Neurobehavioral deficits in premature graduates of intensive care--potential medical and neonatal environmental risk factors.

There is growing evidence that a large number of very low birth weight infants are exhibiting neurobehavioral problems in the absence of cerebral palsy at follow-up that has extended into school age and adolescence. Many clinical factors (ie, chronic lung disease, recurrent apnea and bradycardia, transient hypothyroxemia of prematurity, hyperbilirubinemia, nutritional deficiencies, glucocorticoid exposure), as well as stressful environmental conditions, including infant-provider interaction, constant noise, and bright light, may act in combination to impact on the developing brain, even in the absence of overt hemorrhage and/or ischemia. Any potential intervention strategy designed to prevent cognitive and behavioral problems has to account for the numerous biological and clinical conditions and/or interventions, as well as postdischarge social and environmental influences.

[1]  B. Vohr,et al.  Survival and neonatal morbidity at the limits of viability in the mid 1990s: 22 to 25 weeks. , 2000, The Journal of pediatrics.

[2]  Ana M. García,et al.  Noise levels in an urban hospital and workers' subjective responses. , 1995, Archives of environmental health.

[3]  T. Powell,et al.  The connexions of the striatum and globus pallidus: synthesis and speculation. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  R. Sapolsky Why Stress Is Bad for Your Brain , 1996, Science.

[5]  G. Naulaers,et al.  L-Thyroxine Treatment of Preterm Newborns: Clinical and Endocrine Effects , 1997, Pediatric Research.

[6]  N. Rutter,et al.  Effect of night and day on preterm infants in a newborn nursery: randomised trial. , 1986, British medical journal.

[7]  A. Campagnoni,et al.  Essential fatty acid deficiency: effects of cross-fostering mice at birth on myelin levels and composition. , 1983, The Journal of nutrition.

[8]  T. Yeh,et al.  Early dexamethasone therapy in preterm infants: a follow-up study. , 1998, Pediatrics.

[9]  M. Meaney,et al.  The role of serotonin in the development and environmental regulation of type II corticosteroid receptor binding in rat hippocampus. , 1990, Brain research. Developmental brain research.

[10]  S. Dunlop,et al.  Repeated prenatal corticosteroids delay myelination in the ovine central nervous system. , 1997, The Journal of maternal-fetal medicine.

[11]  D. Stevenson,et al.  Individualized Developmental Care for Very-Low-Birth-Weight Premature Infants , 1995, Clinical pediatrics.

[12]  L. Gray,et al.  The effect of an intensive care unit sound environment on the development of habituation in healthy avian neonates. , 1994, Developmental psychobiology.

[13]  F. Duffy,et al.  Effectiveness of individualized developmental care for low-risk preterm infants: behavioral and electrophysiologic evidence. , 1995, Pediatrics.

[14]  F. Bess,et al.  Further observations on noise levels in infant incubators. , 1979, Pediatrics.

[15]  P. Wainwright,et al.  Neonatal dietary zinc deficiency in artificially reared rat pups retards behavioral development and interacts with essential fatty acid deficiency to alter liver and brain fatty acid composition. , 1999, The Journal of nutrition.

[16]  P. Calabresi,et al.  Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: Evidence for D1 receptor involvement , 1987, Neuroscience.

[17]  R. Brand,et al.  The Relation between Neonatal Thyroxine Levels and Neurodevelopmental Outcome at Age 5 and 9 Years in a National Cohort of Very Preterm and/or Very Low Birth Weight Infants , 1996, Pediatric Research.

[18]  K. Fuxe,et al.  Prenatal corticosterone treatment induces long-term changes in spontaneous and apomorphine-mediated motor activity in male and female rats , 1997, Neuroscience.

[19]  R. Uauy,et al.  Essential fatty acid metabolism in the micropremie. , 2000, Clinics in perinatology.

[20]  G. Shaw,et al.  Music Enhances Spatial-Temporal Reasoning: Towards a Neurophysiological Basis Using EEG , 1999, Clinical EEG.

[21]  A. Lucas,et al.  Low triiodothyronine concentration in preterm infants and subsequent intelligence quotient (IQ) at 8 year follow up , 1996, BMJ.

[22]  F. Rauscher,et al.  Music and spatial task performance , 1993, Nature.

[23]  S. Matthews Antenatal Glucocorticoids and Programming of the Developing CNS , 2000, Pediatric Research.

