Skip to main content

Advertisement

SpringerLink
Log in

Novel applications of quantitative MRI for the fetal brain

  • Advances in Fetal and Neonatal Imaging
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

The advent of ultrafast MRI acquisitions is offering vital insights into the critical maturational events that occur throughout pregnancy. Concurrent with the ongoing enhancement of ultrafast imaging has been the development of innovative image-processing techniques that are enabling us to capture and quantify the exuberant growth, and organizational and remodeling processes that occur during fetal brain development. This paper provides an overview of the role of advanced neuroimaging techniques to study in vivo brain maturation and explores the application of a range of new quantitative imaging biomarkers that can be used clinically to monitor high-risk pregnancies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Garel C (2008) Fetal MRI: what is the future? Ultrasound Obstet Gynecol 31:123–128

    Article  PubMed  CAS  Google Scholar 

  2. Prayer D (2006) Investigation of the normal organ development with fetal MRI. Eur Radiol 17:2458–2471

    Article  Google Scholar 

  3. Limperopoulos C, Clouchoux C (2009) Advancing fetal brain MRI. Targets for the future. Semin Perinatol 33:289–298

    Article  PubMed  Google Scholar 

  4. Gholipour A, Estroff JA, Warfield SK (2010) Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imag 29:1739–1758

    Article  Google Scholar 

  5. Jiang S, Xue H, Counsell S et al (2007) In-utero three dimension high resolution fetal brain diffusion tensor imaging. Med Image Comput Comput Assist Interv 10(Pt 1):18–26

    PubMed  Google Scholar 

  6. Rousseau F, Glenn OA, Iordanova B et al (2006) Registration-based approach for reconstruction of high-resolution in utero fetal MR brain images. Acad Radiol 13:1072–1081

    Article  PubMed  Google Scholar 

  7. Malamateniou C, McGuinness AK, Allsop JM et al (2011) Snapshot inversion recovery: an optimized single-shot T1-weighted inversion-recovery sequence for improved fetal brain anatomic delineation. Radiology 258:229–235

    Article  PubMed  Google Scholar 

  8. Sandrasegaran K, Laal C, Aisen AA et al (2005) Fast fetal magnetic resonance imaging. J Comput Assist Tomogr 29:487–498

    Article  PubMed  Google Scholar 

  9. Clouchoux C, Coupé P, Manjon J et al (2010) A novel approach for high-resolution image reconstruction for in-vivo fetal brain MRI. OHBM Conference, Barcelona, Spain. Abstract

  10. Guizard N, Lepage C, Fonov V et al (2008) Development of fetus brain atlas from multi-axial MR acquisitions. In: Proceedings of the 16th Scientific Meeting, International Society for Magnetic Resonance in Medicine. May 3–9, Toronto, Canada. Abstract 672

  11. Limperopoulos C, Tworetzky W, McElhinney DB et al (2010) Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation 5:26–33

    Article  Google Scholar 

  12. Kazan-Tannus JF, Dialani V, Kataoka ML et al (2007) MR volumetry of brain and CSF in fetuses referred for ventriculomegaly. AJR 189:145–151

    Article  PubMed  Google Scholar 

  13. Grossman R, Hoffman C, Mardor Y et al (2006) Quantitative MRI measurements of human fetal brain development in utero. NeuroImage 33:463–470

    Article  PubMed  Google Scholar 

  14. Fischl B, Dale A (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050

    Article  PubMed  CAS  Google Scholar 

  15. Mangin J-F, Coulon O, Frouin V (1998) Robust brain segmentation using histogram scale-space analysis and mathematical morphology. In: Wells WM, Colchester A, Delp S (eds) Medical image computing and computer-assisted intervention—MICCAI’98. Lecture notes in computer science 1496. Springer-Verlag, Berlin, pp 1230–1241

    Google Scholar 

  16. Gholipour A, Estroff JA, Barnewolt CE et al (2010) Fetal brain volumetry through MRI volumetric reconstruction and segmentation. Int J Comput Assist Radiol Surg 6:329–339

    Article  PubMed  Google Scholar 

  17. Guizard N, Evans AC, Lepage C et al (2009) Automatic model-based fetal brain parcellation to quantify in vivo fetal brain development. OHBM Conference, San Francisco, USA. Abstract

