The genesis of cognitive and behavioral deficits in premature graduates of intensive care

Minerva Pediatrica

Volumn 55, Issue 2, 2003, Pages 89-101

  Perlman, J M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Child behavior disorders; Cognitive disorders; Infant, premature

Indexed keywords

GLUCOCORTICOID; THEOPHYLLINE DERIVATIVE;

APNEA; BEHAVIOR DISORDER; BRADYCARDIA; CHRONIC LUNG DISEASE; COGNITIVE DEFECT; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; HIPPOCAMPUS; HUMAN; HYPERBILIRUBINEMIA; INTENSIVE CARE; LOW BIRTH WEIGHT; NEWBORN; NOISE; NUTRITIONAL DEFICIENCY; PATHOGENESIS; PREMATURITY; REVIEW; SOCIAL SUPPORT; STRESS; SURVIVAL RATE;

BASAL GANGLIA; BRAIN DAMAGE, CHRONIC; CHILD BEHAVIOR DISORDERS; COGNITION DISORDERS; FOLLOW-UP STUDIES; HIPPOCAMPUS; HUMANS; INFANT CARE; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; INFANT, PREMATURE; INFANT, VERY LOW BIRTH WEIGHT; INTENSIVE CARE UNITS, NEONATAL; LIGHTING; NOISE; STRESS; SURVIVORS;

EID: 0038388284     PISSN: 00264946     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (175)

1. Allen MC, Donohue PK, Dusman AE. The limits of viability - neonatal outcomes of infants born at 22 to 25 weeks' gestation. N Engl J Med 1993;329:1597-601.
2. El-Metwally D, Vohr B, Tucker R. Survival and neonatal morbidity at the limits of viability in the mid 1990's: 22-25 weeks. J Pediatr 2000;137:616-22.
3. Lorenz JM. Survival of the extremely preterm infant in North America in the 1990's. Clin Perinatol 2000;27: 255-62.
4. Perlman JM. Neurobehavioral deficits in premature graduates of intensive care. Potential medical and environmental risk factors. Pediatrics 2001;108:1339-48.
5. Hack M, Fanaroff AA. Outcomes of children of extremely low birth weight and gestational age in the 1990's. Early Hum Dev 1999;53:193-218.
6. Chapieski ML, Evankovitch KD. Behavioral effects of prematurity. Semin Perinatol 1997;21:221-39.
7. Saigal S, Szatmari P, Rosenbaum P, Campbell D, King S. Cognitive ability and school performance of extremely low birth weight children and matched term children at age 8 years. A regional study. J Pediatr 1991;118:751-60.
8. Hack M, Taylor HG, Klein N, Eiben R, Schatschneider C, Mercuri-Minich N. School-age outcomes in children with birth weights under 750 g. N Engl J Med 1994;331: 753-9.
9. Whitfield MF, Eckstein RV, Holsti L. Extremely premature (≤800 g) school children: multiple areas of hidden disability. Arch Dis Child 1997;77:F85-90.
10. Sykes DH, Hoy EA, Bill JM, McClure BG, Halliday HL, Reid MM. Behavioral adjustment in school of very low birthweight children. J Child Psychol Psychiatry 1997;38: 315-25.
11. Whitaker AH, Van Rossem R, Feldman JF, Schonfeld IS, Pinto-Martin JA, Tore C et al. Psychiatric outcomes in low-birth-weight children at age 6 years: relation to neonatal cranial ultrasound abnormalities. Arch Gen Psychiatry 1997;54:847-56.
12. Bothing N, Powls, A, Cooke RW, Marlow N. Attention deficit hyperactivity disorders and other psychiatric outcomes in very low birthweight children at 12 years. J Child Psychol Psychiatry 1997;38:931-41.
13. Stjernqvist K, Svenningsen NW. Ten year follow-up of children born before 29 gestational weeks: health, cognitive development, behavior and school achievement. Acta Pediatr 1999;88:557-62.
14. Hack M, Flannery DJ, Schluchter M, Cartar L, Borawski E, Klein N. Outcomes in young adulthood for verylow-birth-weight infants. N Engl J Med 2002;346:149-57.