[24]  F. Dekker,et al.  Effects of thyroxine supplementation on neurologic development in infants born at less than 30 weeks' gestation. , 1997, The New England journal of medicine.

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

[26]  R. Sapolsky,et al.  Glucocorticoids Increase the Accumulation of Reactive Oxygen Species and Enhance Adriamycin-Induced Toxicity in Neuronal Culture , 1996, Experimental Neurology.

[27]  W. Cashore,et al.  Dose-effect relationship of bilirubin on striatal synaptosomes in rats. , 1994, Biology of the neonate.

[28]  R. Cooke Trends in incidence of cranial ultrasound lesions and cerebral palsy in very low birthweight infants 1982–93 , 1999, Archives of disease in childhood. Fetal and neonatal edition.

[29]  R. Wennberg,et al.  Bilirubin-Induced Changes in Brain Energy Metabolism after Osmotic Opening of the Blood-Brain Barrier , 1991, Pediatric Research.

[30]  L. Lilien,et al.  A longitudinal study of developmental outcome of infants with bronchopulmonary dysplasia and very low birth weight. , 1997, Pediatrics.

[31]  S. Balian,et al.  Responses of Premature Infants to Routine Nursing Interventions And Noise in the NICU , 1995, Nursing research.

[32]  H. Halliday Clinical Trials of Postnatal Corticosteroids: Inhaled and Systemic , 1999, Neonatology.

[33]  W. Young,et al.  Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[34]  G Maura,et al.  Release-regulating D-2 dopamine receptors are located on striatal glutamatergic nerve terminals. , 1988, The Journal of pharmacology and experimental therapeutics.

[35]  R W Cooke,et al.  Cranial magnetic resonance imaging and school performance in very low birth weight infants in adolescence , 1999, Archives of disease in childhood. Fetal and neonatal edition.

[36]  C. Shatz,et al.  A role for subplate neurons in the patterning of connections from thalamus to neocortex. , 1993, Development.

[37]  D. Stevenson,et al.  Bilirubin Toxicity and Differentiation of Cultured Astrocytes , 1999, Journal of Perinatology.

[38]  T. Field Massage Therapy for Infants and Children , 1995, Journal of developmental and behavioral pediatrics : JDBP.

[39]  S. Rivkees,et al.  Newborn primate infants are entrained by low intensity lighting. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Tyson,et al.  Very low birth weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, January 1993 through December 1994 , 1998 .

[41]  I. Weiler,et al.  Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. , 1995, Brain research. Molecular brain research.

[42]  J. Olney,et al.  Glutamate and the pathophysiology of hypoxic–ischemic brain damage , 1986, Annals of neurology.

[43]  R. Grunau,et al.  Extremely premature (⩽ 800 g) schoolchildren: multiple areas of hidden disability , 1997, Archives of disease in childhood. Fetal and neonatal edition.

[44]  H. C. Miller,et al.  Perinatal and environmental factors in late neurogenic sequelae. I. Infants having birth weights under 1,500 grams. , 1966, American journal of diseases of children.

[45]  J. Volpe,et al.  Episodes of apnea and bradycardia in the preterm newborn: impact on cerebral circulation. , 1985, Pediatrics.

[46]  M. Shimada,et al.  Development of the Sleep and Wakefulness Rhythm in Preterm Infants Discharged from a Neonatal Care Unit , 1993, Pediatric Research.

[47]  R. Guillet,et al.  Bilirubin and Serial Auditory Brainstem Responses in Premature Infants , 2001, Pediatrics.

[48]  Maya Frankfurt,et al.  Prevention of stress-induced morphological and cognitive consequences , 1997, European Neuropsychopharmacology.

[49]  G L Shaw,et al.  Enhanced learning of proportional math through music training and spatial-temporal training. , 1999, Neurological research.

[50]  M. Mitchell,et al.  Thyroid function in very low birth weight infants , 1997, Clinical endocrinology.

[51]  S. Rosenbaum,et al.  The Sedative and Analgesic Sparing Effect of Music , 1999 .

[52]  S. P. Porterfield,et al.  The role of thyroid hormones in prenatal and neonatal neurological development--current perspectives. , 1993, Endocrine reviews.

[53]  T. Cole,et al.  Breast milk and subsequent intelligence quotient in children born preterm , 1992, The Lancet.

[54]  A. Ohlsson,et al.  Systematic review and meta-analysis of early postnatal dexamethasone for prevention of chronic lung disease , 1998, Archives of disease in childhood. Fetal and neonatal edition.

