MR Imaging of the Term and Preterm Neonate with Diffuse Brain Injury

Magnetic Resonance Imaging Clinics of North America

Volumn 19, Issue 4, 2011, Pages 709-731

  Izbudak, Izlem ^a   Grant, P Ellen ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Brain; Hypoxia ischemia encephalopathy; Magnetic resonance imaging; Newborn; Outcome; Premature

Indexed keywords

BRAIN BLOOD FLOW; BRAIN HEMORRHAGE; BRAIN INJURY; CLINICAL PROTOCOL; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; EARLY DIAGNOSIS; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INDUCED HYPOTHERMIA; NEWBORN HYPOXIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PATIENT TRANSPORT; PERINATAL ASPHYXIA; PREDICTION; PREMATURITY; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SEDATION; TREATMENT OUTCOME; WHITE MATTER; WHITE MATTER INJURY OF PREMATURITY;

BRAIN; BRAIN INJURIES; FEMALE; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; IMAGE ENHANCEMENT; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING; POSTNATAL CARE;

EID: 82755189930     PISSN: 10649689     EISSN: 15579786     Source Type: Journal    
DOI: 10.1016/j.mric.2011.08.014     Document Type: Review

References (108)

1. Volpe J.J. Hypoxic-ischemic encephalopathy: clinical aspects. Neurology of the newborn 2001, 331-394. WB Saunders, Philadelphia. 4th edition. J.J. Vople (Ed.).
2. Vanucci R.C., Vannucci S.J. Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev Neurosci 2005, 27(2-4):81.
3. Ferriero D.M. Neonatal brain injury. N Engl J Med 2004, 351:1985.
4. Jacobs S.H., Hunt R., Tarnow-Mordi W.O., et al. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2007, 4. CD003311.
5. Barkovich A.J. Pediatric neuroimaging 2005, Lippincott Williams andamp; Wilkins, Philadelphia. 4th edition.
6. Volpe J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009, 8:110-124.
7. Rutherford M., Malamateniou C., McGuinness A., et al. Magnetic resonance imaging in hypoxic-ischaemic encephalopathy. Early Hum Dev 2010, 86:351-360.
8. Litman R.S., Soin K., Salam A. Postoperative hypoxemia in term and preterm infants after chloral hydrate sedation. Anesth Analg 2010, 110:739-746.
9. Mellon R.D., Simone A.F., Rappaport B.A. Use of anesthetic agents in neonates and young children. Anesth Analg 2007, 104:509-520.
10. Keil B., Alagappan V., Mareyam A., et al. Size-optimized 32-channel brain arrays for 3T pediatric imaging. Magn Reson Med 2011, 10.1002/mrm.22961.
11. Barkovich A. MRI of the neonatal brain. Neuroimaging Clin N Am 2006, 16:117-135.
12. Perlman J. Summary proceedings from the neurology group on hypoxic-ischemic encephalopathy. Pediatrics 2006, 117:S28-S33.
13. Volpe J.J. Neurology of the newborn 2008, Elsevier, Philadelphia. 5th edition.
14. Calvert J., Zhang J.H. Pathophysiology of the hypoxic-ischemic insult during the perinatal period. Neurol Res 2005, 27:246-260.
15. Banasiak K.J., Xia Y., Haddad G.G. Mechanisms underlying hypoxia-induced neuronal apoptosis. Prog Neurobiol 2000, 62:215-249.
16. Grant P.E., Yu D. Acute injury to the immature brain with hypoxia with or without hypoperfusion. Radiol Clin North Am 2006, 44:63-77.
17. Yakovlev A.G., Faden A.I. Mechanisms of neural cell death: implications for development of neuroprotective treatment strategies. NeuroRx 2004, 1:5-16.
18. Kitanaka C., Kuchino Y. Caspase independent cell death with necrotic morphology. Cell Death Differ 1999, 6(6):508-515.
19. Miller S.P., Newton M., Ferriero D., et al. Predictors of 30-month outcome following perinatal depression: role of proton MRS and socioeconomic factors. Pediatr Res 2002, 52:71-77.
20. Okereafor A., Allsop J., Counsell S.J., et al. Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics 2008, 121:906-914.
