Seminars in Perinatology
Volume 34, Issue 1 , Pages 3-19 , February 2010

Basic Principles and Concepts Underlying Recent Advances in Magnetic Resonance Imaging of the Developing Brain

  • Ashok Panigrahy, MD

      Affiliations

    • Corresponding Author InformationAddress reprint requests to Ashok Panigrahy, MD, Department of Radiology, Children's Hospital Los Angeles, 4650 Sunset Boulevard, Mail Stop 81, Los Angeles, CA 90027
  • ,
  • Matthew Borzage, MSc
  • ,
  • Stefan Blüml, PhD

References 

  1. Ferriero DM. Neonatal brain injury. N Engl J Med. 2004;351:1985–1995
  2. Bluml S, Friedlich P, Erberich S, et al. MR imaging of newborns by using an MR-compatible incubator with integrated radiofrequency coils: initial experience. Radiology. 2004;231:594–601
  3. Dumoulin CL, Rohling KW, Piel JE, et al. Magnetic resonance imaging compatible neonate incubator. Concepts Magn Reson. 2002;15:117–128
  4. Mathur AM, Neil JL, McKinstry RC, et al. Transport, monitoring, and successful MR imaging in unsedated neonates. Pediatr Radiol. 2008;38:260–264
  5. Forbes KPN, Pipe JG, Bird CR, et al. PROPELLER MRI: clinical testing of a novel technique for quantification and compensation of head motion. J Magn Reson Imaging. 2001;14:215–222
  6. Rutherford M, Malamateniou C, Zeka J, et al. MR imaging of the neonatal brain at 3 Tesla. Eur J Paediatr Neurol. 2004;8:281–289
  7. Gilmore JH, Zhai G, Wilber K, et al. 3 Tesla magnetic resonance imaging of the brain in newborns. Psychiatry Res. 2004;132:81–85
  8. Srinivasan L, Dutta R, Counsell SJ, 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;119:759–765
  9. Beaulieu C. The basis of anisotropic water diffusion in the nervous system––a technical review. NMR Biomed. 2002;15:435–455
  10. Le Bihan D, Mangin JF, Poupon C, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging. 2001;13:534–546
  11. Conturo TE, McKinstry RC, Akbudah E, et al. Encoding of anisotropic diffusion with tetrahedral gradients: a general mathematical diffusion formalism and experimental results. Magn Reson Med. 1996;35:399–412
  12. Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis-a technical review. NMR Biomed. 2002;15:456–467
  13. Wimberger DM, Roberts TP, Barkovich AJ, et al. Identification of “premyelination” by diffusion-weighted MRI. J Comput Assist Tomogr. 1995;19:23–33
  14. Prayer D, Barkovich AJ, Kirschner DA, et al. Visualization of nonstructural changes in early white matter development on diffusion-premyelination anisotropy. AJNR Am J Neuroradiol. 2001;22:1572–1576
  15. Shimony JS, McKinstry RC, Akbudak E, et al. Quantitative diffusion-tensor anisotropy imaging: normative human data and anatomic analysis. Radiology. 1999;12:770–784
  16. Neil JJ, Shiran SI, McKinstry RC, 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
  17. Partridge SC, Mukherjee P, Hentry RG, et al. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage. 2004;22:1302–1314
  18. Mukherjee P, Miller JH, Shimony JS, et al. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology. 2001;221:349–358
  19. Mukherjee P, Miller JH, Shimony JS, et al. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol. 2002;23:1445–1456
  20. Miller JH, Mckinstry RC, Philip JC, et al. Diffusion-tensor MR imaging of normal brain maturation: a guide to structural development and myelination. AJR Am J Roentgenol. 2003;180:851–859
  21. Mukherjee P, Mckinstry RC. Diffusion tensor imaging and tractography of human brain development. In:  Castillo M,  Mukherji SK editor. Neuroimaging Clinics of North America. Vol 16:Philadelphia, PA: WB Sauders; 2006;p. 19–43No. 1
  22. Pajevic S, Pierpaoli C. Color schemes to represent the orientation of anisotrpic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med. 1999;42:526–540
  23. Conturo TE, Lri NF, Cull TS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA. 1999;96:10422–10427
  24. Mori S, Crain BJ, Chacko VP, et al. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 1999;45:265–269
  25. Basser PJ, Pajevic S, Pierpaoli C, et al. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000;44:625–632
  26. Huppi PS, Maier SE, Peled S, et al. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res. 1998;44:584–590
