Neuroimaging biomarkers of preterm brain injury: Toward developing the preterm connectome

Pediatric Radiology

Volumn 42, Issue SUPPL. 1, 2012, Pages

  Panigrahy, Ashok ^a,b   Wisnowski, Jessica L ^a,c   Furtado, Andre ^b   Lepore, Natasha ^a   Paquette, Lisa ^a   Bluml, Stefan ^a,d  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d NONE   (United States)

Author keywords

Cranial US; MRI; Neuroimaging biomarkers; White matter injury of prematurity

Indexed keywords

BIOLOGICAL MARKER; CHOLINE; LACTIC ACID; N ACETYLASPARTIC ACID;

ARTICLE; BLOOD FLOW VELOCITY; BRAIN BLOOD FLOW; BRAIN DEVELOPMENT; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN METABOLISM; BRAIN SIZE; BRAIN VENTRICLE; CEREBELLUM; CEREBRAL PALSY; COGNITION; CORPUS CALLOSUM; DIAGNOSTIC VALUE; DISEASE CLASSIFICATION; DISEASE SEVERITY; DOPPLER ECHOGRAPHY; ENCEPHALOMALACIA; FETUS; HUMAN; INFANT; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROSCIENCE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTCOMES RESEARCH; PREMATURITY; PRIORITY JOURNAL; PROGNOSIS; PROTON NUCLEAR MAGNETIC RESONANCE; SCREENING; ULTRASOUND; WHITE MATTER;

BIRTH INJURIES; BRAIN INJURIES; BRAIN MAPPING; FUNCTIONAL NEUROIMAGING; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE, DISEASES; NEUROIMAGING;

EID: 84863482570     PISSN: 03010449     EISSN: 14321998     Source Type: Journal    
DOI: 10.1007/s00247-011-2239-4     Document Type: Article

References (152)

1. Stoll BJ, Hansen NI, Bell EF et al (2010) Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics 126:443-456
2. EXPRESS Group (2010) Incidence of and risk factors for neonatal morbidity after active perinatal care: extremely preterm infants study in Sweden (EXPRESS). Acta Paediatr 99:978-992
3. Lemons JA, Bauer CR, Oh W et al (2001) Very low birth weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, January 1995 through December 1996. NICHD Neonatal Research Network. Pediatrics 107:E1
4. Aarnoudse-Moens CS, Weisglas-Kuperus N, van Goudoever JB et al (2009) Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics 124:717-728
5. Saigal S, Hoult LA, Streiner DL et al (2000) School difficulties at adolescence in a regional cohort of children who were extremely low birth weight. Pediatrics 105:325-331 (Pubitemid 30078672)
6. Hack M (2006) Young adult outcomes of very-low-birth-weight children. Semin Fetal Neonatal Med 11:127-137
7. Sie LT, van der Knaap MS, van Wezel-Meijler G et al (2000) Early MR features of hypoxic-ischemic brain injury in neonates with periventricular densities on sonograms. AJNR 21:852-861 (Pubitemid 30262831)
8. Maalouf EF, Duggan PJ, Counsell SJ et al (2001) Comparison of findings on cranial ultrasound and magnetic resonance imaging in preterm neonates. Pediatrics 107:719-727 (Pubitemid 32268457)
9. Miller SP, Cozzio EE, Goldstein RB et al (2003) Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. AJNR 24:1661-1669 (Pubitemid 37151738)
10. Inder TE, Anderson NJ, Spencer C et al (2003) White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR 24:805-809 (Pubitemid 36617405)
11. Childs A-M, Cornette L, Ramenghi LA et al (2001) Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. Clin Radiol 56:647-655 (Pubitemid 35023782)
12. Hagmann P, Cammoun L, Gigandet X et al (2010) MR connectomics: principles and challenges. J Neurosci Methods 194(1):34-45
13. Sporns O (2011) The human connectome: a complex network. Ann NY Acad Sci 1224(1):109-125
14. Jensen FE (2011) Epilepsy as a spectrum disorder: implications from novel clinical and basic neuroscience. Epilepsia 52(Suppl 1):1-6
15. Rubinov M, Bassett DS (2011) Emerging evidence of connectomic abnormalities in schizophrenia. J Neurosci 31(17):6263-6265
16. Ment LR, Hirtz D, Hüppi PS (2009) Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol 8 (11):1042-1055
