Pediatric Radiology

, Volume 43, Issue 1, pp 80–85

Effect of antenatal growth on brain white matter maturation in preterm infants at term using tract-based spatial statistics

  • Virva Lepomäki
  • Jaakko Matomäki
  • Helena Lapinleimu
  • Liisa Lehtonen
  • Leena Haataja
  • Markku Komu
  • Riitta Parkkola
  • The PIPARI Study Group
Original Article

Abstract

Background

White matter maturation of infants can be studied using diffusion tensor imaging (DTI). DTI of the white matter of the infant brain provides the best available clinical measures of brain tissue organisation and integrity.

Objective

The purpose of this study was to compare white matter maturation between preterm infants born small for gestational age (SGA) and preterms with weight appropriate for gestational age (AGA) at birth.

Materials and methods

A total of 36 preterm infants were enrolled in the study (SGA, n = 9). A rater-independent method called tract-based spatial statistics (TBSS) was used to assess white matter maturation.

Results

When measured by TBSS, the AGA infants showed higher fractional anisotrophy values in several white matter tracts than the SGA infants. Areas with significant differences included anterior thalamic radiation, corticospinal tract, forceps major and minor, inferior fronto-occipital fasciculus, inferior longitudinal fasciculus, superior longitudinal fasciculus, uncinate fasciculus, and superior longitudinal fasciculus (temporal part). No significant difference was found for mean diffusivity.

Conclusion

As an objective and user-independent method, TBSS confirmed that preterm infants with impaired antenatal growth have impaired white matter maturation compared to preterm infants with normal antenatal growth. The differences were mainly detected in radiations that are myelinated first.

