Recent advances in imaging preterm brain injury

Minerva Pediatrica

Volumn 59, Issue 4, 2007, Pages 349-368

  Boardman, J P ^a   Dyet, L E ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Brain injury; Infant, premature; Magnetic resonance imaging

Indexed keywords

STEROID;

BASAL GANGLION; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN VENTRICLE DILATATION; CEREBELLUM DISEASE; CHRONIC LUNG DISEASE; DIFFUSION TENSOR IMAGING; HUMAN; INTRAUTERINE GROWTH RETARDATION; LEUKOMALACIA; MORPHOMETRICS; NERVE CELL DIFFERENTIATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PERINATAL CARE; PREMATURE LABOR; REVIEW;

BRAIN DISEASES; BRAIN INJURIES; DEVELOPMENTAL DISABILITIES; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; NERVOUS SYSTEM;

EID: 35848953002     PISSN: 00264946     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (164)

1. Martin JA, Kochanek KD, Strobino DM, Guyer B, MacDorman MF. Annual summary of vital statistics 2003. Pediatrics 2005;115:619-34.
2. Tucker J, McGuire W. Epidemiology of preterm birth. BMJ 2004;329:675-8.
3. Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand KJ. Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA 2002;288:728-37.
4. Wilson-Costello D, Friedman H, Minich N, Siner B, Taylor G, Schluchter M et al. Improved neurodevelopmental outcomes for extremely low birth weight infants in 2000-2002. Pediatrics 2007;119:37-45.
5. Marlow N, Wolke D, Bracewell MA, Samara M; EPICure Study Group. Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 2005;352:9-19.
6. Seghier ML, Lazeyras F, Huppi PS. Functional MRI of the newborn. Semin Fetal Neonatal Med 2006;11:479-88.
7. Malamateniou C, Counsell SJ, Allsop JM, Fitzpatrick JA, Srinivasan L, Cowan FM et al. The effect of preterm birth on neonatal cerebral vasculature studied with magnetic resonance angiography at 3 Tesla. Neuroimage 2006;32:1050-9.
8. Index of /human-development/Epicure/epicuretwo. Available from: www.nottingham.ac.uk/human-development/Epicure/epicuretwo.
9. Anderson P, Doyle LW, Victorian Infant Collaborative Study Group. Neurobehavioural outcomes of school-age children born extremely low birth weigh or very preterm in the 1990s. JAMA 2003;289:3264-72.
10. Briscoe J, Gathercole SE, Marlow N. Everyday memory and cognitive ability in children born very prematurely. J Child Psychol Psychiatry 2001;42:749-54.
11. 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.
12. Woodward LJ, Edgin JO, Thompson D, Inder TE. Object working memory deficits predicted by early brain injury and development in the preterm infant. Brain 2005;128(Pt 11):2578-87.
13. Botting 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.
14. 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.
15. Foulder-Hughes LA, Cooke RW. Motor, cognitive, and behavioural disorders in children born very preterm. Dev Med Child Neurol 2003;45:97-103.
16. Szatmari P, Saigal S, Rosenbaum P, Campbell D. Psychopathology and adaptive functioning among extremely low birthweight children at eight years of age. Dev Psychopathol 1993;5:345-57.
17. Indredavik MS, Vik T, Heyerdahl S, Kulseng S, Fayers P, Brubakk AM. Psychiatric symptoms and disorders in adolescents with low birth weight. Arch Dis Child Fetal Neonatal Ed 2004;89:F445-50.
18. Platt MJ, Cans C, Johnson A, Surman G, Topp M, Torrioli MG et al. Trends in cerebral palsy among infants of very low birthweight (<1500 g) or born prematurely (<32 weeks) in 16 European centres: a database study. Lancet 2007;369:43-50.
19. The Victorian Infant Collaborative Study Group. Outcome at 2 years of children 23-27 weeks' gestation born in Victoria in 1991-1992. J Paediatr Child Health 1997;33:161-5.
20. Hack M, Wilson-Costello D, Friedman H, Taylor GH, Schluchter M, Fanaroff AA. Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g: 1992-1995. Arch Pediatr Adolesc Med 2000;154:725-31.
21. Sheth RD. Trends in incidence and severity of intraventricular hemorrhage. J Child Neurol 1998;13:261-4.
22. th ed. Phila-delphia: W. B. Saunders Company; 2001.