17. Volpe JJ, Kinney HC, Jensen FE et al (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29(4):423-440
18. Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8(1):110-124
19. Hill A, Melson GL, Clark HB et al (1982) Hemorrhagic periventricular leukomalacia: diagnosis by real time ultrasound and correlation with autopsy findings. Pediatrics 69:282-284 (Pubitemid 12171577)
20. Manger MN, Feldman RC, Brown WJ et al (1984) Intracranial ultrasound diagnosis of neonatal periventricular leukomalacia. J Ultrasound Med 3:59-63 (Pubitemid 14172933)
21. Fawer CL, Calame A, Perentes E et al (1985) Periventricular leukomalacia: a correlation study between real-time ultrasound and autopsy findings. Periventricular leukomalacia in the neonate. Neuroradiology 27:292-300 (Pubitemid 15030941)
22. Correa F, Enriquez G, Rossello J et al (2004) Posterior fontanelle sonography: an acoustic window into the neonatal brain. AJNR 25:1274-1282 (Pubitemid 39095182)
23. Luna JA, Goldstein RB (2000) Sonographic visualization of neonatal posterior fossa abnormalities through the posterolateral fontanelle. AJR 174:561-567 (Pubitemid 30067178)
24. Anderson N, Allan R, Darlow B et al (1994) Diagnosis of intraventricular hemorrhage in the newborn: value of sonography via the posterior fontanelle. AJR 163:893-896 (Pubitemid 24313154)
25. O'Shea TM, Allred EN, Dammann O et al (2009) ELGAN study of the brain and related disorders in extremely low gestational age newborns. Early Hum Dev 85(11):719-725
26. Hintz SR, Slovis T, Bulas D et al (2007) Interobserver reliability and accuracy of cranial ultrasound scanning interpretation in premature infants. J Pediatr 150(6):592-596
27. Barkovich AJ (2006) MR imaging of the neonatal brain. Neuroimaging Clin N Am 16:117-135
28. Blüml S, Friedlich P, Erberich S et al (2004) MR imaging of newborns by using an MR-compatible incubator with integrated radiofrequency coils: initial experience. Radiology 231(2):594-601 (Pubitemid 38552922)
29. Wilson-Costello D, Friedman H, Minich N et al (2005) Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 115 (4):997-1003
30. Papile LA, Burstein J, Burstein R et al (1978) Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weight less than 1,500 gm. J Pediatr 92:529-534 (Pubitemid 8293290)
31. Vohr BR, Wright LL, Poole WK et al (2005) Neurodevelopmental outcomes of extremely low birth weight infants <32 weeks' gestation between 1993 and 1998. Pediatrics 116 (3):635-643 (Pubitemid 44336680)
32. Marlow N, Wolke D, Bracewell MA et al (2005) Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 352(1):9-19 (Pubitemid 40075676)
33. Hack M, Wilson-Costello D, Friedman H et al (2000) Neurodevelopment and predictors of outcomes of children with birth weights of less than 1,000 g: 1992-1995. Arch Pediatr Adolesc Med 154(7):725-731 (Pubitemid 30437556)
34. Patra K, Wilson-Costello D, Taylor HG et al (2006) Grades I-II intraventricular hemorrhage in extremely low birth weight infants: effects on neurodevelopment. J Pediatr 149 (2):169-173 (Pubitemid 44128556)
35. Leijser LM, Srinivasan L, Rutherford MA et al (2007) Structural linear measurements in the newborn brain: accuracy of cranial ultrasound compared to MRI. Pediatr Radiol 37:640-648 (Pubitemid 46929938)
36. Horsch S, Bengtsson J, Nordell A et al (2009) Lateral ventricular size in extremely premature infants: 3D MRI confirms 2D ultrasound measurements. Ultrasound Med Biol 35:360-366
37. Levene MI, Starte DR (1981) A longitudinal study of post-haemorrhagic ventricular dilatation in the newborn. Arch Dis Child 56:905-910 (Pubitemid 12250481)
38. London DA, Carroll BA, Enzmann DR (1980) Sonography of ventricular size and germinal matrix hemorrhage in premature infants. AJR 135:559-564 (Pubitemid 10048786)
39. Grasby DC, Esterman A, Marshall P (2003) Ultrasound grading of cerebral ventricular dilatation in preterm neonates. J Paediatr Child Health 39:186-190 (Pubitemid 36469916)