  18. Dominique Jacob F, Habas P, Kim K et al (2011) Fetal hippocampal development: analysis by magnetic resonance imaging volumetry. Pediatr Res 69(5 Pt 1):425–429

    Article  Google Scholar 

  19. Habas P, Kim K, Corbett-Detig JM et al (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. NeuroImage 53:460–470

    Article  PubMed  Google Scholar 

  20. Limperopoulos C, Soul JS, Gauvreau K et al (2005) Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 115:688–695

    Article  PubMed  Google Scholar 

  21. Kostović I, Judas M (2002) Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267:1–6

    Article  PubMed  Google Scholar 

  22. Corbett-Detig J, Habas PA, Scott JA et al (2010) 3D global and regional patterns of human fetal subplate growth determined in utero. Brain Struct Funct 215:255–263

    Article  PubMed  Google Scholar 

  23. Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310:805–810

    Article  PubMed  CAS  Google Scholar 

  24. 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(Pt 8):2028–2041

    Article  PubMed  CAS  Google Scholar 

  25. Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1:86–93

    Article  PubMed  CAS  Google Scholar 

  26. Batchelor PG, Castellano Smith AD, Hill DL et al (2002) Measures of folding applied to the development of the human fetal brain. IEEE Trans Med Imag 21:953–965

    Article  Google Scholar 

  27. Hu H-H, Guo W-Y, Chen H-Y et al (2009) Morphological regionalization using fetal magnetic resonance images of normal developing brains. Eur J Neurosci 29:1560–1567

    Article  PubMed  Google Scholar 

  28. Clouchoux C, Kudelski D, Gholipour A et al (2011) Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Struct Funct. doi:10.1007/s00429-011-0325-x

  29. Kasprian G, Langs G, Brugger PC et al (2010) The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. Cereb Cortex 21:1076–1083

    Article  PubMed  Google Scholar 

  30. Rajagopalan V, Scott JA, Habas PA et al (2011) Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. J Neurosci 31:2878–2887

    Article  PubMed  CAS  Google Scholar 

  31. Garel C, Delezoide AL, Delezoide L et al (2004) MRI of the fetal brain: normal development and cerebral pathologies. Springer, New York

    Google Scholar 

  32. Baldoli C, Righini A, Parazzini C et al (2002) Demonstration of acute ischemic lesions in the fetal brain by diffusion magnetic resonance imaging. Ann Neurol 52:243–246

    Article  PubMed  Google Scholar 

  33. Righini A, Bianchini E, Parazzini C et al (2003) Apparent diffusion coefficient determination in normal fetal brain: a prenatal MR imaging study. AJNR 24:799–804

    PubMed  Google Scholar 

  34. Agid R, Lieberman S, Nadjari M et al (2006) Prenatal MR diffusion-weighted imaging in a fetus with hemimegalencephaly. Pediatr Radiol 36:138–140

    Article  PubMed  Google Scholar 

  35. Bui T, Daire JL, Chalard F et al (2006) Microstructural development of human brain assessed in utero by diffusion tensor imaging. Pediatr Radiol 36:1133–1140

    Article  PubMed  Google Scholar 

  36. Kim DH, Chung S, Vigneron DB et al (2008) Diffusion-weighted imaging of the fetal brain in vivo. Magn Reson Med 59:216–220

    Article  PubMed  Google Scholar 

  37. Brunel H, Girard N, Confort-Gouny S et al (2004) Fetal brain injury. J Neuroradiol 31:123–137

    Article  PubMed  CAS  Google Scholar 

  38. Schneider JF, Confort-Gouny S, Le Fur Y et al (2007) Diffusion-weighted imaging in normal fetal maturation. Eur Radiol 17:2422–2429

    Article  PubMed  CAS  Google Scholar 

  39. Schneider MM, Berman JI, Baumer FM et al (2009) Normative apparent diffusion coefficient values in the developing fetal brain. AJNR 30:1799–1803

    Article  PubMed  CAS  Google Scholar 

  40. Manganaro L, Perrone A, Savelli S et al (2007) Evaluation of normal brain development by prenatal MR imaging. Radiol Med 112:444–445

    Article  PubMed  CAS  Google Scholar 

  41. Hüppi PS, Warfield S, Kikinis R (1998) Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol 43:224–235

    Article  PubMed  Google Scholar 

  42. Neil JJ, Shiran SI, McKinstry RC et al (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotrophy measured by using diffusion tensor MR imaging. Radiology 209:57–66

