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Predictive value of brain MRI at term-equivalent age in extremely preterm children on neurodevelopmental outcome at school-age

Abstract

This study’s objective was to correlate the abnormalities in brain MRIs performed at corrected-term age for minor or moderate neurocognitive disorders in children school-age born extremely premature (EPT) and without serious sequelae such as autism, cerebral palsy, mental impairment. Data were issued from a cross-sectional multicenter study (GP-Qol study, number NCT01675726). Clinical examination and psychometric assessments were performed when the children were between 7 and 10 years old during a day-long evaluation. Term-equivalent age brain MRIs on EPT were analyzed with a standardized scoring system. There were 114 children included in the study. The mean age at the time of evaluation, was 8.47 years old (± 0.70). 59% of children with at least one cognitive impairment and 53% who had a dysexecutive disorder. Only ten EPT (8.7%) presented moderate to severe white and grey matter abnormalities. These moderate to severe grey matter abnormalities were associated with at least two abnormal executive functions [OR 3.08 (95% CI 1.04–8.79), p = 0.04] and language delay [OR 3.25 (95% CI 1.03–9.80), p = 0.04]. These results remained significant in the multivariate analysis. Moderate to severe ventricular dilatation abnormalities (15%, n = 17) were associated with ideomotor dyspraxia [OR 7.49 (95% CI 1.48–35.95), p = 0.02] and remained significant in multivariate analysis [OR 11.2 (95% CI 1.45–131.4), p = 0.02]. Biparietal corrected diameters were moderate abnormal in 20% of cases (n = 23) and were associated to visuo spatial integration delay [OR 4.13 (95% CI 1.23–13.63), p = 0.02]. Cerebral MRI at term-equivalent age with scoring system analysis can provide information on long-term neuropsychological outcomes at school-age in EPTs children having no severe disability.

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References

  1. Adams-Chapman, I., Heyne, R. J., DeMauro, S. B., Duncan, A. F., Hintz, S. R., Pappas, A., Vohr, B. R., McDonald, S. A., Das, A., Newman, J. E., & Higgins, R. D. (2018). Neurodevelopmental impairment among extremely preterm infants in the neonatal research network. Pediatrics, 141(5), e20173091.

    Article  Google Scholar 

  2. Anderson, P. J., Cheong, J. L. Y., & Thompson, D. K. (2015). The predictive validity of neonatal MRI for neurodevelopmental outcome in very preterm children. Seminars in Perinatology, 39, 147–158.

    Article  Google Scholar 

  3. Anderson, P. J., Treyvaud, K., Neil, J. J., Cheong, J. L. Y., Hunt, R. W., Thompson, D. K., Lee, K. J., Doyle, L. W., & Inder, T. E. (2017). Associations of newborn brain magnetic resonance imaging with long-term neurodevelopmental impairments in very preterm children. Journal of Pediatrics, 187, 58–65.

    Article  Google Scholar 

  4. Andrés, P. (2003). Frontal cortex as the central executive of working memory: Time to revise our view. Cortex, 39, 871–895.

    Article  Google Scholar 

  5. Bartlett, D. J., Galuppi, B., Palisano, R. J., & McCoy, S. W. (2016). Consensus classifications of gross motor, manual ability, and communication function classification systems between therapists and parents of children with cerebral palsy. Developmental Medicine and Child Neurology, 58(1), 98–99.

    Article  Google Scholar 

  6. Bax, M. C. O., Flodmark, O., & Tydeman, C. (2007). Definition and classification of cerebral palsy. From syndrome toward disease. Developmental Medicine and Child Neurology, 109, 39–41.

    CAS  Article  Google Scholar 

  7. Canivez, G. L. (2014). Construct validity of the WISC-IV with a referred sample: Direct versus indirect hierarchical structures. School Psychology Quarterly, 29(1), 38–51.

    Article  Google Scholar 

  8. Dammann, O., Cesario, A., & Hallen, M. (2007). NEOBRAIN–an EU-funded project committed to protect the newborn brain. Neonatology, 92(4), 217–218.