23. Rutherford MA. Hemorrhagic lesions of the newborn brain. In: Rutherford MA, editor. MRI of the neonatal brain. London: W. B. Saunders; 2002.p.172-200.
24. Sherlock RL, Anderson PJ, Doyle LW. Neurodevelopmental sequelae of intraventricular haemorrhage at 8 years of age in a regional cohort of ELBW/very preterm infants. Early Hum Dev 2005; 81:909-16.
25. Patra K, Wilson-Costello D, Taylor HG, Mercuri-Minich N, Hack M. Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. J Pediatr 2006;149:169-73.
26. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978;92:529-34.
27. Hamrick SE, Miller SP, Leonard C, Glidden DV, Goldstein R, Ramaswamy V et al. Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J Pediatr 2004;145:593-9.
28. Larroque B, Marret S, Ancel PY, Arnaud C, Marpeau L, Supernant K et al.; EPIPAGE Study Group. White matter damage and intraventricular hemorrhage in very preterm infants: the EPIPAGE study. J Pediatr 2003;143:477-83.
29. Counsell SJ, Maalouf EF, Rutherford MA, Edwards AD. Periventricular haemorrhagic infarct in a preterm neonate. Eur J Paediatr Neurol 1999;3:25-7.
30. De Vries LS, Groenendaal F, van Haastert IC, Eken P, Rademaker KJ, Meiners LC. Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. Neuropediatrics 1999;30:314-9.
31. Debillon T, N'Guyen S, Muet A, Quere MP, Moussaly F, Roze JC. Limitations of ultrasonography for diagnosing white matter damage in preterm infants. Arch Dis Child Fetal Neonatal Ed 2003;88:F275-9.
32. Rademaker KJ, Groenendaal F, Jansen GH, Eken P, de Vries LS. Unilateral haemorrhagic parenchymal lesions in the preterm infant: shape, site and prognosis. Acta Paediatr 1994;83:602-8.
33. Amess PN, Baudin J, Townsend J, Meek J, Roth SC, Neville BG et al. Epilepsy in very preterm infants: neonatal cranial ultrasound reveals a high-risk subcategory. Dev Med Child Neurol 1998;40:724-30.
34. Maalouf EF, Duggan PJ, Rutherford MA, Counsell SJ, Fletcher AM, Battin M et al. Magnetic resonance imaging of the brain in a cohort of extremely preterm infants. J Pediatr 1999;135:351-7.
35. Inder TE, Wells SJ, Mogridge NB, Spencer C, Volpe JJ. Defining the nature of the cerebral abnormalities in the premature infant: a qualitative magnetic resonance imaging study. J Pediatr 2003;143:171-9.
36. Ment LR, Vohr B, Allan W, Westerveld M, Katz KH, Schneider KC et al. The etiology and outcome of cerebral ventriculomegaly at term in very low birth weight preterm infants. Pediatrics 1999;104(2 Pt 1):243-8.
37. Murphy BP, Inder TE, Rooks V, Taylor GA, Anderson NJ, Mogridge NB et al. Posthaemorrhagic ventricular dilatation in the premature infant: natural history and predictors of outcome. Arch Dis Child 2002;87:F37-F41.
38. Vollmer B, Roth S, Riley K, Sellwood MW, Baudin J, Neville BG et al. Neurodevelopmental outcome of preterm infants with ventricular dilatation with and without associated haemorrhage. Dev Med Child Neurol 2006;48:348-52.
39. Fletcher JM, Landry SH, Bohan TP, Davidson KC, Brookshire BL, Lachar D et al. Effects of intraventricular hemorrhage and hydrocephalus on the long-term neurobehavioral development of preterm very-low-birthweight infants. Dev Med Child Neurol 1997;39:596-606.
40. de Vries LS, Liem KD, van Dijk K, Smit BJ, Sie L, Rademaker KJ et al.; Dutch Working Group of Neonatal Neurology. Early versus late treatment of posthaem-orrhagic ventricular dilatation: results of a retrospective study from five neonatal intensive care units in The Netherlands. Acta Paediatr 2002;91:212-7.
41. Wharton KN, Pinar H, Stonestreet BS, Tucker R, McLean KR, Wallach M et al. Severe umbilical cord inflammation-a predictor of periventricular leukomalacia in very low birth weight infants. Early Hum Dev 2004;77:77-87.