15. Doyle LW, Casalaz D. Outcome at 14 years of extremely low birthweight infants: a regional study. Arch Dis Child Fetal Neonatal Ed 2001;85:F159-64.
16. Cooke RWI, Abernethy LJ. Cranial magnetic imaging and school performance in very low birthweight infants in adolescence. Arch Dis Child Fetal Neonatal Ed 1999;81:F116-21.
17. Stewart AL, Rifkin L, Amess PN, Kirkbride V, Townsend JP, Miller DH et al. Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm. Lancet 1999;353:1653-7.
18. th ed. Philadelphia: WB Saunders; 2000.
19. Rakic P. Prenatal development of the visual system in the rhesus monkey. Philos Trans R Soc Lond 1977;B278:245-60.
20. Kostovic I, Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the Macaque monkey and human brain. J Comp Neurol 1990;297:441-70.
21. Ghosh A, Shatz CJ. A role for subplate neurons in the patterning of connections from thalamus to neocortex. Development 1993;117:1031-47.
22. Shatz CJ, Rakic P. The genesis of efferent connections from the visual cortex of the fetal monkey. J Comp Neurol 1981;196:287-97.
23. Lou HC. Etiology and pathogenesis of attention deficit hyperactivity disorder: significance of prematurity and perinatal hypoxic-hemodynamic encephalopathy. Acta Paediatr 1996;85:1266-71.
24. Kemp JM, Powell TPS. The connections of the striatum and globus pallidus: synthesis and speculation. Phil Trans R Soc Lond Sci 1971;262:441-57.
25. Barks JD, Silverstein FS, Sims K, Greenamyre JT, Johnston MV. Glutamate recognition sites in human fetal brain. Neurosci Lett 1988;84:131-6.
26. Greenamyre T, Penney JB, Young AB, Hudson C, Silverstein FS, Johnston MV. Evidence for transient perinatal glutamatergic innervation of globus pallidus. J Neurosci 1987;7:1022-30.
27. Rothman SM, Olney JW. Glutamate and the pathophysiology of hypoxic ischemic brain damage. Ann Neurol 1986;19:105-10.
28. Silverstein FS, Buchanan K, Johnson MV. Perinatal hypoxia-ischemia disrupts striatal high affinity (3H) glutamate uptake into synaptosomes. J Neurochem 1986;47:1614-8.
29. Mallard EC, Williams CE, Johnson M. Repeated episodes of umbilical cord occlusion in fetal sheep lead to preferential damage to striatum and sensitize the heart to further insults. Pediatr Res 1995;37:707-13.
30. Linde T, Kalimo H, Wieloch T. Protective effect of lesion to the glutamatergic cortico-striatal projection on the hypoglycemic nerve cell injury in rat striatum. Acta Neuropathol 1987;74:334-44.
31. Anden NE, Carlsson A, Dahlstrom A et al. Demonstration and mapping out of nigro-neostriatal dopamine neurons. Life Sci 1964;3:523-30.
32. Garside S, Furtado JCS, Mazurek MF. Dopamine-glutamate interactions in the striatum: behaviorally relevant modification of excitotoxicity by dopamine receptor-mediated mechanisms. Neuroscience 1996;75:1065-74.
33. Calabresi P, Mercuri N, Stanzione P, Stefani A, Bernardi G. Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: evidence for D1 receptor involvement. Neuroscience 1987;20:757-71.
34. Maura G, Giardi A, Raiteri M. Release-regulating D-2 dopamine receptors are located on striatal glutamatergic nerve terminals. J Pharmacol Exp Ther 1988;247: 684-90.
35. Halpain S, Girault J, Greengard P. Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat sliatal slices. Nature 1990;343:369-72.
36. Xu M, Moratalla R, Gold LH, Hiroi N, Koob GF, Graybiel AM et al. Dopamine D1 receptor mutant mice are deficient in striatal expression of dynorphin and in dopamine-mediated behavioral responses. Cell 1994;79: 729-42.
37. Perlman JM, Volpe JJ. Movement disorder of premature infants with severe bronchopulmonary dysplasia. Pediatrics 1989;84:215-8.