40. Maunu J, Lehtonen L, Lapinleimu H et al (2011) Ventricular dilatation in relation to outcome at 2 years of age in very preterm infants: a prospective Finnish cohort study. Dev Med Child Neurol 53:48-54
41. El-Dib M, Massaro AN, Bulas D et al (2010) Neuroimaging and neurodevelopmental outcome of premature infants. Am J Perinatol 27:803-818
42. Del Bigio MR (1993) Neuropathological changes caused by hydrocephalus. Acta Neuropathol 85:573-585 (Pubitemid 23212023)
43. Del Bigio MR (2001) Pathophysiologic consequences of hydrocephalus. Neurosurg Clin N Am 12:639-649 (Pubitemid 32924269)
44. Del Bigio MR, da Silva MC, Drake JM et al (1994) Acute and chronic cerebral white matter damage in neonatal hydrocephalus. Can J Neurol Sci 21:299-305 (Pubitemid 24358530)
45. Kuban KC, Allred EN, O'Shea TM et al (2009) Cranial ultrasound lesions in the NICU predict cerebral palsy at age 2 years in children born at extremely low gestational age. J Child Neurol 24:63-72
46. Skranes JS, Vik T, Nilsen G et al (1993) Cerebral magnetic resonance imaging (MRI) and mental and motor function of very low birth weight infants at one year of corrected age. Neuropediatrics 24:256-262 (Pubitemid 23339375)
47. Dyet LE, Kennea N, Counsell SJ et al (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118:536-548 (Pubitemid 46085408)
48. Volpe JJ (2005) Encephalopathy of prematurity includes neuronal abnormalities. Pediatrics 116(1):221-225
49. de Vries LS, Eken P, Dubowitz LM (1992) The spectrum of leukomalacia using cranial ultrasound. Behav Brain Res 49:1-6
50. Nanba Y, Matsui K, Aida N et al (2007) Magnetic resonance imaging regional T1 abnormalities at term accurately predict motor outcome in preterm infants. Pediatrics 120:e10-e19 (Pubitemid 47036211)
51. Aida N, Nishimura G, Hachiya Y et al (1998) MR imaging of perinatal brain damage: comparison of clinical outcome with initial and follow-up MR findings. AJNR 19:1909-1921 (Pubitemid 30409574)
52. Olsen P, Paakko E, Vainionpaa L et al (1997) Magnetic resonance imaging of periventricular leukomalacia and its clinical correlation in children. Ann Neurol 41:754-761 (Pubitemid 27249180)
53. Rutherford MA, Supramaniam V, Ederies A et al (2010) Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 52(6):505-521
54. Niwa T, de Vries LS, Benders MJ et al (2011) Punctate white matter lesions in infants: new insights using susceptibility-weighted imaging. Neuroradiology 53(9):669-679 [May 7 Epub ahead of print]
55. Ramenghi LA, Fumagalli M, Righini A et al (2007) Magnetic resonance imaging assessment of brain maturation in preterm neonates with punctate white matter lesions. Neuroradiology 49 (2):161-167 (Pubitemid 46218589)
56. Bassi L, Chew A, Merchant N et al (2011) Diffusion tensor imaging in preterm infants with punctate white matter lesions. Pediatr Res 69(6):561-566
57. Cornette LG, Tanner SF, Ramenghi LA et al (2002) Magnetic resonance imaging of the infant brain: anatomical characteristics and clinical significance of punctate lesions. Arch Dis Child Fetal Neonatal Ed 86(3):F171-F177 (Pubitemid 34478247)
58. Miller SP, Ferriero DM, Leonard C et al (2005) Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 147(5):609-616 (Pubitemid 41598332)
59. Volpe JJ (2003) Cerebral white matter injury of the premature infant - more common than you think. Pediatrics 112:176-180 (Pubitemid 36792944)
60. Domizio S, Barbante E, Puglielli C et al (2005) Excessively high magnetic resonance signal in preterm infants and neuropsycho-behavioural follow-up at 2 years. Int J Immunopathol Pharmacol 18:365-375 (Pubitemid 40825898)
61. Skiöld B, Horsch S, Hallberg B et al (2010) White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Paediatr 99(6):842-849