42. Volpe JJ. Cerebral white matter injury of the premature infant-more common than you think. Pediatrics 2003;112:176-80.
43. Inder TE, Anderson NJ, Spencer C, Wells S, Volpe JJ. White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR Am J Neuroradiol 2003;24:805-9.
44. De Vries LS, Van Haastert IL, Rademaker KJ, Koopman C, Groenendaal F. Ultrasound abnormalities preceding cerebral palsy in high-risk preterm infants. J Pediatr 2004;144:815-20.
45. Roelants-van Rijn AM, Groenendaal F, Beek FJ, Eken P, van Haastert IC, de Vries LS. Parenchymal brain injury in the preterm infant: comparison of cranial ultrasound, MRI and neurodevelopmental outcome. Neuropediatrics 2001;32:80-9.
46. de Vries LS, Eken P, Groenendaal F, van Haastert IC, Meiners LC. Con-elation between the degree of periventricular leukomalacia diagnosed using cranial ultrasound and MRI later in infancy in children with cerebral palsy. Neuropediatrics 1993;24:263-8.
47. Pierrat V, Duquennoy C, van Haastert IC, Ernst M, Guilley N, de Vries LS. Ultrasound diagnosis and neurodevelopmental outcome of localised and extensive cystic periventricular leucomalacia. Arch Dis Child Fetal Neonatal Ed 2001;84:F151-6.
48. Jongmans M, Henderson S, de Vries L, Dubowitz L. Duration of periventricular densities in preterm infants and neurological outcome at 6 years of age. Arch Dis Child 1993;69(1 Spec No):9-13.
49. Jacobson L, Ygge J, Flodmark O, Ek U. Visual and perceptual characteristics, ocular motility and strabismus in children with periventricular leukomalacia. Strabismus 2002;10:179-83.
50. Ricci D, Anker S, Cowan F, Pane M, Gallini F, Luciano R et al. Thalamic atrophy in infants with PVL and cerebral visual impairment. Early Hum Dev 2006;82:591-5.
51. Cioni G, Fazzi B, Coluccini M, Bartalena L, Boldrini A, van Hof-van Duin J. Cerebral visual impairment in preterm infants with periventricular leucomalacia. Pediatr Neurol 1997;17:331-8.
52. Dyet LE, Kennea N, Counsell SJ Maalouf EF, Ajayi-Obe M, Duggan PJ et al. Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 2006;118:536-48.
53. Counsell SJ, Allsop JM, Harrison MC, Larkman DJ, Kennea NL, Kapellou O et al. Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 2003;112(1 Pt 1):1-7.
54. Back SA, Rivkees SA. Emerging concepts in periventricular white matter injury. Semin Perinatol 2004;28:405-14.
55. Folkerth RD. Periventricular leukomalacia: overview and recent findings. Pediatr Dev Pathol 2006;9:3-13.
56. Krishnan. Pediatrics. In Press 2007.
57. Cornette LG, Tanner SF, Ramenghi LA, Miall LS, Childs AM, Arthur RJ et al. Magnetic resonance imaging of the infant brain: anatomical characteristics and clinical significance of punctate lesions. Arch Dis Child Fetal Neonatal Ed 2002;86(3):F171-7.
58. Miller SP, Ferriero DM, Leonard C, Piecuch R, Glidden DV, Partridge JC et al. Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 2005;147:609-16.
59. Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 2006;355:685-94.
60. Grunnet ML, Shields WD. Cerebellar hemorrhage in the premature infant. J Pediatr 1976;88:605-8.
61. Merrill JD, Piecuch RE, Fell SC, Barkovich AJ, Goldstein RB. A new pattern of cerebellar hemorrhages in preterm infants. Pediatrics 1998;102:E62.
62. Miall LS, Cornette LG, Tanner SF, Arthur RJ, Levene MI. Posterior fossa abnormalities seen on magnetic resonance brain imaging in a cohort of newborn infants. J Perinatol 2003;23:396-403.
63. Mercuri E, He J, Curati WL, Dubowitz LM, Cowan FM, Bydder GM. Cerebellar infarction and atrophy in infants and children with a history of premature birth. Pediatr Radiol 1997;27:139-43.
64. Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R et al. Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol 2005;26:1659-67.
65. Allin MP, Salaria S, Nosarti C, Wyatt J, Rifkin L, Murray RM. Vermis and lateral lobes of the cerebellum in adolescents born very preterm. Neuroreport 2005;16:1821-4.
66. Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL et al. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 2001;124(Pt 1):60-6.
67. Rollins NK, Wen TS, Dominguez R. Crossed cerebellar atrophy in children: a neurologic sequela of extreme prematurity. Pediatr Radiol 1995;25 Suppl 1:S20-S25.
68. Leijser LM, Klein RH, Veen S, Liauw L, Van Wezel-Meijler G. Hyperechogenicity of the thalamus and basal ganglia in very preterm infants: radiological findings and short-term neurological outcome. Neuropediatrics 2004;35:283-9.
69. van Wezel-Meijler G, Hummel TZ, Oosting J, de Groot L, Sie LT, Huisman J et al. Unilateral thalamic lesions in premature infants: risk factors and short-term prognosis. Neuropediatrics 1999;30:300-6.
70. Barkovich AJ, Sargent SK. Profound asphyxia in the premature infant: imaging findings. AJNR Am J Neuroradiol 1995;16:1837-46.
71. Govaert P, Lequin M, Swarte R, Robben S, De Coo R, Weisglas-Kuperus N et al. Changes in globus pallidus with (pre)term kernicterus. Pediatrics 2003;112(6 Pt 1):1256-63.
72. Boardman JP, Counsell SJ, Rueckert D, Kapellou O, Bhatia KK, Aljabar P et al. Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage 2006;32:70-8.
73. Keeney SE, Adcock EW, McArdle CB. Prospective observations of 100 high-risk neonates by high-field (1.5 Tesla) magnetic resonance imaging of the central nervous system: I. Intraventricular and extracerebral lesions. Pediatrics 1991;87:421-30.
74. Hagmann CF, Schmitt-Mechelke T, Caduff JH, Berger TM. Fetal intracranial injuries in a preterm infant after maternal motor vehicle accident: a case report. Pediatr Crit Care Med 2004;5:396-8.
75. Ng PC, Fok TF, Lee CH, Wong W, Cheung KL. Massive subdural haematoma: an unusual complication of septicaemia in preterm very low birthweight infants. J Paediatr Child Health 1998;34:296-8.
76. Whitby EH, Griffiths PD, Rutter S, Smith MF, Sprigg A, Ohadike P et al. Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors. Lancet 2004;363:846-51.
77. Thompson PM, Giedd JN, Woods RP, MacDonald D, Evans AC, Toga AW. Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature 2000;404:190-3.
78. Ashburner J, Csernansky JG, Davatzikos C, Fox NC, Frisoni GB, Thompson PM. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol 2003;2:79-88.
79. Toga AW, Thompson PM. Genetics of brain structure and intelligence. Annu Rev Neurosci 2004;28:1-23.
80. Luders E, Narr KL, Thompson PM, Rex DE, Jancke L, Steinmetz H et al. Gender differences in cortical complexity. Nat Neurosci 2004;7:799-800.
81. Kapellou O, Counsell SJ, Kennea N, Dyet L, Saeed N, Stark J et al. Abnormal cortical development after premature birth shown by altered allometric scaling of brain growth. PLoS Med 2006;3:e265.
82. Counsell SJ, Maalouf EF, Fletcher AM, Duggan P, Battin M, Lewis HJ et al. MR imaging assessment of myelination in the very preterm brain. AJNR Am J Neuroradiol 2002;23:872-81.
83. 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.
84. Cooke RW, Abernethy LJ. Cranial magnetic resonance imaging and school performance in very low birth weight infants in adolescence. Arch Dis Child Fetal Neonatal Ed 1999;81:F116-F121.
85. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000;284:1939-47.
86. Isaacs EB, Edmonds CJ, Lucas A, Gadian DG. Calculation difficulties in children of very low birthweight: a neural correlate. Brain 2001;124(Pt 9):1701-7.
87. Abernethy LJ, Palaniappan M, Cooke RW. Quantitative magnetic resonance imaging of the brain in survivors of very low birth weight. Arch Dis Child 2002;87:279-83.
88. Isaacs EB, Edmonds CJ, Chong WK, Lucas A, Gadian DG. Cortical anomalies associated with visuospatial processing deficits. Ann Neurol 2003;53:768-73.
