Brain microstructural antecedents of visual difficulties in infants born very preterm

Rahul Chandwani, Karen Harpster, Julia E Kline, Ved Mehta, Hui Wang, Stephanie L Merhar, Terry L Schwartz, Nehal A Parikh, Rahul Chandwani, Karen Harpster, Julia E Kline, Ved Mehta, Hui Wang, Stephanie L Merhar, Terry L Schwartz, Nehal A Parikh

Abstract

Infants born very preterm (VPT) are at risk of later visual problems. Although neonatal screening can identify ophthalmologic abnormalities, subtle perinatal brain injury and/or delayed brain maturation may be significant contributors to complex visual-behavioral problems. Our aim was to assess the micro and macrostructural antecedents of early visual-behavioral difficulties in VPT infants by using diffusion MRI (dMRI) at term-equivalent age. We prospectively recruited a cohort of 262 VPT infants (≤32 weeks gestational age [GA]) from five neonatal intensive care units. We obtained structural and diffusion MRI at term-equivalent age and administered the Preverbal Visual Assessment (PreViAs) questionnaire to parents at 3-4 months corrected age. We used constrained spherical deconvolution to reconstruct nine white matter tracts of the visual pathways with high reliability and performed fixel-based analysis to derive fiber density (FD), fiber-bundle cross-section (FC), and combined fiber density and cross-section (FDC). In multiple logistic regression analyses, we related these tract metrics to visual-behavioral function. Of 262 infants, 191 had both high-quality dMRI and completed PreViAs, constituting the final cohort: mean (SD) GA was 29.3 (2.4) weeks, 90 (47.1%) were males, and postmenstrual age (PMA) at MRI was 42.8 (1.3) weeks. FD and FC of several tracts were altered in infants with (N = 59) versus those without retinopathy of prematurity (N = 132). FDC of the left posterior thalamic radiations (PTR), left inferior longitudinal fasciculus (ILF), right superior longitudinal fasciculus (SLF), and left inferior fronto-occipital fasciculus (IFOF) were significantly associated with visual attention scores, prior to adjusting for confounders. After adjustment for PMA at MRI, GA, severe retinopathy of prematurity, and total brain volume, FDC of the left PTR, left ILF, and left IFOF remained significantly associated with visual attention. Early visual-behavioral difficulties in VPT infants are preceded by micro and macrostructural abnormalities in several major visual pathways at term-equivalent age.

Keywords: Cerebral visual impairment; Diffusion MRI; Neonatology; Very preterm; White matter.

Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
Single tissue constrained spherical deconvolution (CSD) fixel template and whole brain tractograph displayed in MRtrix3. (A) Coronal view of the CSD fixel template demonstrating the fiber orientation distribution (fOD) for all brain voxels (B) Axial view of the same fixel template as in A with a region of interest placed in the right corona radiata. (C) Magnified view of the fOD voxels from the region of interest highlighted in B. (D-F) Whole-brain tractograph produced from the fOD template to segment and generate all white matter tracts in coronal, axial, and sagittal orientations, respectively. Color indicates fiber trajectory: green (anterior to posterior), red (left to right), and blue/purple (superior to inferior) fibers. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Segmented White Matter Tracts of the Visual Pathways in Sagittal and Axial Orientations. A&B) posterior thalamic radiations; C&D) inferior longitudinal fasciculus; E&F) inferior fronto-occipital fasciculus; G&H) splenium of the corpus callosum; I&J) superior longitudinal fasciculus. Color indicates fiber trajectory: green (anterior to posterior), red (left to right), and blue/purple (superior to inferior) fibers. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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