62. Srinivasan L, Dutta R, Counsell SJ et al (2007) Quantification of deep gray matter in preterm infants at term-equivalent age using manual volumetry of 3-tesla magnetic resonance images. Pediatrics 119(4):759-765 (Pubitemid 46556675)
63. Boardman JP, Counsell SJ, Rueckert D et al (2006) Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage 32(1):70-78
64. Hart AR, Smith MF, Rigby AS et al (2010) Appearances of diffuse excessive high signal intensity (DEHSI) on MR imaging following preterm birth. Pediatr Radiol 40:1390-1396
65. Skiöld B (2010) Brain imaging and outcome in extremely preterm infants. Arch Dis Child Fetal Neonatal Ed 95(5):F310-F314
66. Kim JH, Jeon TY, Yoo S-Y et al (2011) Neurodevelopmental outcomes in preterm infants wcbith diffuse excessive high signal intensity seen on MRI at near term-equivalent age. Pediatr Radiol 41(Suppl 1):S296, Abstract NE1-5
67. Kidokoro H, Anderson PJ, Doyle LW et al (2011) High signal intensity on T2-weighted MR imaging at term-equivalent age in preterm infants does not predict 2-year neurodevelopmental putcomes. AJNR. doi:10.3174/ajnr.A2703
68. Counsell SJ, Allsop JM, Harrison MC et al (2003) Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 112:1-7 (Pubitemid 36792921)
69. Krishnan ML, Dyet LE, Boardman JP et al (2007) Relationship between white matter apparent diffusion coefficients in preterm infants at term-equivalent age and developmental outcome at 2 years. Pediatrics 120:e604-e609 (Pubitemid 47364626)
70. Inder TE, Warfield SK, Wang H et al (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286-294 (Pubitemid 43193809)
71. Peterson BS, Anderson AW, Ehrenkranz R et al (2003) Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 111:939-948 (Pubitemid 36542604)
72. Rademaker KJ, Lam JN, Van Haastert IC et al (2004) Larger corpus callosum size with better motor performance in prematurely born children. Semin Perinatol 28:279-287 (Pubitemid 40288069)
73. Iai M, Tanabe Y, Goto M et al (1994) A comparative magnetic resonance imaging study of the corpus callosum in neurologi-cally normal children and children with spastic diplegia. Acta Paediatr 83:1086-1090 (Pubitemid 24335781)
74. Panigrahy A, Barnes PD, Robertson RL et al (2005) Quantitative analysis of the corpus callosum in children with cerebral palsy and developmental delay: correlation with cerebral white matter volume. Pediatr Radiol 35:1199-1207 (Pubitemid 41829708)
75. Nosarti C, Rushe TM, Woodruff PW et al (2004) Corpus callosum size and very preterm birth: relationship to neuropsychological outcome. Brain 127:2080-2089 (Pubitemid 39150265)
76. Anderson NG, Laurent I, Cook N et al (2005) Growth rate of corpus callosum in very premature infants. AJNR 26:2685-2690
77. Anderson NG, Laurent I, Woodward LJ et al (2006) Detection of impaired growth of the corpus callosum in premature infants. Pediatrics 118:951-960 (Pubitemid 46090034)
78. Rose J, Butler EE, Lamont LE et al (2009) Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 51:526-535
79. Counsell SJ, Edwards AD, Chew AT et al (2008) Specific relations between neurodevelopmental abilities and white matter microstructure in children born preterm. Brain 131:3201-3208
80. De Vries LS, Groenendaal F, van Haastert IC et al (1999) Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. Neuropediatrics 30:314-319 (Pubitemid 30088323)
81. Roelants-van Rijn AM, Groenendaal F, Beek FJ et al (2001) Parenchymal brain injury in the preterm infant: comparison of cranial ultrasound, MRI and neurodevelopmental outcome. Neuropediatrics 32:80-89 (Pubitemid 32488001)
82. Arzoumanian Y, Mirmiran M, Barnes PD et al (2003) Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR 24:1646-1653 (Pubitemid 37151736)
83. Rose J, Mirmiran M, Butler EE et al (2007) Neonatal microstructural development of the internal capsule on diffusion tensor imaging correlates with severity of gait and motor deficits. Dev Med Child Neurol 49:745-750 (Pubitemid 47456449)