89. Isaacs EB, Vargha-Khadem F, Watkins KE, Lucas A, Mishkin M, Gadian DG. Developmental amnesia and its relationship to degree of hippocampal atrophy. Proc Natl Acad Sci U S A 2003;100:13060-3.
90. Abernethy LJ, Cooke RW, Foulder-Hughes L. Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatr Res 2004;55:884-93.
91. Isaacs EB, Edmonds CJ, Chong WK, Lucas A, Morley R, Gadian DG. Brain morphometry and IQ measurements in preterm children. Brain 2004;127(Pt 12):2595-607.
92. Nosarti C, Rushe TM, Woodruff PW, Stewart AL, Rifkin L, Murray RM. Corpus callosum size and very preterm birth: relationship to neuropsychological outcome. Brain 2004;127(Pt 9):2080-9.
93. Reiss AL, Kesler SR, Vohr B, Duncan CC, Katz KH, Pajot S et al. Sex differences in cerebral volumes of 8-year-olds born preterm. J Pediatr 2004;145:242-9.
94. Nosarti C, Allin MP, Frangou S, Rifkin L, Murray RM. Hyperactivity in adolescents born very preterm is associated with decreased caudate volume. Biol Psychiatry 2005;57:661-6.
95. Counsell SJ, Boardman JP. Differential brain growth in the infant born preterm: current knowledge and future developments from brain imaging. Semin Fetal Neonatal Med 2005;10:403-10.
96. Ajayi-Obe M, Saeed N, Cowan FM, Rutherford MA, Edwards AD. Reduced development of cerebral cortex in extremely preterm infants. Lancet 2000;356:1162-3.
97. Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M. Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 2006;27:573-9.
98. Srinivasan L, Dutta R, Counsell SJ, Allsop JM, Boardman JP, Rutherford MA et al. Quantification of deep gray matter in preterm infants at term-equivalent age using manual volumetry of 3-tesla magnetic resonance images. Pediatrics 2007;119:759-65.
99. Peterson BS, Anderson AW, Ehrenkranz R, Staib LH, Tageldin M, Colson E et al. Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 2003;111(5 Pt 1):939-48.
100. Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ. Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005;115:286-94.
101. Hunt RW, Warfield SK, Wang H, Kean M, Volpe JJ, Inder TE. Assessment of the impact of the removal of cerebrospinal fluid on cerebral tissue volumes by advanced volumetric 3D-MRI in posthaemorrhagic hydrocephalus in a premature infant. J Neurol Neurosurg Psychiatry 2003;74:658-60.
102. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, Lazeyras F et al. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res 2004;56:132-8.
103. 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.
104. Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK et al. Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 2005;116:844-50.
105. Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ. Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 1999;18:712-21.
106. Shah DK, Guinane C, August P, Austin NC, Woodward LJ. Thompson DK et al. Reduced occipital regional volumes at term predict impaired visual function in early childhood in very low birth weight infants. Invest Ophthalmol Vis Sci 2006;47:3366-73.
107. Arzoumanian Y, Mirmiran M, Barnes PD, Woolley K, Ariagno RL, Moseley ME et al. Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol 2003;24:1646-53.
108. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401-7.
109. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 2002;15:435-55.
110. Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA et al. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 1998;44:584-90.
111. Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR et al. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 1998;209:57-66.
112. Partridge SC, Mukherjee P, Henry RG, Miller SP, Berman JI, Jin H et al. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 2004;22:1302-14.
113. Tanner SF, Ramenghi LA, Ridgway JP, Berry E, Saysell MA, Martinez D et al. Quantitative comparison of intrabrain diffusion in adults and preterm and term neonates and infants. AJR Am J Roentgenol 2000;174:1643-9.
114. Toft PB, Leth H, Peitersen B, Lou HC, Thomsen C. The apparent diffusion coefficient of water in gray and white matter of the infant brain. J Comput Assist Tomogr 1996;20:1006-11.
115. Counsell SJ, Shen Y, Boardman JP, Larkman DJ, Kapellou O, Ward P et al. Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 2006;117:376-86.
116. Hildebrand C, Waxman SG. Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J Comp Neurol 1984;224:25-37.
117. Remahl S, Hilderbrand C. Relation between axons and oligodendroglial cells during initial myelination. I. The glial unit. J Neurocytol 1990;19:313-28.