    PubMed  CAS  Google Scholar 

  43. Miller S, Vigneron DB, Henry RG et al (2002) Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imag 16:621–632

    Article  Google Scholar 

  44. Berman JI, Hamrick SE, McQuillen PS et al (2011) Diffusion-weighted imaging in fetuses with severe congenital heart defects. AJNR 32:E21–E22

    Article  PubMed  CAS  Google Scholar 

  45. Sanz-Cortes M, Padilla N, Falcon C et al (2010) Assessment of brain volumetry and neurodevelopment of preterm born infants with and without IUGR at 12–18 months of age. Ultrasound Obstet Gynecol 36(S1):2

    Google Scholar 

  46. Manganaro L, Fierro F, Tomei A et al (2010) MRI and DWI: feasibility of DWI and ADC maps in the evaluation of placental changes during gestation. Prenat Diagn 30:1178–1184

    Article  PubMed  Google Scholar 

  47. Bonel HM, Stolz B, Diedrichsen L et al (2010) Diffusion-weighted MR imaging of the placenta in fetuses with placental insufficiency. Radiology 257:810–819

    Article  PubMed  Google Scholar 

  48. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267

    Article  PubMed  CAS  Google Scholar 

  49. Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. NeuroImage 22:1302–1314

    Article  PubMed  Google Scholar 

  50. Huang H, Xue R, Zhang J et al (2009) Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci 29:4263–4273

    Article  PubMed  CAS  Google Scholar 

  51. Anjari M, Srinivasan L, Allsop JM et al (2007) Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. NeuroImage 35:1021–1027

    Article  PubMed  Google Scholar 

  52. Dubois J, Dehaene-Lambertz G, Soarès C et al (2008) Microstructural correlates of infant functional development: example of the visual pathways. J Neurosci 28:1943–1948

    Article  PubMed  CAS  Google Scholar 

  53. Maas LC, Mukherjee P, Carballido-Gamio J et al (2004) Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. NeuroImage 22:1134–1140

    Article  PubMed  Google Scholar 

  54. Deipolyi AR, Mukherjee P, Gill K et al (2005) Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. NeuroImage 27:579–586

    Article  PubMed  Google Scholar 

  55. Kasprian G, Brugger PC, Weber M et al (2008) In utero tractography of fetal white matter development. NeuroImage 43:213–224

    Article  PubMed  Google Scholar 

  56. Mitter C, Kasprian G, Brugger PC et al (2011) Three-dimensional visualization of fetal white-matter pathways in utero. Ultrasound Obstet Gynecol 37:252–253

    Article  PubMed  CAS  Google Scholar 

  57. Borowska-Matwiejczuk K, Lemancewicz A, Tarasow E et al (2003) Assessment of fetal distress based on magnetic resonance examinations: preliminary report. Acad Radiol 10:1274–1282

    Article  PubMed  CAS  Google Scholar 

  58. Wolfberg AJ, Robinson JN, Mulkern R et al (2007) Identification of fetal cerebral lactate using magnetic resonance spectroscopy. Am J Obstet Gynecol 196:e9–e11

    Article  PubMed  Google Scholar 

  59. Azpurua H, Alvarado A, Mayobre F et al (2008) Metabolic assessment of the brain using proton magnetic resonance spectroscopy in a growth-restricted human fetus: case report. Am J Perinatol 25:305–309

    Article  PubMed  Google Scholar 

  60. Kok RD, van der Bergh AJ, Heerschap A et al (2001) Metabolic information from the human fetal brain obtained with proton magnetic resonance spectroscopy. Am J Obstet Gynecol 185:1011–1015

    Article  PubMed  CAS  Google Scholar 

  61. Kok RD, van der Berg PP, van der Bergh AJ et al (2002) Maturation of the human fetal brain as observed by 1H MR spectroscopy. Magn Reson Med 48:611–616

    Article  PubMed  CAS  Google Scholar 

  62. Kreis R (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

    Article  PubMed  CAS  Google Scholar 

  63. Fenton BW, Lin CS, Macedonia C et al (2001) The fetus at term: in utero volume-selected proton MR spectroscopy with breath-hold technique—a feasibility study. Radiology 219:563–566

