. , 1997, Pediatrics.

[168]  N. Svenningsen,et al.  Neurobehavioural Development At Term Of Extremely Low‐Birthweight Infants (<901G) , 1990 .

[169]  L. Doyle,et al.  The Obstetrician and the Extremely Immature Fetus (24–26 weeks): Outcome to 5 Years of Age , 1994, The Australian & New Zealand journal of obstetrics & gynaecology.

[170]  T. O'Shea,et al.  SNAP-II and SNAPPE-II and the Risk of Structural and Functional Brain Disorders in Extremely Low Gestational Age Newborns: The ELGAN Study , 2009, Neonatology.

[171]  J. Lau,et al.  Criteria for determining disability in infants and children: low birth weight. , 2002, Evidence report/technology assessment.

[172]  L. Doyle,et al.  Executive functioning in school-aged children who were born very preterm or with extremely low birth weight in the 1990s. , 2004, Pediatrics.

[173]  A. Harvey,et al.  Prefrontal lesions and attentional skills in childhood , 2005, Journal of the International Neuropsychological Society.

[174]  H. Forssberg,et al.  Impulse control, working memory and other executive functions in preterm children when starting school , 2004, Acta paediatrica.

[175]  S. Håkansson,et al.  Proactive management promotes outcome in extremely preterm infants: a population-based comparison of two perinatal management strategies. , 2004, Pediatrics.

[176]  L. Papile Quantification of Deep Gray Matter in Preterm Infants at Term-Equivalent Age Using Manual Volumetry of 3-Tesla Magnetic Resonance Images , 2008 .

[177]  J. Fawke Neurological outcomes following preterm birth. , 2007, Seminars in fetal & neonatal medicine.

[178]  F. Duffy,et al.  A Three-Center, Randomized, Controlled Trial of Individualized Developmental Care for Very Low Birth Weight Preterm Infants: Medical, Neurodevelopmental, Parenting, and Caregiving Effects , 2003, Journal of developmental and behavioral pediatrics : JDBP.

[179]  B LOGAN,et al.  Obstetrics and Gynecology , 1917, Edinburgh Medical Journal.

[180]  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.

[181]  W. Engle,et al.  “Late-Preterm” Infants: A Population at Risk , 2007, Pediatrics.

[182]  R. E. Hoekstra,et al.  Survival and follow‐up of infants born at 23 to 26 weeks of gestational age: Effects of surfactant therapy , 1994, The Journal of pediatrics.

[183]  Ronald F Lamont,et al.  Looking to the future , 2003, BJOG : an international journal of obstetrics and gynaecology.

[184]  M. Giannì,et al.  Twelve-Month Neurofunctional Assessment and Cognitive Performance at 36 Months of Age in Extremely Low Birth Weight Infants , 2007, Pediatrics.

[185]  K. Stjernqvist,et al.  Extremely low–birth–weight infants less than 901 g: development and behaviour after 4 years of life , 1995, Acta paediatrica.

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

[187]  K. Stjernqvist,et al.  Extremely low‐birth‐weight infants less than 901 g. Growth and development after one year of life , 1993, Acta paediatrica.

[188]  N. Minich,et al.  Longitudinal outcomes of very low birth weight: Neuropsychological findings , 2004, Journal of the International Neuropsychological Society.

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

[190]  M. New,et al.  Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: Results of a pilot study , 1995, Psychoneuroendocrinology.

[191]  L. Kreienbrock,et al.  Population based study on the outcome of small for gestational age newborns , 2004, Archives of Disease in Childhood - Fetal and Neonatal Edition.

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

[193]  R. Rosychuk,et al.  Improvement of Short- and Long-Term Outcomes for Very Low Birth Weight Infants: Edmonton NIDCAP Trial , 2009, Pediatrics.

[194]  Karen E. Smith,et al.  Responsive parenting: establishing early foundations for social, communication, and independent problem-solving skills. , 2006, Developmental psychology.

[195]  Saroj Saigal,et al.  An overview of mortality and sequelae of preterm birth from infancy to adulthood , 2008, The Lancet.

[196]  N Marlow,et al.  The EPICure study: growth and associated problems in children born at 25 weeks of gestational age or less , 2003, Archives of disease in childhood. Fetal and neonatal edition.

[197]  N. Paneth,et al.  The Lingering Academic Deficits of Low Birth Weight Children , 2004, Pediatrics.

[198]  Effects of antenatal dexamethasone administration in the infant: long-term follow-up. , 1984, The Journal of pediatrics.

[199]  Joan Stiles,et al.  The Fundamentals of Brain Development: Integrating Nature and Nurture , 2008 .

[200]  D. Hoyert,et al.  Annual Summary of Vital Statistics: 2006 , 2008, Pediatrics.

[201]  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.

[202]  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.

[203]  J. Wyatt,et al.  Survival and neurodevelopmental morbidity at 1 year of age following extremely preterm delivery over a 20‐year period: a single centre cohort study , 2008, Acta paediatrica.

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

[205]  R. Mulhern,et al.  Neuropsychological status of children treated for brain tumors: a critical review and integrative analysis. , 1992, Medical and pediatric oncology.

[206]  M. Whitfield,et al.  Perinatal outcomes of a large cohort of extremely low gestational age infants (twenty-three to twenty-eight completed weeks of gestation). , 1994, The Journal of pediatrics.

[207]  S. Back,et al.  Maturation-Dependent Vulnerability of Perinatal White Matter in Premature Birth , 2007, Stroke.