84. Murakami A, Morimoto M, Yamada K et al (2008) Fibertracking techniques can predict the degree of neurologic impairment for periventricular leukomalacia. Pediatrics 122:500-506
85. O'Connor AR, Fielder AR (2007) Visual outcomes and perinatal adversity. Semin Fetal Neonatal Med 12:408-414 (Pubitemid 47386049)
86. Shah DK, Guinane C, August P et al (2006) Reduced occipital regional volumes at term predict impaired visual function in early childhood in very low birth weight infants. Invest Ophthalmol Vis Sci 47:3366-3373 (Pubitemid 351639699)
87. Berman JI, Glass HC, Miller SP et al (2009) Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns. AJNR 30:120-124
88. Bassi L, Ricci D, Volzone A et al (2008) Probabilistic diffusion tractography of the optic radiations and visual function in preterm infants at term equivalent age. Brain 131:573-582 (Pubitemid 351197622)
89. Kapellou O, Counsell SJ, Kennea N et al (2006) Abnormal cortical development after premature birth shown by altered allometric scaling of brain growth. PLoS Med 3:e265
90. Nosarti C, Al-Asady MH, Frangou S et al (2002) Adolescents who were born very preterm have decreased brain volumes. Brain 125:1616-1623 (Pubitemid 34755175)
91. Dubois J, Benders M, Borradori-Tolsa C et al (2008) Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131:2028-2041
92. Soria-Pastor S, Padilla N, Zubiaurre-Elorza L et al (2009) Decreased regional brain volume and cognitive impairment in preterm children at low risk. Pediatrics 124:e1161-e1170
93. Peterson BS, Vohr B, Staib LH et al (2000) Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 284:1939-1947
94. Anderson P, Doyle LW (2003) Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA 289:3264-3272 (Pubitemid 37430079)
95. Woodward LJ, Edgin JO, Thompson D et al (2005) Object working memory deficits predicted by early brain injury and development in the preterm infant. Brain 128:2578-2587 (Pubitemid 41552943)
96. Beauchamp MH, Thompson DK, Howard K et al (2008) Preterm infant hippocampal volumes correlate with later working memory deficits. Brain 131:2986-2994
97. Limperopoulos C, Bassan H, Gauvreau K et al (2007) Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 120:584-593 (Pubitemid 47358302)
98. Limperopoulos C, Benson CB, Bassan H et al (2005) Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics 116:717-724 (Pubitemid 44336690)
99. Bednarek N, Akhavi A, Pietrement C et al (2008) Outcome of cerebellar injury in very low birth-weight infants: 6 case reports. J Child Neurol 23:906-911
100. Tam EW, Rosenbluth G, Rogers EE et al (2011) Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatri 158:245-250
101. Ecury-Goossen GM, Dudink J, Lequin M et al (2010) The clinical presentation of preterm cerebellar haemorrhage. Eur J Pediatr 169:1249-1253
102. Merrill JD, Piecuch RE, Fell SC et al (1998) A new pattern of cerebellar hemorrhages in preterm infants. Pediatrics 102:E62
103. Steggerda SJ, Leijser LM, Wiggers-de Bruine FT et al (2009) Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology 252:190-199
104. Shah DK, Anderson PJ, Carlin JB et al (2006) Reduction in cerebellar volumes in preterm infants: relationship to white matter injury and neurodevelopment at two years of age. Pediatr Res 60:97-102 (Pubitemid 44297621)
105. Srinivasan L, Allsop J, Counsell SJ et al (2006) Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR 27:573-579 (Pubitemid 44897776)
106. Lind A, Parkkola R, Lehtonen L et al (2011) Associations between regional brain volumes at term-equivalent age and development at 2 years of age in preterm children. Pediatr Radiol 41:953-961
107. Tam EW, Miller SP, Studholme C et al (2011) Differential effects of intraventricular hemorrhage and white matter injury on cerebellar growth. J Pediatr 158(3):366-371
108. Limperopoulos C, Chilingaryan G, Gulzard N et al (2010) Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res 68 (2):145-150
