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Volumetric grey matter alterations in adolescents and adults born very preterm suggest accelerated brain maturation.

ABSTRACT: Previous research investigating structural neurodevelopmental alterations in individuals who were born very preterm demonstrated a complex pattern of grey matter changes that defy straightforward summary. Here we addressed this problem by characterising volumetric brain alterations in individuals who were born very preterm from adolescence to adulthood at three hierarchically related levels - global, modular and regional. We demarcated structural components that were either particularly resilient or vulnerable to the impact of very preterm birth. We showed that individuals who were born very preterm had smaller global grey matter volume compared to controls, with subcortical and medial temporal regions being particularly affected. Conversely, frontal and lateral parieto-temporal cortices were relatively resilient to the effects of very preterm birth, possibly indicating compensatory mechanisms. Exploratory analyses supported this hypothesis by showing a stronger association between lateral parieto-temporal volume and IQ in the very preterm group compared to controls. We then related these alterations to brain maturation processes. Very preterm individuals exhibited a higher maturation index compared to controls, indicating accelerated brain maturation and this was specifically associated with younger gestational age. We discuss how the findings of accelerated maturation might be reconciled with evidence of delayed maturation at earlier stages of development.

SUBMITTER: Karolis VR

PROVIDER: S-EPMC5725310 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Volumetric grey matter alterations in adolescents and adults born very preterm suggest accelerated brain maturation.

Karolis Vyacheslav R VR Froudist-Walsh Sean S Kroll Jasmin J Brittain Philip J PJ Tseng Chieh-En Jane CJ Nam Kie-Woo KW Reinders Antje A T S AATS Murray Robin M RM Williams Steven C R SCR Thompson Paul M PM Nosarti Chiara C

NeuroImage 20170920

Previous research investigating structural neurodevelopmental alterations in individuals who were born very preterm demonstrated a complex pattern of grey matter changes that defy straightforward summary. Here we addressed this problem by characterising volumetric brain alterations in individuals who were born very preterm from adolescence to adulthood at three hierarchically related levels - global, modular and regional. We demarcated structural components that were either particularly resilien ...[more]

PMID: 28942062

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Project description:Very preterm birth is associated with altered white matter microstructure and language difficulties, which may compromise communication, social function and academic achievement, but the relationship between these two factors is unclear. The aim of this study was to explore associations between white matter microstructure and language domains of semantics, grammar and phonological awareness at 7-years of age on a whole-brain level and within the arcuate fasciculus, an important language pathway, in very preterm and term-born children. Language was assessed in 145 very preterm-born (<30?weeks' gestation and/or <1250?g birth weight) and 33 term-born children aged 7?years. Fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD), mean diffusivity (MD), axon orientation dispersion and axon density were estimated from diffusion magnetic resonance images also obtained at 7?years. The correlation between diffusion values and language was assessed using Tract-Based Spatial Statistics (TBSS). The arcuate fasciculus was delineated using constrained spherical deconvolution tractography and diffusion parameters from this tract were related to language measures using linear regression. While there was evidence for widespread associations between white matter microstructure and language, there was little evidence of differences in these associations between very preterm and term-born groups. TBSS analyses revealed that higher FA and lower AD, RD, and MD in major fibre tracts, including those subserving language, were associated with better semantic, grammar and phonological awareness performance. Higher axon density in widespread fibre tracts was also associated with better semantic performance. The tractography analyses of the arcuate fasciculus showed some evidence for associations between white matter microstructure and language outcomes. White matter microstructural organisation in widespread fibre tracts, including language-relevant pathways, was associated with language performance in whole-brain and tract-based analyses. The associations were similar for very preterm and term-born groups, despite very preterm children performing more poorly across language domains.

Project description:IntroductionThe underlying microstructural properties of white matter differences in children born very preterm (<32?weeks gestational age) can be investigated in depth using multi-shell diffusion imaging. The present study compared white matter across the whole brain using diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) metrics in children born very preterm and full-term children at six years of age. We also investigated associations between white matter microstructure with early brain injury and developmental outcomes.MethodMulti-shell diffusion imaging, T1-weighted anatomical MR images and developmental assessments were acquired in 23 children born very preterm (16 males; mean scan age: 6.57?±?0.34?years) and 24 full-term controls (10 males, mean scan age: 6.62?±?0.37?years). DTI metrics were obtained and neurite orientation dispersion index (ODI) and density index (NDI) were estimated using the NODDI diffusion model. FSL's tract-based spatial statistics were performed on traditional DTI metrics and NODDI metrics. Voxel-wise comparisons were performed to test between-group differences and within-group associations with developmental outcomes (intelligence and visual motor abilities) as well as early white matter injury and germinal matrix/intraventricular haemorrhage (GMH/IVH).ResultsIn comparison to term-born children, the children born very preterm exhibited lower fractional anisotropy (FA) across many white matter regions as well as higher mean diffusivity (MD), radial diffusivity (RD), and ODI. Within-group analyses of the children born very preterm revealed associations between higher FA and NDI with higher IQ and VMI. Lower ODI was found within the corona radiata in those with a history of white matter injury. Within the full-term group, associations were found between higher NDI and ODI with lower IQ.ConclusionChildren born very preterm exhibit lower FA and higher ODI than full-term children. NODDI metrics provide more biologically specific information beyond DTI metrics as well as additional information of the impact of prematurity and white matter microstructure on cognitive outcomes at six years of age.

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Volumetric grey matter alterations in adolescents and adults born very preterm suggest accelerated brain maturation.

Publications

Volumetric grey matter alterations in adolescents and adults born very preterm suggest accelerated brain maturation.

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