21. Mercuri E., Ricci D., Cowan F.M., et al. Head growth in infants with hypoxic-ischaemic encephalopathy: correlation with neonatal magnetic resonance imaging. Pediatrics 2000, 106(2):235-243.
22. Barkovich A.J., Miller S.P., Bartha A. MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol 2006, 27:533-547.
23. Barkovich A.J. MR and CT evaluation of profound neonatal and infantile asphyxia. AJNR Am J Neuroradiol 1992, 13:959-972.
24. Rennie J.M., Hagmann C.F., Robertson N.J. Neonatal cerebral investigation 2008, Cambridge University Press, Cambridge (United Kingdom).
25. Barkovich A.J., Sargent S.K. Profound asphyxia in the premature infant: imaging findings. AJNR Am J Neuroradiol 1995, 16:1837-1846.
26. Huang B.Y., Castillo M. Hypoxic-ischemic brain injury: imaging findings from birth to adulthood. Radiographics 2008, 28:417-439.
27. Rutherford M., Srinivasan L., Dyet L., et al. Magnetic resonance imaging in perinatal brain injury: clinical presentation, lesions and outcome. Pediatr Radiol 2006, 36:582-592.
28. Ward P., Counsell S., Allsop J., et al. Reduced fractional anisotropy on diffusion tensor magnetic resonance imaging after hypoxic-ischemic encephalopathy. Pediatrics 2006, 117(4):e619-e630.
29. Bhakoo K., Pearce D. In vitro expression of N-acetyl-aspartate by oligodendrocytes: implications for proton magnetic resonance spectroscopy signal in vivo. J Neurochem 2000, 74:254-262.
30. Robertson N., Cox I.J., Cowan F., et al. Cerebral intracellular lactic alkalosis persisting months after neonatal encephalopathy measured by magnetic resonance spectroscopy. Pediatr Res 1999, 46:287-296.
31. Roelants-van Rijn A., van der Gront J., de Vries L., et al. Value of 1H-MRS using different echo times in neonates with cerebral hypoxia-ischemia. Pediatr Res 2001, 49:356-362.
32. Pu Y., Li Q.Y., Zeng C.M., et al. Increased detectability of alpha-brain glutamate/glutamine in neonatal hypoxic-ischemic encephalopathy. AJNR Am J Neuroradiol 2000, 21:203-212.
33. Arzoumanian Y., Mirmiran M., Barnes P.D., 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, 24:1646-1653.
34. Belet N., Belet U., Incesu L., et al. Hypoxic-ischemic encephalopathy: correlation of serial MRI and outcome. Pediatr Neurol 2004, 31:267-274.
35. Boichot C., Walker P.M., Durand C., et al. Term neonate prognoses after perinatal asphyxia: contributions of MR imaging, MR spectroscopy, relaxation times, and apparent diffusion coefficients. Radiology 2006, 239:839-848.
36. Chau V., Poskitt K.J., Miller S.P. Advanced neuroimaging techniques for the term newborn with encephalopathy. Pediatr Neurol 2009, 40:181-188.
37. Kuenzle C., Baenziger O., Martin E., et al. Prognostic value of early MR imaging in term infants with severe perinatal asphyxia. Neuropediatrics 1994, 25:191-200.
38. Miller S.P., Ramaswamy V., Michelson D., et al. Patterns of brain injury in term neonatal encephalopathy. J Pediatr 2005, 146:453-460.
39. Barkovich A.J., Hajnal B.L., Vigneron D., et al. Prediction of neuromotor outcome in perinatal asphyxia: evaluation of MR scoring systems. AJNR Am J Neuroradiol 1998, 19:143-149.
40. Kraanddie;geloh-Mann I., Helber A., Mader I., et al. Bilateral lesions of thalamus and basal ganglia: origin and outcome. Dev Med Child Neurol 2002, 44:477-484.
41. Himmelmann K., Hagberg G., Wiklund L.M., et al. Dyskinetic cerebral palsy: a population based study of children born between 1991 and 1998. Dev Med Child Neurol 2007, 49:246-251.
42. Hanrahan J., Cox I., Azzopardi D., et al. Relation between proton magnetic resonance spectroscopy within 18 hours of birth asphyxia and neurodevelopment at 1 year of age. Dev Med Child Neurol 1999, 41(2):76-82.