[55]  F. Duffy,et al.  Individualized developmental care for the very low-birth-weight preterm infant. Medical and neurofunctional effects. , 1994, JAMA.

[56]  B. Lester,et al.  Biology versus environment in the extremely low-birth weight infant. , 2000, Clinics in perinatology.

[57]  F. Rauscher,et al.  Improved maze learning through early music exposure in rats. , 1998, Neurological research.

[58]  V. Ramaekers,et al.  Cerebral hyperperfusion following episodes of bradycardia in the preterm infant. , 1993, Early human development.

[59]  M. Meaney,et al.  The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. , 1985, Brain research.

[60]  J. R. Hughes,et al.  The “Mozart Effect” on Epileptiform Activity , 1998, Clinical EEG.

[61]  G. M. D. Escobar The Hypothyroxinemia of Prematurity , 1998 .

[62]  R. Lickliter Premature visual experience facilitates visual responsiveness in bobwhite quail neonates , 1990 .

[63]  J. Altman,et al.  Autoradiographic Examination of the Effects of Enriched Environment on the Rate of Glial Multiplication in the Adult Rat Brain , 1964, Nature.

[64]  A. Robertson,et al.  Sound Transmission Into Incubators in the Neonatal Intensive Care Unit , 1999, Journal of Perinatology.

[65]  C. Hudson,et al.  Evidence for transient perinatal glutamatergic innervation of globus pallidus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  S. Rivkees Developing circadian rhythmicity. Basic and clinical aspects. , 1997, Pediatric clinics of North America.

[67]  F. Gage,et al.  More hippocampal neurons in adult mice living in an enriched environment , 1997, Nature.

[68]  R. Lickliter The Role of Sensory Stimulation in Perinatal Development: Insights from Comparative Research for Care of the High‐Risk Infant , 2000, Journal of developmental and behavioral pediatrics : JDBP.

[69]  R. Brand,et al.  Hyperbilirubinemia in preterm infants and neurodevelopmental outcome at 2 years of age: results of a national collaborative survey. , 1989, Pediatrics.

[70]  I. McMillen,et al.  Development of Circadian Sleep-Wake Rhythms in Preterm and Full-Term Infants , 1991, Pediatric Research.

[71]  S. Garside,et al.  Dopamine–glutamate interactions in the striatum: behaviourally relevant modification of excitotoxicity by dopamine receptor-mediated mechanisms , 1996, Neuroscience.

[72]  A. Fanaroff,et al.  Perinatal Correlates of Cerebral Palsy and Other Neurologic Impairment Among Very Low Birth Weight Children , 1998, Pediatrics.

[73]  P. Rakić,et al.  The genesis of efferent connections from the visual cortex of the fetal rhesus monkey , 1981, The Journal of comparative neurology.

[74]  J. Preisser,et al.  Trends in Mortality and Cerebral Palsy in a Geographically Based Cohort of Very Low Birth Weight Neonates Born Between 1982 to 1994 , 1998, Pediatrics.

[75]  M C McCormick,et al.  The behavioral and emotional well-being of school-age children with different birth weights. , 1996, Pediatrics.

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

[77]  S. C. Butler,et al.  Maternal depressive symptoms affect infant cognitive development in Barbados. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[78]  D. J. Goldstein,et al.  Serum bilirubin levels, intracranial hemorrhage, and the risk of developmental problems in very low birth weight neonates. , 1992, Pediatrics.

[79]  L. Siegel,et al.  Reproductive, perinatal, and environmental factors as predictors of the cognitive and language development of preterm and full-term infants. , 1982, Child development.

[80]  H. Lou,et al.  Etiology and pathogenesis of Attention‐deficit Hyperactivity Disorder (ADHD): significance of prematurity and perinatal hypoxic‐haemodynamic encephalopathy , 1996, Acta paediatrica.

[81]  K. Sano,et al.  Effects of dexamethasone on the expression of myelin basic protein, proteolipid protein, and glial fibrillary acidic protein genes in developing rat brain. , 1991, Brain research. Developmental brain research.

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

[83]  S. Greenspan,et al.  Intelligence quotient scores of 4-year-old children: social-environmental risk factors. , 1987, Pediatrics.

[84]  W. Cashore The neurotoxicity of bilirubin. , 1990, Clinics in perinatology.