109. Woodward LJ, Anderson PJ, Austin NC et al (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 355:685-694
110. Valkama AM, Paakko EL, Vainionpaa LK et al (2000) Magnetic resonance imaging at term and neuromotor outcome in preterm infants. Acta Paediatr 89:348-355 (Pubitemid 30625362)
111. Kreis R, Hofmann L, Kuhlmann B et al (2002) Brain metabolite composition during early human brain development as measured by quantitative in vivo 1H magnetic resonance spectroscopy. Magn Reson Med 48:949-958 (Pubitemid 35398524)
112. Leth H, Toft PB, Pryds O et al (1995) Brain lactate in preterm and growth-retarded neonates. Acta Paediatr 84:495-499
113. Wang ZJ, Vigneron DB, Miller SP et al (2008) Brain metabolite levels assessed by lactate-edited MR spectroscopy in premature neonates with and without pentobarbital sedation. AJNR 29:798-801 (Pubitemid 351571567)
114. Roelants-van Rijn AM, van der Grond J, Stigter RH et al (2004) Cerebral structure and metabolism and long-term outcome in smallfor-gestational-age preterm neonates. Pediatr Res 56:285-290 (Pubitemid 38971825)
115. Augustine EM, Spielman DM, Barnes PD et al (2008) Can magnetic resonance spectroscopy predict neurodevelopmental outcome in very low birth weight preterm infants? J Perinatol 28:611-618
116. Bode H, Wais U (1988) Age dependence of flow velocities in basal cerebral arteries. Arch Dis Child 63:606-611
117. Kehrer M, Krageloh-Mann I, Goelz R et al (2003) The development of cerebral perfusion in healthy preterm and term neonates. Neuropediatrics 34:281-286 (Pubitemid 38057032)
118. Perlman JM, McMenamin JB, Volpe JJ (1983) Fluctuating cerebral blood-flow velocity in respiratory-distress syndrome. Relation to the development of intraventricular hemorrhage. N Engl J Med 309:204-209 (Pubitemid 13070238)
119. Julkunen M, Parviainen T, Janas M et al (2008) End-diastolic block in cerebral circulation may predict intraventricular hemorrhage in hypotensive extremely-low-birth-weight infants. Ultrasound Med Biol 34:538-545 (Pubitemid 351417694)
120. Westra SJ, Lazareff J, Curran JG et al (1998) Transcranial Doppler ultrasonography to evaluate need for cerebrospinal fluid drainage in hydrocephalic children. J Ultrasound Med 17:561-569 (Pubitemid 28397574)
121. Taylor GA, Madsen JR (1996) Neonatal hydrocephalus: hemodynamic response to fontanelle compression - correlation with intracranial pressure and need for shunt placement. Radiology 201:685-689
122. Nguyen The Tich S, Anderson PJ, Shimony JS (2009) A novel quantitative simple brain metric using MR imaging for preterm infants. AJNR 30(1):125-131
123. Tich SN, Anderson PJ, Hunt RW et al (2011) Neurodevelopmental and perinatal correlates of simple brain metrics in very preterm infants. Arch Pediatr Adolesc Med 165(3):216-222
124. Biswal B, Yetkin FZ, Haughton VM et al (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541
125. Lowe MJ, Mock BJ, Sorenson JA (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7:119-132 (Pubitemid 28355547)
126. Beckmann CF, DeLuca M, Devlin JT et al (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001-1013 (Pubitemid 41672861)
127. Fox MD, Snyder AZ, Vincent JL et al (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673-9678 (Pubitemid 40981739)
128. Fransson P, Skiold B, Horsch S et al (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci USA 104:15531-15536 (Pubitemid 47502951)
129. Smyser CD, Inder TE, Shimony JS et al (2010) Longitudinal analysis of neural network development in preterm infants. Cereb Cortex 20:2852-2862
130. Doria V, Beckmann CF, Arichi T et al (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci USA 107(46):20015-20020
131. Kostovic I, Jovanov-Milosevic N (2006) The development of cerebral connections during the first 20-45 weeks' gestation. Semin Fetal Neonatal Med 11:415-422 (Pubitemid 44666590)