38. Chamnanvanakij S, Rogers CG, Luppino C, Broyles SR, Hickman J, Perlman JM. Linear hyperechogenicity within the basal ganglia and thalamus of preterm infants. Pediatr Neurol 2000;23:129-33,
39. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999;22:105-22.
40. Porterfield SP, Hendrick CH. The role of thyroid hormones in prenatal and neonatal neurological development. Current perspectives. Endocr Rev 1993;14: 94-106.
41. Bernal J, Nunez J. Thyroid hormones and brain development. Eur J Endocrinol 1995;133:390-8.
42. Bradley D, Young W, Weinberger C. Differential expression of and thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci 1989;86:7250-4.
43. Jobe AH. Glucocorticoids in perinatal medicine: misguided rockets? J Pediatr 2000;137:1-3.
44. Whitelaw A, Thoresen M. Antenatal steroids and the developing brain. Arch Dis Child Fetal Neonatal Ed 2000; 83:F154-7.
45. Sapolsky RM, Uno H, Robert CS, Finch CC. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J Neurosci 1990;531:225-31.
46. Isaacs EB, Lucas A, Chong WK, Wood SJ, Johnson CL, Marshall C et al. Hippocampal volume and everyday memory in children of very low birth weight. Pediatr Res 2000;47:713-20.
47. Stevenson DK, Wright LL, Lemons JA, Oh W, Korones SB, Papile LA 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. Am J Obstet Gynecol 1998;179:1632-9.
48. Vohr BR, Wright LL, Dusick AM, Mele L, Verter J, Steichen JJ 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. Pediatrics 2000;105:1216-26.
49. Murphy BP, Inder TE, Huppi PS, Warfield S, Zientara GP, Kikinis R et al. Impaired cerebral cortical gray matter growth after treatment with dexamethasone for neonatal chronic lung disease. Pediatrics 2001;107: 217-21.
50. Campbell LR, McAlister W, Volpe JJ. Neurologic aspects of bronchopulmonary dysplasia. Clin Pediatr 1998;27:7-13.
51. Smith JF, Reynolds EOR, Taghizadeh A. Brain maturation and damage in infants dying from chronic pulmonary insufficiency in the postneonatal period. Arch Dis Childh 1974;49:359-65.
52. Henderson-Smart DJ. The effect of gestational age on the incidence and duration of recurrent apnea in newborn babies. Aust Paediatr J 1981;17:273-6.
53. Perlman JM, Volpe JJ. Episodes of apnea and bradycardia in the preterm newborn. Impact on the cerebral circulation. Pediatrics 1987;76:333-8.
54. Ramackers VT, Casaer P, Daniels H. Cerebral hyperperfusion following episodes of bradycardia in the preterm infant. Early Hum Dev 1993;34:199-208.
55. Bacola E, Behrle FC, De Schweinitz L, Miller HC, Mira M. Perinatal and environmental factors in late neurogenic sequelae. I. Infants having birth weights under 1,500 grams. Am J Dis Child 1966;112:359-68.
56. Koons AH, Mojica N, Jadeja N, Ostfeld B, Hiatt M, Hegyi T. Neurodevelopmental outcome of infants with apnea of infancy. Am J Perinatol 1993;10:208-11.
57. Taylor HG, Klein N, Schatschneider C. Predictors of early school age outcomes in very low birth weight children. J Dev Behav Pediatr 1998;19:235-43.
58. Thurston JH, Hauhard RE, Dirgo JA. Aminophylline increases cerebral metabolic rate and decreases anoxic survival in young mice. Science 1978;201:649-51.
59. Rudolphi KA, Keil M, Hinze HJ. Effect of theophylline on ischemically induced hippocampal damage in Mongolian gerbils: a behavioral and histopathological study. J Cereb Blood Flow Metab 1987;7:74-81.
60. Turski WA, Cavalheiro EA, Ikonomidou C. Effects of aminophylline and 2-chloroadenosine on seizures produced by pilocarpine in rats: morphological and electroencephalographic correlates. Brain Res 1985;361: 309-23.
61. Sreenan C, Etches PC, Demianczuk N. Isolated mental developmental delay in very low birthweight infants: association with prolonged doxapram therapy for apnea. J Pediatr 2001;139:832-7.