[85]  S. Reppert,et al.  The suprachiasmatic nuclei of the fetal rat: characterization of a functional circadian clock using 14C-labeled deoxyglucose , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  J. Pinto-Martin,et al.  The relation of transient hypothyroxinemia in preterm infants to neurologic development at two years of age. , 1996, The New England journal of medicine.

[87]  J. Volpe,et al.  Movement disorder of premature infants with severe bronchopulmonary dysplasia: a new syndrome. , 1989, Pediatrics.

[88]  F. Dekker,et al.  Neonatal Thyroxine Supplementation in Very Preterm Children: Developmental Outcome Evaluated at Early School Age , 2001, Pediatrics.

[89]  A. Jobe Glucocorticoids in perinatal medicine: misguided rockets? , 2000, The Journal of pediatrics.

[90]  F. Fonnum,et al.  Bilirubin Inhibits Transport of Neurotransmitters in Synaptic Vesicles , 1998, Pediatric Research.

[91]  J. A. Churchill,et al.  Learning Impairment in Rats Administered a Lipid Free Diet during Pregnancy , 1966, Psychological reports.

[92]  P Szatmari,et al.  Cognitive abilities and school performance of extremely low birth weight children and matched term control children at age 8 years: a regional study. , 1991, The Journal of pediatrics.

[93]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged glucocorticoid exposure in primates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  A. Whitelaw,et al.  Antenatal steroids and the developing brain , 2000, Archives of disease in childhood. Fetal and neonatal edition.

[95]  Mark A. Smith Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors , 1996, Behavioural Brain Research.

[96]  M. Gunning,et al.  Repeated Episodes of Umbilical Cord Occlusion in Fetal Sheep Lead to Preferential Damage to the Striatum and Sensitize the Heart to Further Insults , 1995, Pediatric Research.

[97]  H. Uno,et al.  Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. , 1990, Brain research. Developmental brain research.

[98]  J. M. White,et al.  Effects of relaxing music on cardiac autonomic balance and anxiety after acute myocardial infarction. , 1999, American journal of critical care : an official publication, American Association of Critical-Care Nurses.

[99]  T. Achenbach,et al.  Nine-year outcome of the Vermont intervention program for low birth weight infants. , 1993, Pediatrics.

[100]  J. Bernal Thyroid hormones and brain development. , 1995, Vitamins and hormones.

[101]  Moore Ry Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. , 1983 .

[102]  J. Scanlon,et al.  Results of controlled double-blind study of thyroid replacement in very low-birth-weight premature infants with hypothyroxinemia. , 1984, Pediatrics.

[103]  P. Mullaney,et al.  Outcomes of extremely premature infants related to their peak serum bilirubin concentrations and exposure to phototherapy. , 1998, Pediatrics.

[104]  N. Menon,et al.  Essential fatty acid deficiency and brain development. , 1982, Progress in lipid research.

[105]  N Paneth,et al.  Psychiatric outcomes in low-birth-weight children at age 6 years: relation to neonatal cranial ultrasound abnormalities. , 1997, Archives of general psychiatry.

[106]  N. Sloan,et al.  Kangaroo mother method: randomised controlled trial of an alternative method of care for stabilised low-birthweight infants , 1994, The Lancet.

[107]  F. Dekker,et al.  Thyroid Function in Very Preterm Infants: Influences of Gestational Age and Disease , 1997, Pediatric Research.

[108]  V. Mcloyd,et al.  Socioeconomic disadvantage and child development. , 1998, The American psychologist.

[109]  S. Reppert Maternal Entrainment of the Developing Orcadian System a , 1985, Annals of the New York Academy of Sciences.

[110]  J. Lucey,et al.  Noise and hypoxemia in the intensive care nursery. , 1980, Pediatrics.

[111]  M. Allen,et al.  The Limit of Viability -- Neonatal Outcome of Infants Born at 22 to 25 Weeks' Gestation , 1993 .

[112]  P. Rakić,et al.  Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain , 1990, The Journal of comparative neurology.

[113]  P. Messmer,et al.  Effect of kangaroo care on sleep time for neonates. , 1997, Pediatric nursing.

[114]  W. Greenough,et al.  Experiential modification of the developing brain. , 1975, American scientist.

[115]  L. P. Morin The circadian visual system , 1994, Brain Research Reviews.

[116]  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.

[117]  F. Pidcock,et al.  Neurodevelopment of preterm infants: neonatal neurosonographic and serum bilirubin studies. , 1992, Pediatrics.

