Abstract
Alterations in cortical development and impaired neurodevelopmental outcomes have been described following very preterm (VPT) birth in childhood and adolescence, but only a few studies to date have investigated grey matter (GM) and white matter (WM) maturation in VPT samples in early adult life. Using voxel-based morphometry (VBM) we studied regional GM and WM volumes in 68 VPT-born individuals (mean gestational age 30 weeks) and 43 term-born controls aged 19–20 years, and their association with cognitive outcomes (Hayling Sentence Completion Test, Controlled Oral Word Association Test, Visual Reproduction test of the Wechsler Memory Scale-Revised) and gestational age. Structural MRI data were obtained with a 1.5 Tesla system and analysed using the VBM8 toolbox in SPM8 with a customized study-specific template. Similarly to results obtained at adolescent assessment, VPT young adults compared to controls demonstrated reduced GM volume in temporal, frontal, insular and occipital areas, thalamus, caudate nucleus and putamen. Increases in GM volume were noted in medial/anterior frontal gyrus. Smaller subcortical WM volume in the VPT group was observed in temporal, parietal and frontal regions, and in a cluster centred on posterior corpus callosum/thalamus/fornix. Larger subcortical WM volume was found predominantly in posterior brain regions, in areas beneath the parahippocampal and occipital gyri and in cerebellum. Gestational age was associated with GM and WM volumes in areas where VPT individuals demonstrated GM and WM volumetric alterations, especially in temporal, parietal and occipital regions. VPT participants scored lower than controls on measures of IQ, executive function and non-verbal memory. When investigating GM and WM alterations and cognitive outcome scores, subcortical WM volume in an area beneath the left inferior frontal gyrus accounted for 14% of the variance of full-scale IQ (F = 12.9, p < 0.0001). WM volume in posterior corpus callosum/thalamus/fornix and GM volume in temporal gyri bilaterally, accounted for 21% of the variance of executive function (F = 9.9, p < 0.0001) and WM in the posterior corpus callosum/thalamus/fornix alone accounted for 17% of the variance of total non-verbal memory scores (F = 9.9, p < 0.0001). These results reveal that VPT birth continues to be associated with altered structural brain anatomy in early adult life, although it remains to be ascertained whether these changes reflect neurodevelopmental delays or long lasting structural alterations due to prematurity. GM and WM alterations correlate with length of gestation and mediate cognitive outcome.
Highlights
Due to its rapidly developing and complex characteristics, the preterm brain is vulnerable to exogenous and endogenous insults in the third trimester of gestation (Volpe, 2009), during which the volume of the whole brain more than doubles and the volume of cortical grey matter (GM) increases approximately four-fold (Huppi et al, 1998)
In the very preterm (VPT)/VLBW cohort from the University Hospital in Trondheim, Norway, cortical thickness deviations seemed to be more pronounced at age 15 (Martinussen et al, 2005) compared to age 20 (Bjuland et al, 2013), and we previously reported that the surface area of the corpus callosum did not differ between VPT born individuals at age 19 compared to controls, while it was significantly smaller in the VPT group when the same sample was studied in mid-adolescence (Allin et al, 2007)
The 93 VPT individuals assessed at age 19–20 did not differ from the 302 individuals who were enrolled for follow-up in terms of gestational age (F(301) = 2.4, p N 0.05), birth weight (F(301) = 0.8, p N 0.05) and Apgar score at 1 and 5 min (F(301) = 0.005, p N 0.05 and F(301) = 0.03, p N 0.05, respectively)
Summary
Due to its rapidly developing and complex characteristics, the preterm brain is vulnerable to exogenous and endogenous insults in the third trimester of gestation (Volpe, 2009), during which the volume of the whole brain more than doubles and the volume of cortical grey matter (GM) increases approximately four-fold (Huppi et al, 1998). Nosarti et al / NeuroImage: Clinical 6 (2014) 180–191 studies in similar samples obtained consistent findings (Gimenez et al, 2006b; Nagy et al, 2009), whereas investigations on cortical morphology reported a thinner inferior frontal cortex in VPT adolescents vs controls (Frye et al, 2010) Such findings could be interpreted within a ‘neuroplastic’ framework, which posits that developmental changes in any brain region may result in a cascade of alterations in many other regions (Hack and Taylor, 2000). Despite strong evidence that neurodevelopmental anatomical alterations are present in VPT/VLBW children and adolescents, little is known about the nature and course of their brain development when they reach adulthood Both increases and decreases in GM and WM volumes have been described in VPT/VLBW young adults compared to controls, especially in internal capsule, insula, prefrontal cortex, medial temporal/parahippocampal gyrus and putamen (Allin et al, 2004). Changes in WM microstructure, as assessed by diffusion tensor imaging, have been reported in several areas including the corpus callosum, corticospinal tracts, cortical association tracts, cerebellar penducle and corona radiata (Allin et al, 2011; Eikenes et al, 2011)
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