62. Van Wassenaer AG, Kok JH, Dekker FW, De Nijlder JJM. Thyroid function in very premature infants: influences of gestational age and disease. Pediatr Res 1997;42:604-9.
63. Klein RZ, Carlton EL, Faix JD, Frank JE, Hermos RJ, Mullaney D et al. Thyroid function in very low birth weight infants. Clin Endocrinol (Oxf) 1997;47:411-7.
64. Fisher DA. The hypothyroxinemia of prematurity. J Clin Endocrinal Metab 1997;82:1701-3.
65. Den Ouden AL, Kok JH, Verkerk PH, Brand R, Verloove-Vanhorick SP. 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 birthweight infants. Pediatr Res 1996;39:142-5.
66. Reuss ML, Paneth N, Pinto Martin JA, Lorenz JM, Susser M. The relation of transient hypothryoxinemia in preterm infants to neurologic development at 2 years of age. N Engl J Med 1996:334:821-7.
67. Lucas A, Morley R, Fentrell MS. Low triiodothyronine concentrations in preterm infants and subsequent intelligent quotient (IQ) at 8 year follow-up. BMJ 1996;312:1132-3.
68. Wilson-Costello D, Borawski E, Friedman H, Redline R, Fanaroff AA, Hack M. Perinatal correlates of cerebral palsy and other neurologic impairment among very low birth weight children. Pediatrics 1998;102:315-22.
69. Paneth N. Does transient hypothyroxinemia cause abnormal neurodevelopment in premature infants? Clin Perinatol 1998;25:627-43.
70. Chowdhry P, Scanlon JW, Auerbach R, Abbassi V. Results of controlled double-blind study of thyroid replacement in very low-birth-weight premature infants with hypothyroxinemia. Pediatrics 1984;73:301-5.
71. Vanhole C, Aerssens P, Naulaers G, Casneuf A, Devlieger H, Van den Berghe G et al. L-thyroxine treatment of preterm newborns: clinical and endocrine effects. Pediatr Res 1997;42:87-92.
72. van Wassenaer AG, Kok JH, de Vijlder JJ, Briet JM, Smit BJ, Tamminga P et al. Effects of thyroxine supplementation on neurologic development in infants born at less than 30 weeks' gestation. N Engl J Med 1997;336: 21-6.
73. Briet JM, van Wassenaer AG, Dekker FW, de Vijlder JJ, van Baar A, Kok JH. Neonatal thyroxine supplementation in very preterm children: developmental outcome evaluated at early school age. Pediatrics 2001;107:712-8.
74. Cashore WJ. The neurotoxicity of bilirubin. Clin Perinatol 1990;17:437-47.
75. Wennberg RP, Johansson BB, Folbergrova J, Siesjo BK. Bilirubin-induced changes in brain energy metabolism after osmotic opening of the blood-brain barrier. Pediatr Res 1991;30:473-8.
76. Amato MM, Kilguss NV, Gelardi NL, Cashore WJ. Dose-effect relationship of bilirubin on striatal synaptosomes in rats. Biol Neonate 1994;66:288-93.
77. Hansen TWR, Mathiesen SBW, Walaas SI. Bilirubin has widespread inhibition effects on protein phosphorylation. Pediatric Res 1996;39:1072-7.
78. McDonald JW, Shapriro SM, Silverstein FS, Johnson MV. Role of glutamate receptor-mediated excitotoxicity in bilirubin-induced brain injury in the Gunn rat model Exp Neurol 1998;150:21-9.
79. Roseth S, Hansen TW, Fonnum F, Walaas SI. Bilirubin inhibits transport of neurotransmitters in synaptic vesicles. Pediatr Res 1998;44:312-6.
80. Rhine WD, Schmitter SP, Yu AC, Eng LF, Stevenson DK. Bilirubin toxicity and differentiation of cultured astrocytes. J Perinatol 1999;19:206-11.
81. Bergman I, Hirsch RP, Fria TJ, Shapiro SM, Holzman I, Painter MJ. Causes of hearing loss in the high risk premature infant. J Pediatr 1985;106:95-101.
