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Diffuse excessive high signal intensity in low-risk preterm infants at term-equivalent age does not predict outcome at 1 year: a prospective study

Abstract

Introduction

The outcome of premature infants with only diffuse excessive high signal intensity (DEHSI) is not clear. We explored the relationship between DEHSI, white matter (WM) diffusion characteristics, perinatal characteristics, and neurobehavioral outcome at 1 year in a homogenous group of preterm infants without major brain abnormalities.

Methods

Fifty-eight preterm infants, gestational age 29 ± 2.6 weeks, underwent an MRI at term-equivalent age (TEA). Griffiths Mental Developmental Scales, neurological assessment, and Parental Stress Index (PSI) were performed at 1 year corrected age. These measures were compared between preterm infants according to DEHSI classification (none, mild, moderate). Diffusion tensor imaging was used in major WM volumes of interest to objectively measure the degree of WM maturation.

Results

No significant differences were detected in the perinatal risk characteristics, neurobehavioral outcome, and PSI at 1 year between infants with different DEHSI classifications. In infants with DEHSI, increased axial and radial diffusivities were detected in the optic radiations, centrum semiovale, and posterior limb of the internal capsule, indicating less advanced maturation of the WM. Significant correlations were detected between the time interval from birth to MRI and the WM microstructure in infants without DEHSI.

Conclusion

DEHSI in premature infants is neither a predictive measure for short-term adverse neurobehavioral outcome nor related to perinatal risk characteristics. Extrauterine exposure time had a differential effect on WM maturational trajectories in infants with DEHSI compared to those without. We suggest DEHSI may represent an alteration in WM maturational characteristics. Further follow-up studies may verify later consequences of DEHSI in premature infants.

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References

  1. Anderson P, Doyle LW (2003) Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA 289(24):3264–3272

    PubMed  Article  Google Scholar 

  2. Potharst ES, van Wassenaer AG, Houtzager BA, van Hus JW, Last BF, Kok JH (2011) High incidence of multi-domain disabilities in very preterm children at five years of age. J Pediatr 159(1):79–85

    PubMed  Article  Google Scholar 

  3. Bassan H, Limperopoulos C, Visconti K, Mayer DL, Feldman HA, Avery L, Benson CB, Stewart J, Ringer SA, Soul JS, Volpe JJ, du Plessis AJ (2007) Neurodevelopmental outcome in survivors of periventricular hemorrhagic infarction. Pediatrics 120(4):785–792

    PubMed  Article  Google Scholar 

  4. Mathur A, Inder T (2009) Magnetic resonance imaging—insights into brain injury and outcomes in premature infants. J Commun Disord 42(4):248–255

    PubMed Central  PubMed  Article  Google Scholar 

  5. Mathur AM, Neil JJ, Inder TE (2010) Understanding brain injury and neurodevelopmental disabilities in the preterm infant: the evolving role of advanced magnetic resonance imaging. Semin Perinatol 34(1):57–66

    PubMed Central  PubMed  Article  Google Scholar 

  6. Rutherford MA, Supramaniam V, Ederies A, Chew A, Bassi L, Groppo M, Anjari M, Counsell S, Ramenghi LA (2010) Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 52(6):505–521

    PubMed  Article  Google Scholar 

  7. Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, Duggan PJ, Harrison M, Allsop JM, Hajnal J, Herlihy AH, Edwards B, Laroche S, Cowan FM, Rutherford MA, Edwards AD (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118(2):536–548

    PubMed  Article  Google Scholar 

  8. Domizio S, Barbante E, Puglielli C, Clementini E, Domizio R, Sabatino GM, Albanese A, Colosimo C, Sabatino G (2005) Excessively high magnetic resonance signal in preterm infants and neuropsychobehavioural follow-up at 2 years. Int J Immunopathol Pharmacol 18(2):365–375

    CAS  PubMed  Google Scholar 

  9. Hart A, Whitby E, Wilkinson S, Alladi S, Paley M, Smith M (2011) Neuro-developmental outcome at 18 months in premature infants with diffuse excessive high signal intensity on MR imaging of the brain. Pediatr Radiol 41(10):1284–1292

    PubMed  Article  Google Scholar 

  10. Jeon TY, Kim JH, Yoo SY, Eo H, Kwon JY, Lee J, Lee M, Chang YS, Park WS (2012) Neurodevelopmental outcomes in preterm infants: comparison of infants with and without diffuse excessive high signal intensity on MR images at near-term-equivalent age. Radiology 263(2):518–26

    PubMed  Article  Google Scholar 

  11. Kidokoro H, Anderson PJ, Doyle LW, Neil JJ, Inder TE (2011) High signal intensity on T2-weighted MR imaging at term-equivalent age in preterm infants does not predict 2-year neurodevelopmental outcomes. AJNR Am J Neuroradiol 32(11):2005–10

    CAS  PubMed  Article  Google Scholar 

  12. de Bruine FT, van den Berg-Huysmans AA, Leijser LM, Rijken M, Steggerda SJ, van der Grond J, van Wezel-Meijler G (2011) Clinical implications of MR imaging findings in the white matter in very preterm infants: a 2-year follow-up study. Radiology 261(3):899–906

    PubMed  Article  Google Scholar 

  13. Pandit AS, Ball G, Edwards AD, Counsell SJ (2013) Diffusion magnetic resonance imaging in preterm brain injury. Neuroradiology 55(Suppl 2):65–95

    PubMed  Article  Google Scholar 

  14. Parikh NA, He L, Bonfante-Mejia E, Hochhauser L, Wilder PE, Burson K, Kaur S (2013) Automatically quantified diffuse excessive high signal intensity on MRI predicts cognitive development in preterm infants. Pediatr Neurol 49(6):424–430