Keywords

Diffusion tensor imaging Tract-based spatial statistics Brain Preterm infant 

References

  1. 1.
    Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455PubMedCrossRefGoogle Scholar
  2. 2.
    Neil J, Miller J, Mukherjee P et al (2002) Diffusion tensor imaging of normal and injured developing human brain—a technical review. NMR Biomed 15:543–552PubMedCrossRefGoogle Scholar
  3. 3.
    Dubois J, Dehaene-Lambertz G, Soares C et al (2008) Microstructural correlates of infant functional development: example of the visual pathways. J Neurosci 28:1943–1948PubMedCrossRefGoogle Scholar
  4. 4.
    Mori S, Zhang JY (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539PubMedCrossRefGoogle Scholar
  5. 5.
    Mukherjee P, Miller JH, Shimony JS et al (2002) Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR 23:1445–1456PubMedGoogle Scholar
  6. 6.
    Dubois J, Dehaene-Lambertz G, Perrin M et al (2008) Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp 29:14–27PubMedCrossRefGoogle Scholar
  7. 7.
    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 35:1021–1027PubMedCrossRefGoogle Scholar
  8. 8.
    Berman JI, Mukherjee P, Partridge SC et al (2005) Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage 27:862–871PubMedCrossRefGoogle Scholar
  9. 9.
    Provenzale JM, Liang L, DeLong D et al (2007) Diffusion tensor imaging assessment of brain white matter maturation during the first postnatal year. AJR 189:476–486PubMedCrossRefGoogle Scholar
  10. 10.
    Saksena S, Husain N, Malik GK et al (2008) Comparative evaluation of the cerebral and cerebellar white matter development in pediatric age group using quantitative diffusion tensor imaging. Cerebellum 7:392–400PubMedCrossRefGoogle Scholar
  11. 11.
    Kostovic I, Judas M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127PubMedCrossRefGoogle Scholar
  12. 12.
    Ramenghi LA, Martinelli A, De Carli A et al (2011) Cerebral maturation in IUGR and appropriate for gestational age preterm babies. Reprod Sci 18:469–475PubMedCrossRefGoogle Scholar
  13. 13.
    Pierpaoli C, Jezzard P, Basser PJ et al (1996) Diffusion tensor MR imaging of the human brain. Radiology 201:637–648PubMedGoogle Scholar
  14. 14.
    Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906PubMedCrossRefGoogle Scholar
  15. 15.
    Huppi PS, Maier SE, Peled S et al (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590PubMedCrossRefGoogle Scholar
  16. 16.
    Hasegawa T, Yamada K, Morimoto M et al (2011) Development of corpus callosum in preterm infants is affected by the prematurity: in vivo assessment of diffusion tensor imaging at term-equivalent age. Pediatr Res 69:249–254PubMedCrossRefGoogle Scholar
  17. 17.
    Thompson DK, Inder TE, Faggian N et al (2011) Characterization of the corpus callosum in very preterm and full-term infants utilizing MRI. Neuroimage 55:479–490PubMedCrossRefGoogle Scholar
  18. 18.
    Rose SE, Hatziaeorgiou X, Strudwick MW et al (2008) Altered white matter diffusion anisotropy in normal and preterm infants at term-equivalent age. Magn Reson Med 60:761–767PubMedCrossRefGoogle Scholar
  19. 19.
    Bonifacio SL, Glass HC, Chau V et al (2010) Extreme premature birth is not associated with impaired development of brain microstructure. J Pediatr 157:726–732PubMedCrossRefGoogle Scholar
  20. 20.
    Huppi PS, Zimine S, Borradori-Tolsa C et al (2004) Microstructural changes in brain development in premature infants with intrauterine growth restriction (IUGR): a voxel-based analysis of diffusion tensor imaging (DTI). Pediatr Res 55:582AGoogle Scholar
  21. 21.
    Thompson DK, Warfield SK, Carlin JB et al (2007) Perinatal risk factors altering regional brain structure in the preterm infant. Brain 130:667–677PubMedCrossRefGoogle Scholar
  22. 22.
    Inder TE, Warfield SK, Wang H et al (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286–294PubMedCrossRefGoogle Scholar
  23. 23.
    Sizonenko SV, Borradori-Tolsa C, Bauthay DM et al (2006) Impact of intrauterine growth restriction and glucocorticoids on brain development: insights using advanced magnetic resonance imaging. Mol Cell Endocrinol 254–255:163–171Google Scholar
  24. 24.
    Lepomaki V, Paavilainen T, Matomaki J et al (2012) Effect of antenatal growth and prematurity on brain white matter: diffusion tensor study. Pediatr Radiol 42:692–698Google Scholar
  25. 25.
    Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219PubMedCrossRefGoogle Scholar
  26. 26.
    Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMedCrossRefGoogle Scholar
  27. 27.
    Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83–98PubMedCrossRefGoogle Scholar
  28. 28.
    Pryor J (1997) The identification and long term effects of fetal growth restriction. Br J Obstet Gynaecol 104:1116–1122PubMedCrossRefGoogle Scholar
  29. 29.
    Reiman M, Parkkola R, Johansson R et al (2009) Diffusion tensor imaging of the inferior colliculus and brainstem auditory-evoked potentials in preterm infants. Pediatr Radiol 39:804–809PubMedCrossRefGoogle Scholar
  30. 30.
    Van Kooij BJ, de Vries LS, Ball G et al (2012) Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR 33:188–194PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Virva Lepomäki
    • 1
    • 2
  • Jaakko Matomäki
    • 3
  • Helena Lapinleimu
    • 3
  • Liisa Lehtonen
    • 3
  • Leena Haataja
    • 4
  • Markku Komu
    • 1
  • Riitta Parkkola
    • 1
    • 2
    • 5
  • The PIPARI Study Group
  1. 1.Medical Imaging Centre of Southwest FinlandTurku University HospitalTurkuFinland
  2. 2.Turku PET-CentreTurku University HospitalTurkuFinland
  3. 3.Department of PediatricsTurku University Hospital and University of TurkuTurkuFinland
  4. 4.Department of Pediatric NeurologyTurku University Hospital and University of TurkuTurkuFinland
  5. 5.Department of Diagnostic RadiologyUniversity of TurkuTurkuFinland

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