132. Damaraju E, Phillips JR, Lowe JR et al (2010) Resting-state functional connectivity differences in premature children. Front Syst Neuro 4:23
133. de Vries LS, Cowan FM (2007) Should cranial MRI screening of preterm infants become routine? Nat Clin Pract Neurol 3 (10):532-533 (Pubitemid 47528024)
134. Hintz SR, O'Shea M (2008) Neuroimaging and neurodevelopmental outcomes in preterm infants. Semin Perinatol 32(1):11-19 (Pubitemid 351174358)
135. Hart AR, Whitby EW, Griffiths PD et al (2008) Magnetic resonance imaging and developmental outcome following preterm birth: review of current evidence. Dev Med Child Neurol 50(9):655-663
136. Ment LR, Bada HS, Barnes P et al (2002) Practice parameter: neuroimaging of the neonate. Report of the quality standards subcommittee of the American academy of neurology and the practice committee of the child neurology society. Neurology 58:1726-1738 (Pubitemid 34663570)
137. Nosarti C, Walshe M, Rushe TM et al (2011) Neonatal ultrasound results following very preterm birth predict adolescent behavioral and cognitive outcome. Dev Neuropsychol 36(1):118-135
138. Clark CA, Woodward LJ (2010) Neonatal cerebral abnormalities and later verbal and visuospatial working memory abilities of children born very preterm. Dev Neuropsychol 35(6):622-642
139. Woodward LJ, Clark CA, Pritchard VE et al (2011) Neonatal white matter abnormalities predict global executive function impairment in children born very preterm. Dev Neuropsychol 36 (1):22-41
140. Munck P, Haataja L, Maunu J et al (2010) Cognitive outcome at 2 years of age in Finnish infants with very low birth weight born between 2001 and 2006. Acta Paediatr 99(3):359-366
141. Horsch S, Skiold B, Hallberg B et al (2009) Cranial ultrasound and MRI at term age in extremely preterm infants. Arch Dis Child Fetal Neonatal Ed 95:19
142. Kinney HC (2006) The near term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol 30(2):81-88 (Pubitemid 43767144)
143. O'Shea TM, Klinepeter KL, Dillard RG (1998) Prenatal events and the risk of cerebral palsy in very low birth weight infants. Am J Epidemiol 147:362-369
144. Laptook AR, O'Shea TM, Shankaran S et al (2005) Adverse neurodevelopmental outcomes among extremely low birth weight infants with a normal head ultrasound: prevalence and antecedents. Pediatrics 115:673-680 (Pubitemid 43373028)
145. Wood NS, Costeloe K, Gibson AT et al (2005) The EPICure study: associations and antecedents of neurological and developmental disability at 30 months of age following extremely preterm birth. Arch Dis Child Fetal Neonatal Ed 90:F134-F140 (Pubitemid 40333082)
146. Shah DK, Doyle LW, Anderson PJ et al (2008) Adverse neurodevelopment in preterm infants with postnatal sepsis or necrotizing enterocolitis is mediated by white matter abnormalities on magnetic resonance imaging at term. J Pediatr 153:170-175
147. Glass HC, Bonifacio SL, Chau V et al (2008) Recurrent postnatal infections are associated with progressive white matter injury in premature infants. Pediatrics 122:299-305
148. Chau V, Poskitt KJ, McFadden DE et al (2009) Effect of chorioamnionitis on brain development and injury in premature newborns. Ann Neurol 66:155-164
149. Doyle LW, Cheong J, Hunt RW (2010) Caffeine and brain development in very preterm infants. Ann Neurol 68(5):734-742
150. Murphy BP, Inder TE, Huppi PS et al (2001) Impaired cerebral cortical gray matter growth after treatment with dexamethasone for neonatal chronic lung disease. Pediatrics 107(2):217-221 (Pubitemid 32121232)
151. Als H, Duffy FH, McAnulty GB et al (2004) Early experience alters brain function and structure. Pediatrics 113(4):846-857 (Pubitemid 38437393)
152. Milgrom J, Newnham C, Anderson PJ et al (2010) Early sensitivity training for parents of preterm infants: impact on the developing brain. Pediatric Res 67(3):330-335