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Acute pediatric traumatic brain injury severity predicts long-term verbal memory performance through suppression by white matter integrity on diffusion tensor imaging

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Abstract

Mediation analysis was used to investigate the role of white matter integrity in the relationship between injury severity and verbal memory performance in participants with chronic pediatric traumatic brain injury (TBI). DTI tractography was used to measure fractional anisotropy (FA) within the corpus callosum, fornix, cingulum bundles, perforant pathways, and uncinate fasciculi. Injury severity was indexed using Glasgow Coma Scale (GCS) scores obtained at the time of the injury. Verbal memory was measured by performance on the long-delay free recall (LDFR) trial of the California Verbal Learning Test–Children’s version. Participants were between the ages of 10–18 and included 21 children with TBI (injured before age 9) and 19 typically-developing children (TDC). Children with TBI showed lower FA across all pathways and poorer LDFR performance relative to TDC. Within the TBI group, mediation analysis revealed neither a significant total effect of GCS on LDFR nor significant direct effects of GCS on LDFR across pathways; however, the indirect effects of GCS on LDFR through FA of the corpus callosum, left perforant pathway, and left uncinate fasciculus were significant and opposite in sign to their respective direct effects. These results suggests that the predictive validity of GCS for LDFR is initially suppressed by the substantial variance accounted for by FA, which is uncorrelated with GCS, and the predictive validity of GCS increases only when FA is considered, and the opposing path is controlled. These findings illustrate the complex associations between acute injury severity, white matter pathways, and verbal memory several years following pediatric TBI.

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Acknowledgments

We wish to express our gratitude to our participants and their family members. The study was funded by the National Institute of Health grant R21 NS065937 (‘Trauma to Developing Brain: Model Refinement and Therapeutic Intervention’; Levin, PI and Noble, PI). The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Health.

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Authors and Affiliations

  1. Department of Psychology, Brigham Young University, Provo, UT, USA

    Hannah M. Lindsey, Sanam J. Lalani, Jonathan Mietchen & Shawn D. Gale

  2. The Neuroscience Center, Brigham Young University, Provo, UT, USA

    Shawn D. Gale

  3. Department of Neurology, University of Utah, Salt Lake City, UT, USA

    Hannah M. Lindsey & Elisabeth A. Wilde

  4. Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX, USA

    Elisabeth A. Wilde, Jessica Faber, Marianne C. MacLeod, Jill V. Hunter & Harvey S. Levin

  5. Department of Neurology, Baylor College of Medicine, Houston, TX, USA

    Elisabeth A. Wilde & Harvey S. Levin

  6. Department of Radiology, Baylor College of Medicine, Houston, TX, USA

    Elisabeth A. Wilde, Jill V. Hunter & Zili D. Chu

  7. Department of Pediatric Radiology, Texas Children’s Hospital, Houston, TX, USA

    Jill V. Hunter & Zili D. Chu

  8. Department of Pediatrics, University of Arkansas for Medical Sciences and Arkansas Children’s Research Institute, Little Rock, AR, USA

    Mary E. Aitken

  9. Children’s Learning Institute and Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, TX, USA

    Linda Ewing-Cobbs

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Hannah M. Lindsey, Sanam Jivani Lalani, Jonathan Mietchen, Shawn D. Gale, Elisabeth A. Wilde, Jessica Faber, Marianne MacLeod, Jill V. Hunter, Zili D. Chu, Mary E. Aitken, Linda Ewing-Cobbs, and Harvey S. Levin declare that they have no conflict of interest.

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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

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Lindsey, H.M., Lalani, S.J., Mietchen, J. et al. Acute pediatric traumatic brain injury severity predicts long-term verbal memory performance through suppression by white matter integrity on diffusion tensor imaging. Brain Imaging and Behavior 14, 1626–1637 (2020). https://doi.org/10.1007/s11682-019-00093-9

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