    Article  Google Scholar 

  9. De Vries, L. S., & Volpe, J. J. (2013). Value of sequential MRI in preterm infants. Neurology, 81(24), 2062–2063.

    Article  Google Scholar 

  10. Ego, A., Prunet, C., Lebreton, E., & Zeitilin, J. (2016). Customized and non-customized French intrauterine growth curves. I—Methodology. J Gynecol Obstet Biol Reprod, 45(2), 155–64.

    CAS  Article  Google Scholar 

  11. Farooqi, A., Adamsson, M., Serenius, F., & Hägglöf, B. (2016). Executive functioning and learning skills of adolescent children born at fewer than 26 weeks of gestation. PLoS ONE, 11(3), e0151819.

    CAS  Article  Google Scholar 

  12. Gire, C., Resseguier, N., Brévaut-Malaty, V., Marret, S., Cambonie, G., Souksi-Medioni, I., Müller, J.-B., Garcia, P., Berbis, J., Tosello, B., & Auquier, P. (2018). Quality of life of extremly preterm school-age children without major handicap: A cross sectional observational study. Archives of Disease in Childhood. https://doi.org/10.1136/archdischild-2018-315046

    Article  PubMed  Google Scholar 

  13. Hadders-Algra, M., Heineman, K. R., Bos, A. F., & Middelburg, K. J. (2010). The assessment of minor neurological dysfunction in infancy using the Touwen infant neurological examination: Strengthsand limitations. Developmental Medicine and Child Neurology, 52, 87–92.

    Article  Google Scholar 

  14. Hinojosa-Rodríguez, M., Harmony, T., Carrillo-Prado, C., Van Horn, J. D., Irimia, A., Torgerson, C., & Jacokes, Z. (2017). Clinical neuroimaging in the preterm infant: Diagnosis and prognosis. NeuroImage Clin, 16, 355–368.

    Article  Google Scholar 

  15. Hintz, S. R., Vohr, B. R., Bann, C. M., Taylor, H. G., Das, A., Gustafson, K. E., Yolton, K., Watson, V. E., Lowe, J., DeAnda, M. E., Ball, M. B., Finer, N. N., Van Meurs, K. P., Shankaran, S., Pappas, A., Barnes, P. D., Bulas, D., Newman, J. E., Wilson-Costello, D. E.,...Higgins, R. D. (2018). Preterm neuroimaging and school-age cognitive outcomes. Pediatrics, 142(1), e20174058.

    Article  Google Scholar 

  16. Hutchinson, E. A., De Luca, C. R., Doyle, L. W., Roberts, G., Anderson, P. J., & Victorian Infant Collaborative Study Group. (2013). School-age outcomes of extremely preterm or extremely low birth weight children. Pediatrics, 131, 1053–1061.

    Article  Google Scholar 

  17. Inder, T. E., Wells, S. J., Mogridge, N. B., Spencer, C., & Volpe, J. J. (2003). Defining the nature of the cerebral abnormalities in the premature infant: A qualitative magnetic resonance imaging study. Journal of Pediatrics, 143, 171–179.

    Article  Google Scholar 

  18. Janvier, A., & Barrington, K. (2012). Trying to predict the future of ex-preterm infants: Who benefits from a brain MRI at term? Acta Paediatrica, 101(10), 1016–1017.

    Article  Google Scholar 

  19. Johnson, S., Strauss, V., Gilmore, C., Jaekel, J., Marlow, N., & Wolke, D. (2016). Learning disabilities among extremely preterm children without neurosensory impairment: Comorbidity, neuropsychological profiles and scholastic outcomes. Early Human Development, 103, 69–75.

    Article  Google Scholar 

  20. Kidokoro, H., Neil, J. J., & Inder, T. E. (2011). New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR Am J. Neuroradiol, 34, 2208–2214.

    Article  Google Scholar 

  21. Korkman, M., Kemp, S. L., & Kirk, U. (2001). Effects of age on neurocognitive measures of children ages 5 to 12: A cross-sectional study on 800 children from the United States. Developmental Neuropsychology, 20, 331–354.