    PubMed  Article  Google Scholar 

  15. Cheong JL, Thompson DK, Wang HX, Hunt RW, Anderson PJ, Inder TE, Doyle LW (2009) Abnormal white matter signal on MR imaging is related to abnormal tissue microstructure. AJNR Am J Neuroradiol 30(3):623–628

    CAS  PubMed  Article  Google Scholar 

  16. Counsell SJ, Allsop JM, Harrison MC, Larkman DJ, Kennea NL, Kapellou O, Cowan FM, Hajnal JV, Edwards AD, Rutherford MA (2003) Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 112(1 Pt 1):1–7

    PubMed  Article  Google Scholar 

  17. Counsell SJ, Shen Y, Boardman JP, Larkman DJ, Kapellou O, Ward P, Allsop JM, Cowan FM, Hajnal JV, Edwards AD, Rutherford MA (2006) Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 117(2):376–386

    PubMed  Article  Google Scholar 

  18. Skiold B, Horsch S, Hallberg B, Engstrom M, Nagy Z, Mosskin M, Blennow M, Aden U (2010) White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Paediatr 99(6):842–849

    PubMed  Article  Google Scholar 

  19. Weinstein M, Ben Bashat D, Gross-Tsur V, Leitner Y, Berger I, Marom R, Geva R, Uliel S, Ben-Sira L (2014) Isolated mild white matter signal changes in preterm infants: a regional approach for comparison of cranial ultrasound and MRI findings. J Perinatol. doi:10.1038/jp.2014.33

    PubMed  Google Scholar 

  20. Volpe JJ (2000) Intracranial hemorrhage. In: Volpe JJ (ed) Neurology of the newborn. WB Saunders Company, Philadelphia, pp 428–493

    Google Scholar 

  21. Mathur AM, Neil JJ, McKinstry RC, Inder TE (2008) Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol 38(3):260–264

    PubMed  Article  Google Scholar 

  22. Judas M, Rados M, Jovanov-Milosevic N, Hrabac P, Stern-Padovan R, Kostovic I (2005) Structural, immunocytochemical, and MR imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. AJNR Am J Neuroradiol 26(10):2671–2684

    PubMed  Google Scholar 

  23. Kostovic I, Judas M, Rados M, Hrabac P (2002) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12(5):536–544

    PubMed  Article  Google Scholar 

  24. Oishi K, Mori S, Donohue PK, Ernst T, Anderson L, Buchthal S, Faria A, Jiang H, Li X, Miller MI, van Zijl PC, Chang L (2011) Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage 56(1):8–20

    PubMed Central  PubMed  Article  Google Scholar 

  25. Griffiths R (1984) The abilities of young children. A comprehensive system of measurement for the first eight years of life. Bucks: Association for Research in Infant and Child Development. The Test Agency, Thames

    Google Scholar 

  26. Loyd BH, Abidin RR (1985) Revision of the Parenting Stress Index. J Pediatr Psychol 10(2):169–177

    CAS  PubMed  Article  Google Scholar 

  27. Schappin R, Wijnroks L, Uniken Venema MM, Jongmans MJ (2013) Rethinking stress in parents of preterm infants: a meta-analysis. PLoS ONE 8(2):e54992

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  28. Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 355(7):685–694

    CAS  PubMed  Article  Google Scholar 

  29. Sansavini A, Savini S, Guarini A, Broccoli S, Alessandroni R, Faldella G (2011) The effect of gestational age on developmental outcomes: a longitudinal study in the first 2 years of life. Child Care Health Dev 37(1):26–36

    CAS  PubMed  Article  Google Scholar 

  30. Mukherjee P, Miller JH, Shimony JS, Conturo TE, Lee BC, Almli CR, McKinstry RC (2001) Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology 221(2):349–358

    CAS  PubMed  Article  Google Scholar 

  31. Dubois J, Dehaene-Lambertz G, Perrin M, Mangin JF, Cointepas Y, Duchesnay E, Le Bihan D, Hertz-Pannier L (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(1):14–27

    PubMed  Article  Google Scholar 

  32. Gimenez M, Miranda MJ, Born AP, Nagy Z, Rostrup E, Jernigan TL (2008) Accelerated cerebral white matter development in preterm infants: a voxel-based morphometry study with diffusion tensor MR imaging. Neuroimage 41(3):728–734

    PubMed  Article  Google Scholar 

  33. Groppo M, Ricci D, Bassi L, Merchant N, Doria V, Arichi T, Allsop JM, Ramenghi L, Fox MJ, Cowan FM, Counsell SJ, Edwards AD (2012) Development of the optic radiations and visual function after premature birth. Cortex

  34. Iwata S, Nakamura T, Hizume E, Kihara H, Takashima S, Matsuishi T, Iwata O (2012) Qualitative brain MRI at term and cognitive outcomes at 9 years after very preterm birth. Pediatrics 129(5):e1138–1147

    PubMed  Article  Google Scholar 

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Ethical standards and patient consent

We declare that all human and animal studies have been approved by the Institutional Review Board of the Ministry of Health and the Hospital Ethics Committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all participants gave informed consent prior to inclusion in this study.

Conflict of interest

We declare that we have no conflict of interest.

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Correspondence to Yael Leitner.

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Yael Leitner and Maya Weinstein contributed equally to this work.

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Leitner, Y., Weinstein, M., Myers, V. et al. Diffuse excessive high signal intensity in low-risk preterm infants at term-equivalent age does not predict outcome at 1 year: a prospective study. Neuroradiology 56, 669–678 (2014). https://doi.org/10.1007/s00234-014-1373-8

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  • DOI: https://doi.org/10.1007/s00234-014-1373-8

Keywords

  • Prematurity
  • DEHSI
  • MRI
  • Developmental outcome
  • DTI