  27. Barkovich AJ. Pediatric Neuroimaging. 4th ed.. Philadelphia, PA: Lippincott; 2005;
  28. Yakovlev PI, Loecours AR. The myelogenic cycles of regional maturation of the brain. In:  Minkowski A editors. Regional Development of the Brain in Early Life. Oxford, UK: Blackwell; 1967;p. 3–70
  29. Richardson EP. Myelination in the human central nervous system. In:  Haymaker W,  Adams RD editor. Histology and Histopathology of the Nervous System. Springfield, IL: Charles C. Thomas Publishers; 1982;p. 146–173
  30. Kinney HC, Brody BA, Kloman AS, et al. Sequence of central nervous system myelination in human infancy (II. Patterns of myelination in autopsied infants). J Neuropathol Exp Neurol. 1988;47:217–234
  31. Evans AC Brain Development Cooperative Group. The NIH MRI study of normal brain development. Neuroimage. 2006;30:184–202
  32. McKinstry RC; Brain Development Cooperative Group: The NIH MRI Study of Normal Brain Development. In: Proceedings from the Thirteenth Annual Meeting of the International Society for Magnetic Resonance in Medicine; 2005; Miami, FL
  33. Cheong JL, Thompson DK, Wang HX, et al. Abnormal white matter signal on MR imaging is related to abnormal tissue microstructure. AJNR Am J Neuroradiol. 2009;30:623–628
  34. Mukherjee P, Berman JI, Chung SW, et al. Diffusion tensor MR imaging and fiber tractography: theoretical underpinnings. AJNR Am J Neuroradiol. 2008;29:632–641
  35. Mukherjee P, Chung SW, Berman JI, et al. Diffusion tensor MR imaging and fiber tractography: technical considerations. AJNR Am J Neuroradiol. 2008;29:843–852
  36. Lien YH, Shapiro JI, Chan L. Effects of hypernatremia on organic brain osmoles. J Clin Invest. 1990;85:1427–1435
  37. Videen JS. Human cerebral osmolytes during chronic hyponatremia (A proton magnetic resonance spectroscopy study). [see comments] J Clin Invest. 1995;95:788–793
  38. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30:672–679
  39. Erecinska M, Silver IA. Metabolism and role of glutamate in mammalian brain. Prog Neurobiol. 1990;35:245–296
  40. Daikhin Y, Yudkoff M. Compartmentation of brain glutamate metabolism in neurons and glia. J Nutr. 2000;130(suppl 4S):1026S–1031S
  41. Kreis R. Metabolic disorders of the brain in chronic hepatic encephalopathy detected with H-1 MR spectroscopy [see comments]. Radiology. 1992;182:19–27
  42. Seymour KJ, Bluml S, Sutherling J, et al. Identification of cerebral acetone by 1H-MRS in patients with epilepsy controlled by ketogenic diet. Magma. 1999;8:33–42
  43. Ball WS, Holland SK. Perfusion imaging in the pediatric patient. Magn Reson Imaging Clin N Am. 2001;9:207–230
  44. Huisman TA, Sorensen AG. Perfusion-weighted magnetic resonance imaging of the brain: techniques and application in children. Eur Radiol. 2004;14:59–72
  45. Ostergaard L, Weisskoff RM, Chelser DA, et al. High-resolution measurement of cerebral blood flow using intravascular tracer bolus passages (Part I: mathematical approach and statistical analysis). Magn Reson Med. 1996;36:715–725
  46. Detre JA, Aslop DC. Perfusion fMRI with arterial spin labeling based perfusion imaging techniques for MRI. In:  Moonen CTW,  Bandetti PA editor. Functional MRI. Heidelberg, Germany: Springer-Verlag; 1999;p. 47–62
  47. Detre JA, Leigh JS, Williams DS, et al. Perfusion imaging. Magn Reson Med. 1992;23:37–45
  48. Calamante F, Thomas Dl, Pell GS, et al. Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb Blood Flow Metab. 1999;19:701–735
  49. Wong EC, Buxton RB, Frank LR. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn Reson Med. 1998;39:702–708
  50. Buxton RB, Frank LR, Wong EC, et al. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med. 1998;40:383–396
  51. Tanner SF, Cornette L, Ramenghi LA, et al. Cerebral perfusion in infants and neonates: preliminary results obtained using dynamic susceptibility contrast enhanced magnetic resonance imaging. Arch Dis Child Fetal Neonatal Ed. 2003;88:F525–F530
  52. Miranda MJ, Olofsson K, Sidaros K. Noninvasive measurements of regional cerebral perfusion in preterm and term neonates by magnetic resonance arterial spin labeling. Pediatr Res. 2006;60:359–363
  53. Deibler AR, Pollock JM, Kraft RA, et al. Arterial spin-labeling in routine clinical practice, part 1: technique and artifacts. AJNR Am J Neuroradiol. 2008;29:1228-1223