82. Van de Bor M, van Zeben-van der Aa TM, Verloove-Vanhorick SP, Brand R, Ruys JH. Hyperbilirubinuria in preterm infants and neurodevelopmental outcome at 2 years of age: results of a national collaborative study. Pediatrics 1989;83:915-20.
83. O'Shea TM, Dillard RG, Klinepeter KL, Goldstein DJ. Serum bilirubin levels, intracranial hemorrhage and the risk of developmental problems in very low birth weight neonates. Pediatrics 1992;90:888-92.
84. Graziani LJ, Mitchell DG, Kornhauser M, Pidcock FS, Merton DA, Stanley C et al. Neonatal neurosographic and serum bilirubin studies. Pediatrics 1992;89: 229-34.
85. Yeo KL, Perlman M, Hao Y, Mullaney P. Outcomes of extremely premature infants related to their peak serum bilirubin concentrations and exposure to phototherapy. Pediatrics 1998;102:1426-31.
86. Menon NK, Dhopeshwaker GA. Essential fatty acid deficiency and brain development. Prog Lipid Res 1982; 221:309-26.
87. Uauy R, Mena P, Rojas C. Essential fatty acid metabolism in the micropremie. Clin Perinatol 2000;27:81-93.
88. Berkow SE, Campagnoni AT. Essential fatty acid deficiency: effect of cross fostering mice at birth on myelin levels and composition. J Nutr 1983;113:582-91.
89. Caldwell DF, Churchill JH. Learning impairment in rats administered a lipid free diet during pregnancy. Psychol Rep 1996;19:99-102.
90. Wauben IP, Xing HC, Wainwright PE. Neonatal dietary Zn deficiency in artificially reared rat pup retards behavioral development and interacts with essential fatty acid deficiency to alter liver and brain fatty acid composition. J Nutr 1999;129:1773-81.
91. Lucus A, Morley R, Cole TJ, Lister G, Leeson-Payne C. Breast milk and subsequent intelligence quotient in children born preterm. Lancet 1992;339:261-4.
92. Bhuta T, Ohlsson A. Systematic review and meta-analysis of early postnatal dexamethasone for prevention of chronic lung disease. Arch Dis Childh Fetal Neonatal Ed 1998;79:F26-33.
93. Halliday HL. Clinical trials of postnatal corticosteroids: inhaled and systemic. Biol Neonate 1999;76 Suppl 1:29-40.
94. Yeh TF, Lin YJ, Huang CC, Chen YJ, Lin CH, Lin HC et al. Early dexamethasone therapy in preterm infants: a follow-up study. Pediatrics 1998;101:E7.
95. O'Shea TM, Kothadia JM, Klinepeter KL, Goldstein DJ, Jackson BG, Weaver RG 3rd 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. Pediatrics 1999;104:15-21.
96. Gould E. The effects of adrenal steroids and excitatory impact on neuronal birth and survival. Ann N Y Acad Sci 1994;743:73-94.
97. Mathews SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res 2000;47: 291-300.
98. Endo Y, Nishimura JI, Kobayashi S, Kimura F. Longterm glucocorticoid treatments decrease local cerebral blood flow in the rat hippocampus, in association with histological damage. Neuroscience 1997;79: 745-52.
99. Tsuneishi S, Takada S, Motoike T, Ohashi T, Sano K, Nakamura H. Effects of dexamethasone on the expression of myelin basic protein, proteolipid protein, and glial fibrillary acidic protein genes in developing rat brain. Brain Res Dev Brain Res 1991;61:117-23.
100. Dunlop SA, Archer MA, Quinlivan JA, Beazley LD, Newnham JP. Repeated prenatal cortiosteroids delay myelination in the ovine central nervous system. J Matern Fetal Med 1997;6:309-13.
101. Diaz R, Fuxe K, Ogren SO. Prenatal corticosterone treatment induces long-term changes in spontaneous and apomorphine mediated motor activity in male and female rats. Neuroscience 1997;81:129-40.
102. Chen J, Adachi N, Tsubota S, Nagoro T, Arai T. Dexamethasone augments ischemia-induced extra cellular accumulation of glutamate in gerbils. Eur J Pharmacol 1998;347:67-70.
103. Homer HC, Packan DR, Sapolsky RM. Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glial. Neuroendocrinology 1990;52:57-64.