[118]  R. Lickliter,et al.  Intersensory experience and early perceptual development: postnatal experience with multimodal maternal cues affects intersensory responsiveness in bobwhite quail chicks. , 1998, Developmental psychology.

[119]  G. Pascal,et al.  Brain cell and tissue recovery in rats made deficient in n-3 fatty acids by alteration of dietary fat. , 1989, The Journal of nutrition.

[120]  Ming Xu,et al.  Dopamine D1 receptor mutant mice are deficient in striatal expression of dynorphin and in dopamine-mediated behavioral responses , 1994, Cell.

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

[122]  P. Rakić Prenatal development of the visual system in rhesus monkey. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[123]  Shakti Sharma,et al.  Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. , 1996, Developmental neuroscience.

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

[125]  H. Tamai,et al.  Vigintiphobia, unbound bilirubin, and auditory brainstem responses. , 1994, Pediatrics.

[126]  J. Birnholz,et al.  The development of human fetal hearing. , 1983, Science.

[127]  P. Greengard,et al.  Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices , 1990, Nature.

[128]  S. Detera-Wadleigh,et al.  Characterization of the human glucocorticoid receptor promoter. , 1995, Biochemistry.

[129]  D. J. Goldstein,et al.  Randomized Placebo-controlled Trial of a 42-Day Tapering Course of Dexamethasone to Reduce the Duration of Ventilator Dependency in Very Low Birth Weight Infants: Outcome of Study Participants at 1-Year Adjusted Age , 1999, Pediatrics.

[130]  Neil Marlow,et al.  Neurologic and developmental disability after extremely preterm birth , 2000 .

[131]  J. M. Park,et al.  Family factors and social support in the developmental outcomes of very low-birth weight children. , 2000, Clinics in perinatology.

[132]  T. Slotkin,et al.  Glucocorticoid administration alters nuclear transcription factors in fetal rat brain: implications for the use of antenatal steroids. , 1998, Brain research. Developmental brain research.

[133]  B. McEwen Stress and hippocampal plasticity. , 1999, Annual review of neuroscience.

[134]  M. Johnston,et al.  Role of Glutamate Receptor-Mediated Excitotoxicity in Bilirubin-Induced Brain Injury in the Gunn Rat Model , 1998, Experimental Neurology.

[135]  S. Rivkees,et al.  The biological clock of very premature primate infants is responsive to light. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[136]  S. Pfeiffer,et al.  Outcome for Preschoolers of Very Low Birthweight: Sociocultural and Environmental Influences , 1990, Perceptual and motor skills.

[137]  M. Hiatt,et al.  Neurodevelopmental Outcome of Infants with Apnea of Infancy , 1993, American journal of perinatology.

[138]  Y. Endo,et al.  Long-term glucocorticoid treatments decrease local cerebral blood flow in the rat hippocampus, in association with histological damage , 1997, Neuroscience.

[139]  R. Ariagno,et al.  Biological rhythmicity in preterm infants prior to discharge from neonatal intensive care. , 1995, Pediatrics.

[140]  G. Koren,et al.  Pregnancy outcome and neurodevelopment of children exposed in utero to psychoactive drugs: the Motherisk experience. , 1997, Journal of psychiatry & neuroscience : JPN.

[141]  M. Meaney,et al.  Postnatal Handling Increases the Expression of cAMP-Inducible Transcription Factors in the Rat Hippocampus: The Effects of Thyroid Hormones and Serotonin , 2000, The Journal of Neuroscience.

[142]  N Marlow,et al.  Attention deficit hyperactivity disorders and other psychiatric outcomes in very low birthweight children at 12 years. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[143]  H. Halliday,et al.  Behavioural adjustment in school of very low birthweight children. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[144]  K. Fuxe,et al.  DEMONSTRATION AND MAPPING OUT OF NIGRO-NEOSTRIATAL DOPAMINE NEURONS. , 1964, Life sciences.

[145]  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.

[146]  R. Sapolsky,et al.  Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. , 1990, Neuroendocrinology.

[147]  M. Johnston,et al.  Glutamate recognition sites in human fetal brain , 1988, Neuroscience Letters.

[148]  M. Johnston,et al.  Perinatal Hypoxia‐Ischemia Disrupts Striatal High‐Affinity [3H]Glutamate Uptake into Synaptosomes , 1986, Journal of neurochemistry.

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