  54. Ogawa S, Lee TM, Kay AR, et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87:9868–9872
  55. Calderon-Arnulphi M, Alaraj A, Slavin KV. Near infrared technology in neuroscience: past, present and future. Neurol Res. 2009;31:605–614
  56. Rolfe P. In vivo near-infrared spectroscopy. Annu Rev Biomed Eng. 2000;2:715–754
  57. Cui W, Kumar C, Chance B. Experimental study of migration depth for the photons measured at sample surface. In: Proceedings of Time-Resolved Spectroscopy and Imaging of Tissues. Los Angeles, CA: SPIE; 1991;p. 180–191
  58. Hoshi Y. Functional near-infrared optical imaging: utility and limitations in human brain mapping. Psychophysiology. 2003;40:511–520
  59. Schmitz C, Locker M, Laskeret JM, et al. Instrumentation for fast functional optical tomography. Rev Sci Instrum. 2002;73:429–439
  60. D'Esposito M, Deouell LY, Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci. 2003;4:863–872
  61. Duncan A, Meek JH, Clemence M, et al. Measurement of cranial optical path length as a function of age using phase resolved near infrared spectroscopy. Pediatr Res. 1996;37:889–894
  62. Huppi PS. MR imaging and spectroscopy of brain development. Magn Reson Imaging Clin N Am. 2001;9:1–17
  63. Kinney HC, Brody BA, Kloman AS, et al. Sequence of central nervous system myelination in human infancy (II. Patterns of myelination in autopsied infants). J Neurolpathol Exp Neurol. 1988;47:217–234
  64. Dubois J, Benders M, Borradori-Tolsa C, et al. Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 2008;131:2028–2041
  65. Boardman JP, Counsell SJ, Rueckert D, et al. Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage. 2006;32:70–78
  66. Gimenez M, Miranda MJ, Born AP, et al. Accelerated cerebral white matter development in preterm infants: a voxel-based morphometry study with diffusion tensor MR imaging. Neuroimage. 2008;41:728–734
  67. Barkovich AJ, Westmark KD, Bedi HS, et al. Proton spectroscopy and diffusion imaging on the first day of life after perinatal asphyxia: preliminary report. AJNR Am J Neuroradiol. 2001;22:1786–1794
  68. Barkovich AJ, Miller SP, Bartha A, et al. MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol. 2006;27:533–547
  69. Grant PE, Yu D. Acute injury to the immature brain with hypoxia with or without hypoperfusion. Radiol Clin North Am. 2006;44:63–77
  70. Penrice J, Cady EB, Lorek A, et al. Proton magnetic resonance spectroscopy of the brain in normal and term infants and early changes after perinatal hypoxia-ischemia. Pediatr Res. 1996;40:6–14
  71. Hanrahan JD, Sargentoni J, Azzopardi D, et al. Cerebral metabolism within 18 hours of birth asphyxia: a proton magnetic resonance spectroscopy study. Pediatr Res. 1996;39:584–590
  72. Leth H, Toft PB, Peitersen B, et al. Use of brain lactate levels to predict outcome after perinatal asphyxia. Acta Paediatr. 1996;85:859–864
  73. Holshouser BA, Ashwal S, Luh GY, et al. Proton MR spectroscopy after acute central nervous system injury: outcome prediction in neonates, infants, and children. Radiology. 1997;202:487–496
  74. Groenendaal F, Veenhoven RH, van der Grond J, et al. Cerebral lactate and N-acetyl-aspertate/choline ratios in asphyxiated full term neonates demonstrated in-vivo using proton magnetic resonance spectroscopy. Pediatr Res. 1994;35:148–151
  75. Huppi PS, Posse S, Lazeyras F, et al. Magnetic resonance in preterm and term newborns: H-1 spectroscopy in developing brain. Pediatr Res. 1991;30:574–578
  76. Cheong JLY, Cady EB, Penrice J, et al. Proton MR spectroscopy in neonates with perinatal cerebral hypoxic-ischemic injury: metabolite peak-area ratios, relaxation times, and absolute concentrations. AJNR Am J Neuroradiol. 2006;27:1546–1554
  77. Moorcraft J, Bolas NM, Ives NK, et al. Spatially localized magnetic resonance spectroscopy of the brains of normal and asphyxiated newborns. Pediatrics. 1991;87:273–282
  78. Peden CJ, Cowan FM, Bryant DJ, et al. Proton MR spectroscopy of the brain in infants. J Comput Assist Tomogr. 1990;14:886–894
  79. Barkovich AJ, Baranski K, Vigneron DB, et al. Proton MR spectroscopy for the evaluation of asphyxiated term neonates. AJNR Am J Neuroradiol. 1999;20:1399–1405