104. Behl C, Lezoualc'h F, Trapp T, Widmann M, Skutella T, Holsboer F. Glucocorticoids enhance oxidative stress-induced cell death in hippocampal neurons in vitro. Endocrinology 1997;138:101-6.
105. McIntosh LJ, Sapolsky RM. Glucocorticoids increase the accumulation of reactive oxygen species and enhance Adriamycin-induced toxicity in neuronal culture. Exp Neurol 1996;141:201-6.
106. Smith MA. Hippocampal vulnerability to stress and aging: possible role of neurotrophic factors. Behav Brain Res 1996;78:25-6.
107. Slotkin TA, Zang J, McCook EC, Seidler FJ. Glucorticoid administration alters nuclear transcription factors in fetal rat brain: implications for use of antenatal steroids. Dev Brain Res 1998;111:11-24.
108. Sapolsky RM. Why stress is bad for your brain. Science 1996;273:749-50.
109. Meaney MJ, Aitken DH. The effects of early postnatal handling on the development of hippocampal glucocorticoid receptors: temporal parameters. Dev Brain Res 1985;22:301-4.
110. Meany MJ, Dioro J, Francis D, Weaver S, Yaw J, Chapman K et al. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin. Neuroscience 2000;20:3926-35.
111. Meaney MJ, Aitken DH, Bhatnagar S, Berkel CV, Sapolsky RM. Postnatal handling attenuates neuroendocrine, anatomical and cognitive impairments related to the aged hippocampus. Science 1988;238:766-8.
112. Meany M, Diario J, Widdowson J, LaPlante P, Caldji C, Seckl JR et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 1996;18:49-52.
113. Mitchell JB, Iny LJ, Meany MJ. The role of serotonin in the development and environmental regulation of hippocampal type II corticosteroid receptors. Dev Brain Res 1990;55:231-5.
114. Nobukuni Y, Smith C, Hager GL, Detera-Wadleigh SD. Characterization of the human glucocorticoid receptor promotor. Biochemistry 1995;34:8207-14.
115. O'Donnell D, Larocque S, Seck L, Meany MJ. Postnatal handling alters glucocorticoid but not mineralocorticoid mRNA expression in adult rats. Mol Brain Res 1994;26:242-8.
116. Altman J, Das GD. Autoradiographic examination of the effects of enriched environment on the rat of glial multiplication in the adult rat brain. Nature 1964;204: 1161-3.
117. Greenough WT. Experimental modification of the developing brain. Am Sci 1975;63:37-46.
118. Kempermann G, Kuhn G, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997;386:493-5.
119. Wallace C, Withers G, Weiler I, George J, Clayton D, Greenough W. Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. Mol Brain Res 1996;32:211-20.
120. Lickliter R. The role of sensory stimulation in perinatal development: insights from comparative research for care of the high-risk infant. J Dev Behav Pediatr 2000;21:437-47.
121. Lickliter R. Premature visual experience facilitates visual responsiveness in bobwhite quail neonates. Infant Behav Dev 1990;13:487-96.
122. Sleigh MJ, Columbus RF, Lickliter R. Intersensory experience and early perceptual development: postnatal experience with multimodal maternal cues affects intersensory responsiveness in bobwhite quail chicks. Dev Psychol 1998;34:215-23.
123. Als H, Lawhon G, Duffy FH, McAnulty GB, Gibes-Grossman R, Blickman JG. Individualized developmental care for the very low-birth-weight preterm infant. Medical and neurofunctional effects. JAMA 1994; 272:853-8.
124. Fleisher BE, VandenBerg K, Constantinou J, Heller C, Benitz WE, Johnson A et al. Individualized developmental care for very-low-birth-weight premature infants. Clin Pediatr (Phila) 1995;34:523-9.
125. Field T. Massage therapy for infants and children. J Behav Dev Pediatr 1995;16:105-11.
126. Resnick MB, Eyler FD, Nelson RM, Eitzman DV, Bucciarelli RL. Developmental intervention for low birth weight infants: improved early development outcome. Pediatrics 1987;80:68-74.