    CAS  Article  Google Scholar 

  22. Limperopoulos, C. (2016). The vulnerable immature cerebellum. Seminars in Fetal and Neonatal Medicine, 21, 293–294.

    Article  Google Scholar 

  23. Limperopoulos, C., Bassan, H., Gauvreau, K., Robertson, R. L., Sullivan, N. R., Benson, C. B., Avery, L., Stewart, J., MD, J. S. S., Ringer, S. A., Volpe, J. J., & duPlessis, A. J. (2007). Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics, 120, 584–593.

    Article  Google Scholar 

  24. Morel, B., Bertault, P., Favrais, G., Tavernier, E., Tosello, B., Proisy, M., Xu, Y., Bloch, I., Sirinelli, D., Adamsbaum, C., Tauber, C., Saliba, E., & EPIRMEX study group. (2020). Automated brain MRI metrics in the EPIRMEX cohort of preterm newborns: Correlation with the neurodevelopmental outcome at 2 years. Diagn Interv Imaging., 10, S2211-5684(20)30270–9.

    Google Scholar 

  25. Nguyen The Tich, S., Anderson, P. J., Shimony, J. S., Hunt, R. W., Doyle, L. W., & Inder, T. E. (2009). A novel quantitative simple brain metric using MR imaging for preterm infants. AJNR American Journal of Neuroradiology, 30(1), 125–131.

    CAS  Article  Google Scholar 

  26. Nguyen, T. N., Spencer-Smith, M., Zannino, D., Burnett, A., Scratch, S. E., Pascoe, L., Ellis, R., Cheong, J., Thompson, D., Inder, T., Doyle, L. W., & Anderson, P. J. (2018). Developmental trajectory of language from 2 to 13 years in children born very preterm. Pediatrics, 141(5), e20172831.

    Article  Google Scholar 

  27. Pierrat, V., Marchand-Martin, L., Arnaud, C., Kaminski, M., Resche-Rigon, M., Lebeaux, C., Bodeau-Livinec, F., Morgan, A. S., Goffinet, F., Marret, S., & Ancel, P. Y. (2014). Neurodevelopmental outcome at 2 years for preterm children born at 22 to 34 weeks’ gestation in France in 2011: EPIPAGE-2 cohort study. BMJ, 358, j3448.

    Google Scholar 

  28. Senese, V. P., De Lucia, N., & Consonb, M. (2015). Cognitive predictors of copying and drawing from memory of the Rey-Osterrieth complex figure in 7- to 10-year-old children. The Clinical Neuropsychologist, 29, 118–132.

    Article  Google Scholar 

  29. Serenius, F., Ewald, U., Farooqi, A., Fellman, V., Hafström, M., Hellgren, K., Maršál, K., Ohlin, A., Olhager, E., Stjernqvist, K., Strömberg, B., Ådén, U., & Källén, K. (2016). Neurodevelopmental outcomes among extremely preterm infants 6.5 years after active perinatal care in Sweden. JAMA Pediatrics, 170(10), 954–963.

    Article  Google Scholar 

  30. Shepherd, E., Salam, R. A., Middleton, P., Han, S., Makrides, M., McIntyre, S., Badawi, N., & Crowther, C. A. (2018). Neonatal interventions for preventing cerebral palsy: An overview of cochrane systematic reviews. Cochrane Database Syst Review, 6, CD012409.

    Google Scholar 

  31. Spittle, A. J., Cheong, J., Doyle, L. W., Roberts, G., Lee, K. J., Lim, J., Hunt, R. W., Inder, T. E., & Anderson, P. J. (2011). Neonatal white matter abnormality predicts childhood motor impairment in very preterm children. Developmental Medicine and Child Neurology, 53, 1000–1006.

    Article  Google Scholar 

  32. Tich, S. N. T., Anderson, P. J., Hunt, R. W., Lee, K. J., Doyle, L. W., & Inder, T. E. (2011). Neurodevelopmental and perinatal correlates of simple brain metrics in very preterm infants. Archives of Pediatrics and Adolescent Medicine, 165, 216–222.