118. Riederer BM. Some aspects of the neuronal cytoskeleton in development. Eur J Morphol 1990;28:347-78.
119. Watson D. Regional variation in the abundance of axonal cytoskeletal proteins. J Neurosci Res 1991;30:226-31.
120. Miller SP, Vigneron DB, Henry RG, Bohland MA, Ceppi-Cozzio C, Hoffman C et al. Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging 2002;16:621-32.
121. Huppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD et al. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 2001;107:455-60.
122. Berman JI, Mukherjee P, Partridge SC, Miller SP, Ferriero DM, Barkovich AJ et al. Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage 2005;27: 862-71.
123. Partridge SC, Mukherjee P, Berman JI, Henry RG, Miller SP, Lu Y et al. Tractography-based quantitation of diffusion tensor imaging parameters in white matter tracts of preterm newborns. J Magn Reson Imaging 2005;22: 467-74.
124. Yoo SS, Park HJ, Soul JS, Mamata H, Park H, Westin CF et al. In vivo visualization of white matter fiber tracts of preterm- and term-infant brains with diffusion tensor magnetic resonance imaging. Invest Radiol 2005;40:110-5.
125. Dubois J, Hertz-Pannier L, Dehaene-Lambertz G, Cointepas Y, Le Bihan D. Assessment of the early organization and maturation of infants' cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. Neuroimage 2006;30:1121-32.
126. Hoon AH Jr, Lawrie WT Jr, Melhem ER, Reinhardt EM, Van Zijl PC, Solaiyappan M et al. Diffusion tensor imaging of periventricular leukomalacia shows affected sensory cortex white matter pathways. Neurology 2002;59:752-6.
127. Seghier ML, Lazeyras F, Zimine S, Saudan-Frei S, Safran AB, Huppi PS. Visual recovery after perinatal stroke evidenced by functional and diffusion MRI: case report. BMC Neurol 2005;5:17.
128. Partridge SC, Vigneron DB, Charlton NN, Berman JI, Henry RG, Mukherjee P et al. Pyramidal tract maturation after brain injury in newborns with heart disease. Ann Neurol 2006;59:640-51.
129. Thomas B, Eyssen M, Peeters R, Molenaers G, Van Hecke P, De Cock P et al. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 2005;128(Pt 11):2562-77.
130. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003;6:750-7.
131. Counsell SJ, Dyet LE, Larkman DJ, Nunes RG, Boardman JP, Allsop JM et al. Thalamocortical connectivity in children born preterm mapped using probabilistic magnetic resonance tractography. Neuroimage 2007;34:896-904.
132. Anjari M, Srinivasan L, Allsop JM, Hajnal JV, Rutherford MA, Edwards AD et al. Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 2007;35:1021-7.
133. McKinstry RC, Mathur A, Miller JH, Ozcan A, Snyder AZ, Schefft GL et al. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex 2002;12:1237-43.
134. Gupta RK, Hasan KM, Trivedi R, Pradhan M, Das V, Parikh NA et al. Diffusion tensor imaging of the developing human cerebrum. J Neurosci Res 2005;81:172-8.
135. Marin-Padilla M. Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 1992;321: 223-40.
136. 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.
137. Deipolyi AR, Mukherjee P, Gill K, Henry RG, Partridge SC, Veeraraghavan S et al. Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. Neuroimage 2005;27:579-86.
138. Inder TE, Huppi PS, Warfield S, Kikinis R, Zientara GP, Barnes PD et al. Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann Neurol 1999;46:755-60.
139. Marin-Padilla M. Developmental neuropathology and impact of perinatal brain damage. III: gray matter lesions of the neocortex. J Neuropathol Exp Neurol 1999;58:407-29.
140. Lin Y, Okumura A, Hayakawa F, Kato K, Kuno T, Watanabe K. Quantitative evaluation of thalami and basal ganglia in infants with periventricular leukomalacia. Dev Med Child Neurol 2001;43:481-5.
141. Hughes CA, O'Gorman LA, Shyr Y, Schork MA, Bozynski ME, McCormick MC. Cognitive performance at school age of very low birth weight infants with bronchopulmonary dysplasia. J Dev Behav Pediatr 1999;20:1-8.
142. Short EJ, Klein NK, Lewis BA, Fulton S, Eisengart S, Kercsmar C et al. Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes. Pediatrics 2003;112:e359.
143. Thompson DK, Warfield SK, Carlin JB, Pavlovic M, Wang HX, Bear M et al. Perinatal risk factors altering regional brain structure in the preterm infant. Brain 2007; 130(Pt 3):667-77.