127. Sloan NL, Camacho LW, Rojas EP, Stern C. Kangaroo mother method: randomised controlled trial of an alternative method of care for stabilised low-birthweight infants. Maternidad Isidro Ayora Study Team. Lancet 1994;344:782-5.
128. Messmer PR, Rodriguez S, Adams J, Wells-Gentry J, Washburn K, Zabaleta I et al. Effect of kangaroo care on sleep time for neonates. Pediatr Nurs 1997;23:8-14.
129. Buehler DM, Als H, Duffy FH, McAnulty GB, Liederman J. Effectiveness of individualized developmental care for low-risk preterm infants: behavioral and electrophysiologic evidence. Pediatrics 1995;96:923-32.
130. Feldman R, Eidelman AJ, Sirota L, Weller A. Comparison of skin to skin care (kangaroo) and traditional care: parenting outcomes and preterm infant development. Pediatrics 2002;110:16-6.
131. Birnholz JC, Benacerrah BR. The development of human fetal hearing. Science 1983;222:516-8.
132. American Academy of Pediatrics: Committee on Environmental Health. Noise: a hazard for the fetus and newborn. Pediatrics 1997;100:724-7.
133. Robertson A, Cooper-Peel C, Vos P. Sound transmission into incubators in the neonatal intensive care unit. J Perinatol 1999;19:494-7.
134. Philbin MK, Ballweg DD, Gray L. The effect of an intensive care unit sound environment on the development of habituation in healthy Avian neonates. Dev Psychobiol 1994;27:11-21.
135. Bess FH, Peek BF, Chapman JJ. Further observations on noise levels in infant incubators. Pediatrics 1979;63: 100-6.
136. Long JG, Lucey JF, Philip AG. Noise and hypoxemia in the intensive care nursery. Pediatrics 1980;65:143-5.
137. Zahr LR, Balian S. Responses of premature infants to routine nursing interventions and noise in the NICU. Nurs Res 1995;44:179-85.
138. Bayo MV, Garcia AM, Garcia A. Noise levels in an urban hospital and worker's subjective responses. Arch Environ Health 1995;50:247-51.
139. White JM. Effects of relaxing music on cardiac autonomic balance and anxiety after acute myocardial infarction. Am J Crit Care 1999;8:220-30.
140. Koch ME, Kain ZN, Ayoub C, Rosenbaum SH. The sedative and analgesic sparing effect of music. Anesthesiology 1998;89:300-6.
141. Hughes JR, Daaboul Y, Fino JJ, Shaw GL. The "Mozart Effect" on epileptiform activity. Clin Electroencephalogr 1998;29:109-19.
142. Rauscher FH, Shaw GL, Ky KN. Music and spatial task performance. Nature 1993;365:611.
143. Rauscher FH, Robinson D, Jens JJ. Improved maze learning through early music exposure in rats. Neurol Res 1998;20:427-32.
144. Graziano AB, Peterson M, Shaw GL. Enhanced learning of proportional math through music training and spatial-temporal training. Neurol Res 1999;21:139-52.
145. Shaw GL, Bodner M. Music enhances spatial-temporal reasoning: towards a neurophysiological basis using EEG. Clin Electroencephalogr 1999;30:151-5.
146. Mirmiran M, Ariagno RL. Influence of light in the NICU on the development of circadian rhythms in preterm infants. Semin Perinatol 2000;24:247-57.
147. Rivkees SA. Developing circadian rhythmicity. Basic and clinical aspects. Pediatr Clin North Am 1997;44: 467-87.
148. Moore RY. Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed Proc 1983;42:2783-9.
149. Morin LP. The circadian visual system. Brain Res Rev 1994;19:102-27.
150. Reppert SM. Maternal entrainment of the developing circadian system. Ann N Y Acad Sci U S A 1985;453:162-9.
151. Reppert SM, Schwartz WJ. The suprachiasmatic nuclei of the fetal rat: characterization of a functional biologic clock using 14C-labelled deoxyglucose. J Neurosci 1984;4:1677-82.
152. Shimada M, Segawa M, Higurashi M, Akamatsu H. Development of the sleep and wakefulness rhythm in preterm infants discharged from a neonatal care unit. Pediatr Res 1993;33:159-63.