43. Robertson N.J., Cowan F.M., Cox I.J., et al. Brain alkaline intracellular pH after neonatal encephalopathy. Ann Neurol 2002, 52(6):732-742.
44. Zhu W., Zhong W., Qi J., et al. Proton magnetic resonance spectroscopy in neonates with hypoxic-ischemic injury and its prognostic value. Transl Res 2008, 152:225-232.
45. Thayyil S., Chandrasekaran M., Taylor A., et al. Cerebral magnetic resonance biomarkers for predicting neurodevelopmental outcome following neonatal encephalopathy: a meta-analysis. Pediatrics 2010, 125(2):e382-e395.
46. Rutherford M., Ramenghi L., Edwards A.D., et al. Assessment of brain tissue injury after moderate hypothermia in neonates with hypoxic-ischaemic injury: a nested substudy of a randomized controlled trial. Lancet Neurol 2010, 9:39.
47. Volpe J.J., Pasternak J.F. Parasagittal cerebral injury in neonatal hypoxic-ischaemic encephalopathy. J Pediatr 1977, 91:472-476.
48. Byrne P., Welch R., Johnson M.A., et al. Serial magnetic resonance imaging in neonatal hypoxic-ischemic encephalopathy. J Pediatr 1990, 117:694-700.
49. Barkovich A.J., Baranski K., Vigneron D., et al. Proton MR spectroscopy in the evaluation of asphyxiated term neonates. AJNR Am J Neuroradiol 1999, 20:1399-1405.
50. Volpe J.J. Hypoxic-ischemic encephalopathy. Neurology of the newborn 2001, 331. WB Saunders, Philadelphia. 4th edition. J.J. Volpe (Ed.).
51. Steinman K.J., Gorno-Tempini M.L., Glidden D.V., et al. Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 2009, 123(3):1025-1030.
52. Oguni H., Sugawa M., Osawa M. Symptomatic parieto-occipital epilepsy as sequela of perinatal asphyxia. Pediatr Neurol 2008, 38(5):345-352.
53. Twomey E., Twomey A., Ryan S., et al. MR imaging of term infants with hypoxic-ischaemic encephalopathy as a predictor of neurodevelopmental outcome and late MRI appearances. Pediatr Radiol 2010, 40(9):1526-1535.
54. de Vries L.S., Jongmans M.J. Long-term outcome after neonatal hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 2010, 95(3):F220-F224.
55. Logitharajah P., Rutherford M.A., Cowan F. Hypoxic-ischemic encephalopathy in preterm infants: antecedent factors, brain imaging and outcomes. Pediatr Res 2009, 66(2):222-229.
56. Keeney S.E., Adcock E.W., McArdle C.B. Prospective observations of 100 high-risk neonates by high-field (1.5 Tesla) magnetic resonance imaging of the central nervous system. II. Lesions associated with hypoxic-ischemic encephalopathy. Pediatrics 1991, 87(4):431-438.
57. Sie L.T., van der Knaap M.S., Oosting J., et al. MR patterns of hypoxic-ischemic brain damage after prenatal, perinatal, or postnatal asphyxia. Neuropediatrics 2000, 31(3):128-136.
58. Talos D.M., Follett P.L., Folkerth R.D., et al. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in the forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 2006, 497:61-77.
59. Hasegawa M., Houdou S., Mito T., et al. Development of myelination in the human fetal and infant cerebrum: a myelin basic protein immunohistochemical study. Brain Dev 1992, 14:1-6.
60. Dyet L.E., Kennea R., Counsell S.J., et al. Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance from birth and neurodevelopmental assessment. Pediatrics 2006, 118:536-548.
61. Nosarti C., Giouroukou E., Healy E., et al. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain 2008, 131:205-217.
62. Ment L.R., Vohr B., Allan W., et al. Change in cognitive function over time in very low-birth-weight infants. JAMA 2003, 289(6):705-711.
63. Inder T.E., Warfield S.K., Wang H., et al. Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005, 115:286-294.
64. Khwaja O., Volpe J.J. Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008, 93:F153-F161.