144. Boardman. Ann Neurol. In Press 2007.
145. Felderhoff-Mueser U, Sifringer M, Polley O, Dzietko M, Leineweber B, Mahler L et al. Caspase-1-processed interleukins in hyperoxia-induced cell death in the developing brain. Ann Neurol 2005;57:50-9.
146. Loeliger M, Inder T, Cain S, Ramesh RC, Camm E, Thomson MA et al. Cerebral outcomes in a preterm baboon model of early versus delayed nasal continuous positive airway pressure. Pediatrics 2006;118:1640-53.
147. Cunningham S, Fleck BW, Elton RA, McIntosh N. Transcutaneous oxygen levels in retinopathy of prematurity. Lancet 1995;346:1464-5.
148. Barrington KJ. The adverse neuro-developmental effects of postnatal steroids in the preterm infant: a systematic review of RCTs. BMC Pediatr 2001;1:1.
149. Lodygensky GA, Rademaker K, Zimine S, Gex-Fabry M, Lieftink AF, Lazeyras F et al. Structural and functional brain development after hydrocortisone treatment for neonatal chronic lung disease. Pediatrics 2005;116:1-7.
150. Sung IK, Vohr B, Oh W. Growth and neurodevelopmental outcome of very low birth weight infants with intrauterine growth retardation: comparison with control subjects matched by birth weight and gestational age. J Pediatr 1993;123:618-24.
151. Low JA, Handley-Derry MH, Burke SO, Peters RD, Pater EA, Killen HL et al. Association of intrauterine fetal growth retardation and learning deficits at age 9 to 11 years. Am J Obstet Gynecol 1992;167:1499-505.
152. Hack M, Flannery DJ, Schluchter M, Cartar L, Borawski E, Klein N. Outcomes in young adulthood for very-low-birth-weight infants. N Engl J Med 2002;346:149-57.
153. Hindmarsh GJ, O'Callaghan MJ, Mohay HA, Rogers YM. Gender differences in cognitive abilities at 2 years in ELBW infants. Extremely low birth weight. Early Hum Dev 2000;60:115-22.
154. Ment LR, Vohr BR, Makuch RW, Westerveld M, Katz KH, Schneider KC et al. Prevention of intraventricular hemorrhage by indomethacin in male preterm infants. J Pediatr 2004;145:832-4.
155. Ohlsson A, Roberts RS, Schmidt B, Davis P, Moddeman D, Saigal S et al.; The Trial Of Indomethacin Prophylaxis In Preterms Tipp Investigators. Male/female differences in indomethacin effects in preterm infants. J Pediatr 2005;147:860-2.
156. Giedd JN, Clasen LS, Lenroot R, Greenstein D, Wallace GL, Ordaz S et al. Puberty-related influences on brain development. Mol Cell Endocrinol 2006;254-255:154-62.
157. Arnold AP. Sex chromosomes and brain gender. Nat Rev Neurosci 2004;5:701-8.
158. Yoon BH, Romero R, Yang SH, Jun JK, Kim IO, Choi JH et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996;174:1433-40.
159. Wu YW. Systematic review of chorioamnionitis and cerebral palsy. Ment Retard Dev Disabil Res Rev 2002;8:25-9.
160. Duggan PJ, Maalouf EF, Watts TL, Sullivan MH, Counsell SJ, Allsop J et al. Intrauterine T-cell activation and increased proinflammatory cytokine concentrations in preterm infants with cerebral lesions. Lancet 2001;358:1699-700.
161. Leviton A, Paneth N, Reuss ML, Susser M, Allred EN, Dammann O et al. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Developmental Epidemiology Network Investigators. Pediatr Res 1999;46:566-75.
162. Nelson KB, Dambrosia JM, Grether JK, Phillips TM. Neonatal cytokines and coagulation factors in children with cerebral palsy. Ann Neurol 1998;44:665-75.
163. Grether JK, Nelson KB, Dambrosia JM, Phillips TM. Interferons and cerebral palsy. J Pediatr 1999;134:324-32.
164. Redline RW, Wilson-Costello D, Borawski E, Fanaroff AA, Hack M. Placental lesions associated with neurologic impairment and cerebral palsy in very low-birth-weight infants. Arch Pathol Lab Med 1998;122:1091-8.