[208]  B. Bajuk,et al.  Population-based study of infants born at less than 28 weeks' gestation in New South Wales, Australia, in 1992-3. New South Wales Neonatal Intensive Care Unit Study Group. , 1999, Paediatric and perinatal epidemiology.

[209]  R. Cooke,et al.  Perinatal and postnatal factors in very preterm infants and subsequent cognitive and motor abilities , 2004, Archives of Disease in Childhood - Fetal and Neonatal Edition.

[210]  K. Stjernqvist Extremely low birth weight infants less than 901 g. Impact on the family during the first year , 1992, Scandinavian journal of social medicine.

[211]  J. Oosterlaan,et al.  Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children , 2009, Pediatrics.

[212]  H. Mohay,et al.  Executive function of children with extremely low birthweight: a case control study , 1999, Developmental medicine and child neurology.

[213]  G. Sedin,et al.  Mental Health and Social Competencies of 10- to 12-Year-Old Children Born at 23 to 25 Weeks of Gestation in the 1990s: A Swedish National Prospective Follow-up Study , 2007, Pediatrics.

[214]  N. Paneth,et al.  A quantitative review of mortality and developmental disability in extremely premature newborns. , 1998, Archives of pediatrics & adolescent medicine.

[215]  S. Verhulst,et al.  Outcome studies of low birth weight infants published in the last decade: a metaanalysis. , 1989, The Journal of pediatrics.

[216]  I. Baron,et al.  Visuospatial and verbal fluency relative deficits in 'complicated' late-preterm preschool children. , 2009, Early human development.

[217]  R. Grunau,et al.  Pattern of learning disabilities in children with extremely low birth weight and broadly average intelligence. , 2002, Archives of pediatrics & adolescent medicine.

[218]  M. Castillo,et al.  Hypoxic-ischemic brain injury: imaging findings from birth to adulthood. , 2008, Radiographics : a review publication of the Radiological Society of North America, Inc.

[219]  Assuring Healthy Outcomes,et al.  Preterm Birth : Causes , Consequences , and Prevention , 2005 .

[220]  L. Calzà,et al.  Prenatal glucocorticoid exposure affects learning and vulnerability of cholinergic neurons , 2007, Neurobiology of Aging.

[221]  I. Baron,et al.  Age-appropriate early school age neurobehavioral outcomes of extremely preterm birth without severe intraventricular hemorrhage: a single center experience. , 2009, Early human development.

[222]  S. Brophy,et al.  Interventions for latent autoimmune diabetes (LADA) in adults. , 2011, The Cochrane database of systematic reviews.

[223]  Chiara Nosarti,et al.  Vermis and lateral lobes of the cerebellum in adolescents born very preterm , 2005, Neuroreport.

[224]  Mónica Giménez,et al.  Hippocampal gray matter reduction associates with memory deficits in adolescents with history of prematurity , 2004, NeuroImage.

[225]  J. Kaempf,et al.  Medical Staff Guidelines for Periviability Pregnancy Counseling and Medical Treatment of Extremely Premature Infants , 2006, Pediatrics.

[226]  Y. Burns,et al.  The association between early minor motor difficulties in extreme low birth weight infants and school age attentional difficulties. , 2006, Early human development.

[227]  A. Jobe Postnatal corticosteroids for preterm infants--do what we say, not what we do. , 2004, The New England journal of medicine.

[228]  Survival of very tiny babies--good news and bad news. , 1994, The New England journal of medicine.

[229]  M. Msall Measuring functional skills in preschool children at risk for neurodevelopmental disabilities. , 2005, Mental retardation and developmental disabilities research reviews.

[230]  R. Romero,et al.  Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. , 1997, American journal of obstetrics and gynecology.

[231]  A. Edwards,et al.  RELATION BETWEEN ULTRASOUND APPEARANCE OF THE BRAIN OF VERY PRETERM INFANTS AND NEURODEVELOPMENTAL IMPARIMENT AT EIGHT YEARS , 1993, Developmental medicine and child neurology.

[232]  P. Rezaie,et al.  Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system , 2002, Neuropathology : official journal of the Japanese Society of Neuropathology.

[233]  D. Batton Antenatal Counseling Regarding Resuscitation at an Extremely Low Gestational Age , 2009, Pediatrics.

[234]  T. Hirai,et al.  MR signal intensity of the perirolandic cortex in the neonate and infant , 1996, Neuroradiology.

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

[236]  J. Stockman,et al.  Chronic Conditions, Functional Limitations, and Special Health Care Needs of School-aged Children Born With Extremely Low-Birth-Weight in the 1990s , 2007 .

[237]  L. Doyle,et al.  Early developmental intervention programs post hospital discharge to prevent motor and cognitive impairments in preterm infants. , 2008, The Cochrane database of systematic reviews.

[238]  A. Leviton,et al.  Neuroimaging and the prediction of outcomes in preterm infants. , 2006, The New England journal of medicine.

[239]  A. Neubauer,et al.  Outcome of extremely low birth weight survivors at school age: the influence of perinatal parameters on neurodevelopment , 2007, European Journal of Pediatrics.

[240]  M. Pezzani,et al.  Management of extremely low‐birth‐weight infants , 1992, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[241]  Renate Meyer,et al.  Behavioural problems in children who weigh 1000 g or less at birth in four countries , 2001, The Lancet.

[242]  R. Plomin,et al.  The interaction of prematurity with genetic and environmental influences on cognitive development in twins. , 2000, The Journal of pediatrics.

[243]  M. Schluchter,et al.  The Impact of Extremely Low Birth Weight on the Families of School-Aged Children , 2006, Pediatrics.