    Article  Google Scholar 

  33. Vaivre-Douret, L., Lalanne, C., Ingster-Moati, I., Boddaert, N., Cabrol, D., Dufier, J. L., Golse, B., & Falissard, B. (2011). Subtypes of developmental coordination disorder: Research on their nature and etiology. Developmental Neuropsychology, 36(5), 614–43.

    Article  Google Scholar 

  34. Volpe, J. J. (2009). Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurology, 8, 110–124.

    Article  Google Scholar 

  35. Wolke, D., Strauss, V. Y. C., Johnson, S., Gilmore, C., Marlow, N., & Jaekel, J. (2015). Universal gestational age effects on cognitive and basic mathematic processing: 2 cohorts in 2 countries. Journal of Pediatrics, 166, 1410–1416.

    Article  Google Scholar 

  36. Wood, N. S., Costeloe, K., Gibson, A. T., Hennessy, E. M., Marlow, N., Wilkinson, A. R., & EPICure Study Group. (2005). The EPICure study: associations and antecedents of neurological and developmental disability at 30 months of age following extremely preterm birth. Archives of Disease Child Fetal Neonatal Edition, 90(2), F134–F140.

    CAS  Article  Google Scholar 

  37. Woodward, L. J., Anderson, P. J., Austin, N. C., Howard, K., & Inder, T. E. (2006). Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. New England Journal of Medicine, 55(7), 685–694.

    Article  Google Scholar 

  38. Woodward, L. J., Clark, C. A. C., Pritchard, V. E., Anderson, P. J., & Inder, T. E. (2011). Neonatal white matter abnormalities predict global executive function impairment in children born very preterm. Developmental Neuropsychology, 36, 22–41.

    Article  Google Scholar 

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Acknowledgements

We are grateful for the participation of all families of preterm infants in the GPQoL study and for the cooperation of the five neonatal units participating in the study. Group Information: The GPQOL Group members. The GPQOL Study Group: MC Lemarchand, Neuropsychologist, N Mestre, Scientific Research Manager (Department of Neonatal Medicine, Rouen University Hospital, Rouen), M Rebattel, Neuropsychologist (Department of Neonatal Medicine, Nimes University Hospital, Nimes), JC Rozé, MD, PhD, C Coudronnières, Neuropsychologist (Departement of neonatal medicine, Nantes University Hospital, Nantes), G Menard, Neuropsychologist, M Pache, Neuropsychologist, C Morando, Scientific Research Manager (Department of Neonatology, North Hospital, APHM University Hospital, Marseille, France), MA Einaudi MD, PhD (UMR 7268 ADÉS, Aix-Marseille University-EFS-CNRS, Faculty of Medicine, Marseille, France).

Funding

This study was supported by the promoter APHM, University Hospital and its partners, The French Health Ministry, Grant PHRC Ref ANSM B120183-30, Ref CPP: 12.018, Ref promoter: 2012-02.

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Conception and study design (CG and AG), data collection or acquisition (AG, GS and BT), statistical analysis (NR and CG), interpretation of results (AG, GS, SC, BT and CG), drafting the manuscript work or revising it critically for important intellectual content (GS, AG, SC, NR, BT and CG) approval of final version to be published agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors).

Corresponding author

Correspondence to Barthélémy Tosello.

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Ethical approval

This study was approved by the CPP (Committee for the Protection of Persons) (18/12/2012 ref 12.018) and is registered on ClinicalTrials.gov, number NCT01675726.

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Authors declare no conflict of interest.

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The members of the GPQOL study Group are listed in acknowledgements section.

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Garbi, A., Sorin, G., Coze, S. et al. Predictive value of brain MRI at term-equivalent age in extremely preterm children on neurodevelopmental outcome at school-age. Brain Imaging and Behavior (2021). https://doi.org/10.1007/s11682-021-00559-9

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Keywords

  • Brain MRI
  • Neurodevelopmental outcome
  • Impairment
  • Extremely preterm
  • School age