  80. Vigneron DB, Barkovich AJ, Noworolski SM, et al. Three-dimensional proton MR spectroscopic imaging of premature and term neonates. AJNR Am J Neuroradiol. 2001;22:1424–1433
  81. Kreis R, Hofmann L, Kuhlmann B, et al. Brain metabolite composition during early human brain development as measured by quantitative in vivo 1H magnetic resonance spectroscopy. Magn Reson Med. 2002;48:949–958
  82. Volpe JJ. Cerebral white matter injury of the premature infant––more common than you think. Pediatrics. 2003;112:176–180
  83. Banker BQ, Larroche JC. Periventricular leukomalacia of infancy. Arch Neurol. 1962;7:386–410
  84. Leviton A, Gilles FH. An epidemiologic study of perinatal telencephalic leucoencephalopathy in an autopsy population. J Neurol Sci. 1973;18:53–66
  85. Gilles FH, Leviton A, Dooling EC. The Developing Human Brain: Growth and Epidemiologic Neuropathology. Littleton, MA: Wright-PSG; 1983;
  86. Volpe J. J Neurology of the Newborn. 4th ed.. Philadelphia, PA: WB Saunders; 2000;
  87. Wood NS, Marlow N, Costeloe K, et al. Neurologic and developmental disability after extremely preterm birth. N Engl J Med. 2000;343:378–384
  88. Kinney HC. The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol. 2006;30:81–88
  89. Back SA. Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. MRDD Res Rev. 2006;12:129–140
  90. Inder TE, Wells SJ, Mogridge NB, et al. Defining the nature of cerebral abnormalities in the premature infant: qualitative magnetic resonance imaging study. J Pediatr. 2003;143:171–179
  91. Uggetti C, Egitto ME, Fazzi E, et al. Cerebral visual impaired in periventricular leukomalacia: MR correlation. AJNR Am J Neuroradiol. 1996;17:979–985
  92. Jacobson L, Ek U, Fernell E, et al. Visual impairment in preterm children with periventricular leukomalacia––visual, cognitive, and neuropaediatric characteristics related to cerebral imaging. Dev Med Child Neurol. 1996;38:724–735
  93. Wu YW, Colford JM. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA. 2000;284:1417–1424
  94. Kinney HC, Armstrong DD. Perinatal neuropathology. In:  Graham DI,  Lantos PI editor. Greenfield's Neuropathology. London, England: Arnold; 2002;p. 557–559
  95. Kadhim H, Tabarki B, Verellen G, et al. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology. 2001;56:1278–1284
  96. Follett PL, Rosenberg PA, Volpe JJ, et al. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci. 2000;20:9235–9241
  97. Back SA, Han BE, Luo NL, et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci. 2002;22:455–463
  98. Gilles FH, Leviton A, Kerr CS. Endotoxin leucoencephalopathy in the telencephalon of the newborn kitten. J Neurol Sci. 1976;27:183–191
  99. Back SA, Gan X, Li Y, et al. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced cell death caused by glutathione depletion. J Neurosci. 1998;18:6241–6253
  100. Inder T, Anderson N, Spencer C, et al. White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR Am J Neuroradiol. 2003;24:805–809
  101. Miller S, Cozzio C, Goldstein R, 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;241:1661–1669
  102. Counsell SJ, Allsop JM, Harrison MC, 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
  103. Miller SP, Ferriero DM, Leonard C, et al. Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr. 2005;147:609–616
  104. Kreis R, Ernst T, Ross BD. Development of the human brain: in vivo quantification of metabolite and water content with proton magnetic resonance spectroscopy. Magn Reson Med. 1993;30:424–437
  105. Ernst T, Kreis RRoss BD. Absolute quantitation of water and metabolites in the human brain (I. Compartments and water). J Magn Reson. 1993;102:1–8
  106. Shu SK, Ashwal S, Hosouser BA, et al. Prognostic value of 1-H MRS in perinatal CNS insults. Pediatr Neurol. 1997;17:309–318
  107. Kinney HC, Panigrahy A, Newberger J, et al. Hypoxic-ischemic brain injury in infants with congenital heart disease dying after cardiopulmonary bypass surgery. Acta Neuropathol. 2005;110:563–578

 Supported by NIH NS063371-01A1, Radiological Society of North American and Rudi Schulte Research Institute, and NIH pediatric research loan repayment grant.

PII: S0146-0005(09)00089-5

doi: 10.1053/j.semperi.2009.10.001

Seminars in Perinatology
Volume 34, Issue 1 , Pages 3-19 , February 2010