65. Counsell S.J., Allsop J., Harrison M., et al. Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 2003, 112:176-180.
66. Inder T.E., Andersen N.J., Spencer C., et al. White matter injury in the premature infant: a comparison between serial cranial ultrasound and MRI at term. AJNR Am J Neuroradiol 2003, 24:805-809.
67. Miller S.P., Cozzio C.C., Goldstein R.B., et al. Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am J Neuroradiol 2003, 24:1661-1669.
68. Kinney H.C., Back S.A. Human oligodendroglial development: relationship to periventricular leukomalacia. Semin Pediatr Neurol 1998, 5:180-189.
69. Perlman J.M., Risser R., Broyles R.S. Bilateral cystic periventricular leukomalacia in the premature infant: associated risk factors. Pediatrics 1996, 97:822-827.
70. Rodriguez J., Claus D., Verellen G., et al. Periventricular leukomalacia: ultrasonic and neuropathologic correlations. Dev Med Child Neurol 1990, 32:347-352.
71. Paneth N., Rudelli R., Monte W., et al. White matter necrosis in very low birth weight infants: neuropathologic and ultrasonographic findings in infants surviving six days or longer. J Pediatr 1990, 116:975-984.
72. Hope P.L., Gould S.J., Howard S., et al. Precision of ultrasound diagnosis of pathologically verified lesions in the brains of very preterm infants. Dev Med Child Neurol 1988, 30:457-471.
73. Maalouf E.F., Duggan P.J., Counsell S., et al. Comparison of findings on cranial ultrasound and magnetic resonance imaging in preterm infants. Pediatrics 2001, 107:719-727.
74. Roelants-van Rijn A.M., Groenendaal F., Beek F.J., et al. Parenchymal brain injury in the preterm infant: comparison of cranial ultrasound, MRI and neurodevelopmental outcome. Neuropediatrics 2001, 32:80-89.
75. van Mezel-Meijler G., van der Knaap M.S., Oosting J., et al. Predictive value of neonatal MRI as compared to ultrasound in premature infants with mild periventricular white matter changes. Neuropediatrics 1999, 30:231-238.
76. Childs A.M., Cornette L., Ramenghi L.A., et al. Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. Clin Radiol 2001, 56:647-655.
77. Leijser L.M., de Bruianddie;ne F.T., van der Grond J., et al. Is sequential cranial ultrasound reliable for detection of white matter injury in very preterm infants?. Neuroradiology 2010, 52(5):397-406.
78. Horsch S., Skioanddie;ld B., Hallberg B., et al. Cranial ultrasound and MRI at term age in extremely preterm infants. Arch Dis Child Fetal Neonatal Ed 2010, 95(5):F310-F314.
79. Felderhoff-Mueser U., Rutherford M.A., Squier W.V., et al. Relationship between MR imaging and histopathologic findings of the brain in extremely sick preterm infants. AJNR Am J Neuroradiol 1999, 20:1349-1357.
80. Schouman-Claeys E., Henry-Feugeas M.C., Roset F., et al. Periventricular leukomalacia: correlation between MR imaging and autopsy findings during the first 2 months of life. Radiology 1993, 189:59-64.
81. Rutherford M.A., Supramaniam V., Ederies A., et al. Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 2010, 52(6):505-521.
82. Kidokoro H., Kubota T., Ohe H., et al. Diffusion-weighted magnetic resonance imaging in infants with periventricular leukomalacia. Neuropediatrics 2008, 39:233-238.
83. Inder T.E., Huppi P.S., Warfield S.K., 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(5):755-760.
84. Domi T., deVeber G., Shroff M., et al. Corticospinal tract pre-wallerian degeneration: a novel outcome predictor for pediatric stroke on acute MRI. Stroke 2009, 40(3):780-787.
85. Skiold B., Horsch S., Hallberg B., et al. White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Paediatr 2010, 99:842-849.
86. Counsell S.J., Shen Y., Boardman J.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(2):376-386.