153. Glotzbach SF, Edgar DM, Ariagno RL. Biologic rhythms in preterm infants prior to discharge from neonatal intensive care. Pediatrics 1995;95:231-7.
154. McMillen IC, Kok JS, Adamson TM, Deayton JM, Nowak R. Development of circadian sleep-wake rhythms in preterm and full-term infants. Pediatr Res 1991;29:381-4.
155. Mann NP, Haddow R, Stokes L, Goodley S, Rutter N. Effect of night and day on preterm infants in a newborn nursery: randomised trial. Br Med J (Clin Res Ed) 1986;293:1265-7.
156. Lester BM, Miller-Loncar CL. Biology versus environment in the extremely low-birth weight infant. Clin Perinatol 2000;27:461-81.
157. Weisglas-Kuperus N, Baerts W, Smrkovsky M, Sauer PJ. Effects of biologic and social factors on the cognitive development of very low birth weight children. Pediatrics 1993;92:658-65.
158. Hogan DP, Park JM. Family factors and social support in the developmental outcomes of the very lowbirth weight children. Clin Perinatol 2000;27:433-54.
159. McLoyd VC. Socioeconomic disadvantage and child development. Am Psychol 1998;53:185-204.
160. Miller JE. Developmental screening scores among preschool-aged children: the roles of poverty and child health. J Urban Health 1998;75:135-52.
161. Sameroff AJ, Seifer R, Barocas R, Zax M, Greenspan S. Intelligence quotient scores of 4-year-old children: social-environmental risk factors. Pediatrics 1987;79: 343-50.
162. Siegel LS. Reproductive, perinatal and environmental factors as pediatrics of the cognitive and language development of preterm and full-term infants. Child Dev 1982;53:963-73.
163. Pfeiffer SI, Aylward GP. Outcome for preschoolers of very low birth weight: socioeconomic and environmental influence. Percept Mot Skills 1990;70:1376-8.
164. McCormick MC, Workman-Daniels K, Brooks-Gunn J. The behavioral and emotional well-being of school-aged children with different birth weights. Pediatrics 1996;97:18-25.
165. Galler JR, Harrison RH. Maternal depressive symptoms affect infant cognitive development in Barbados. J Child Psychol Psychiatry 2000;41:747-57.
166. Resnick MB, Gueorguieva RV, Carter RL, Ariet M, Sun Y, Roth J et al. The impact of low birth weight, perinatal conditions, and sociodemographic factors on educational outcome in kindergarten. Pediatrics 1999;104:74.
167. Horwood LJ, Mogridge N, Darlow BA. Cognitive, educational, and behavioral outcomes at 7 to 8 years in a national very low birthweight cohort. Arch Dis Child Fetal Neonatal Ed 1998;79:F12-20.
168. Infants Health and Development Program. Enhancing the outcomes of low-birth weight: premature infants: a multisite, randomized trial. JAMA 1990;263:3035-42.
169. Achenbach TM, Howell CT, Aoki MF, Rauh VA. Nine year outcome of the Vermont intervention program for low birth weight infants. Pediatrics 1993;91:45-55.
170. Infants Health and Development Program. Results at age 8 years of early intervention for low-birth-weight premature infants. JAMA 1997;277:126-32.
171. Lipton JW, Ling Z, Vu TQ, Robie HC, Mangan KP, Weese-Mayer DE et al. Prenatal cocaine exposure reduces glial cell line-derived neurotrophic factor (GDNF) in the striatum and the carotid body of the rat: implications for DA neurodevelopment. Brain Res Dev Brain Res 1999;118:231-5.
172. Loebstein R, Koren G. Pregnancy outcome and neurodevelopment of children exposed in utero to psychoactive drugs: the Motherisk experience. J Psychiatry Neurosci 1997;22:192-6.
173. Edwards HE, Mcintyre Burnham W. The impact of corticosteroids on the developing animal. Pediatr Res 2001;50:433-40.
174. Hack M, Wilson-Costello D, Friedman H, Taylor GH, Schuster M. Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g. Arch Pediatr Adolesc Med 2000;154:725-31.
175. Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR. Neurologic and developmental disability after extremely preterm birth. EPICure Study Group. N Engl J Med 2000;343:378-84.