    PubMed  CAS  Google Scholar 

  64. Limperopoulos C, Tworetzky W, Robertson RL et al (2008) Impaired brain metabolism in fetuses with congenital heart disease. Circulation 118:S651–S652

    Google Scholar 

  65. Preissl H, Lowery CL, Eswaran H (2004) Fetal magnetoencephalography: current progress and trends. Exp Neurol 190(Supp 1):S28–S36

    Article  PubMed  Google Scholar 

  66. Blum T, Saling E, Bauer R (1985) First magnetoencephalography recordings of the brain activity of a human fetus. Br J Obstet Gynaecol 92:1224

    Article  PubMed  CAS  Google Scholar 

  67. Lengel JM, Chen M, Wakai RT (2001) Improved neuromagnetic detection of fetal and neonatal auditory evoked responses. Clin Neurophysiol 112:785–792

    Article  Google Scholar 

  68. Eswaran H, Wilson JD, Preissl H et al (2002) Magnetoencephalograppic recordings of visual evoked brain activity in the human fetus. Lancet 360:779–780

    Article  PubMed  Google Scholar 

  69. Moore RJ, Vadeyar S, Tyler DJ et al (2001) Antenatal determination of fetal brain activity in response to an acoustic stimulus using functional magnetic resonance imaging. Hum Brain Mapp 12:94–99

    Article  PubMed  CAS  Google Scholar 

  70. Hykin J, Moore R, Duncan K et al (1999) Fetal brain activity demonstrated by functional magnetic resonance imaging. Lancet 35:645–646

    Article  Google Scholar 

  71. Jardri R, Pins D, Houfflin-Debarge V et al (2008) Fetal cortical activation to sound at 33 weeks of gestation: a functional MRI study. NeuroImage 42:10–18

    Article  PubMed  Google Scholar 

  72. Fulford J, Vadeyar SH, Dodampahala SH et al (2004) Fetal brain activity and hemodynamic response to a vibroacoustic stimulus. Hum Brain Mapp 22:116–121

    Article  PubMed  Google Scholar 

  73. Fulford J, Vadeyar SH, Dodampahala SH et al (2003) Fetal brain activity in response to a visual stimulus. Hum Brain Mapp 20:239–245

    Article  PubMed  Google Scholar 

  74. Sparling JW (ed) (1993) Concepts in fetal movements research. Haworth, New York

    Google Scholar 

  75. Olesen AG, Svare JA (2004) Decreased fetal movements: background, assessment, and clinical management. Acta Obstet Gynecol Scand 83:818–826

    PubMed  Google Scholar 

  76. Prechtl HF, Einspieler C (1997) Is neurological assessment of the fetus possible? Eur J Obstet Gynecol Reprod Biol 75:81–84

    Article  PubMed  CAS  Google Scholar 

  77. Hayat TT, Nihat A, Martinez-Biarge M et al (2011) Optimization and initial experience of a multislice balanced steady-state free precession cine sequence for the assessment of fetal behavior in utero. AJNR 32:331–338

    Article  PubMed  CAS  Google Scholar 

  78. Guo WY, Ono S, Oi S et al (2006) Dynamic motion analysis of fetuses with central nervous system disorders by cine magnetic resonance imaging using fast imaging employing steady-state acquisition and parallel imaging: a preliminary result. J Neurosurg 105:94–100

    PubMed  Google Scholar 

Download references

Disclaimer

The supplement this article is part of is not sponsored by the industry. Dr. Clouchoux and Dr. Limperopoulos have no financial interest, investigational or off-label uses to disclose.

Author information

Authors and Affiliations

  1. Division of Diagnostic Imaging and Radiology, Children’s National Medical Center, Washington, DC, USA

    Cédric Clouchoux & Catherine Limperopoulos

  2. McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, Canada

    Catherine Limperopoulos

  3. Department of Neurology and Neurosurgery, McGill University, Montreal, Canada

    Catherine Limperopoulos

  4. Division of Fetal and Transitional Medicine, Children’s National Medical Center, Washington, DC, USA

    Catherine Limperopoulos

Authors
  1. Cédric Clouchoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catherine Limperopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catherine Limperopoulos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clouchoux, C., Limperopoulos, C. Novel applications of quantitative MRI for the fetal brain. Pediatr Radiol 42 (Suppl 1), 24–32 (2012). https://doi.org/10.1007/s00247-011-2178-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-011-2178-0

Keywords

Search

Navigation