87. Lanzi G., Fazzi E., Uggetti C., et al. Cerebral visual impairment in periventricular leukomalacia. Neuropediatrics 1998, 29:145-150.
88. Woodward L.J., Anderson P.J., Austin N.C., et al. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 2006, 355:685-694.
89. Nosarti C., Al-Asady M.H., Frangou S., et al. Adolescents who were born very preterm have decreased brain volumes. Brain 2002, 125:1616-1623.
90. Panigrahy A., Barnes P.D., Robertson R.L., et al. Volumetric brain differences in children with periventricular T2-signal hyperintensities: a grouping by gestational age at birth. AJR Am J Roentgenol 2001, 177:695-702.
91. Melhem E.R., Hoon A.H., Ferrucci J.T., et al. Periventricular leukomalacia: relationship between lateral ventricular volume on brain MR images and severity of cognitive and motor impairment. Radiology 2000, 214:199-204.
92. Peterson B.S., Vohr B., Staib L.H., et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000, 284:1939-1947.
93. Krishnan M.L., Dyet L.E., Boardman J.P., et al. Relationship between white matter apparent diffusion coefficients in preterm infants at term-equivalent age and developmental outcome at 2 years. Pediatrics 2007, 120:e604-e609.
94. Drobyshevsky A., Bregman J., Store P., et al. Serial diffusion tensor imaging detects white matter changes that correlate with motor outcome in premature infants. Dev Neurosci 2007, 29:289-301.
95. Rose J., Mirmiran M., Butler E.E., et al. Neonatal microstructural development of the internal capsule on diffusion tensor imaging correlates with severity of gait. Dev Med Child Neurol 2007, 49:745-750.
96. Song S.K., Sun S.W., Ju W.K., et al. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003, 20:1714-1722.
97. Mathur A.M., Neil J.J., Inder T.E. Understanding brain injury and neurodevelopmental disabilities in the preterm infant: the evolving role of advanced magnetic resonance imaging. Semin Perinatol 2010, 34(1):57-66.
98. Bassi L., Ricci D., Volzone A., et al. Probabilistic diffusion tractography of the optic radiations and visual function in preterm infants at term equivalent age. Brain 2008, 131:573-582.
99. Berman J.I., Glass H.C., Miller S.P., et al. Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns. AJNR Am J Neuroradiol 2009, 30:120-124.
100. Saigal S., Doyle L.W. An overview of mortality and sequela of preterm birth from infancy to adulthood. Lancet 2008, 371(9608):261-269.
101. Scafidi J., Fagel D.M., Ment L.R., et al. Modeling premature brain injury and recovery. Int J Dev Neurosci 2009, 27(8):863-871.
102. Allin M., Henderson M., Suckling J., et al. Effects of very low birthweight on brain structure in adulthood. Dev Med Child Neurol 2004, 46(1):46-53.
103. Ment L.R., Constable R.T. Injury and recovery in the developing brain: evidence from functional MRI studies of prematurely born children. Nat Clin Pract Neurol 2007, 3:558-571.
104. Ment L.R., Peterson B.S., Vohr B., et al. Cortical recruitment patterns in children born prematurely compared with control subjects during a passive listening functional magnetic resonance imaging test. J Pediatr 2006, 149:490-498.
105. Schafer R.J., Lacadie C., Vohr B., et al. Alterations in functional connectivity for language in prematurely born adolescents. Brain 2009, 132:661-670.
106. Thompson P.M., Cannon T.D., Narr K.L., et al. Genetic influences on brain structure. Nat Neurosci 2001, 4:1253-1258.
107. Als H., Duffy F.H., McAnulty G.B., et al. Early experience alters brain function and structure. Pediatrics 2004, 113:846-857.
108. Chiang M.C., Barysheva M., Shattuck D.W., et al. Genetics of brain fiber architecture and intellectual performance. J Neurosci 2009, 29:2212-2224.