Elsevier

NeuroImage

Volume 47, Issue 4, 1 October 2009, Pages 1148-1153
NeuroImage

Age-related grey matter changes in preterm infants: An MRI study

https://doi.org/10.1016/j.neuroimage.2009.03.072Get rights and content

Abstract

Grey matter (GM) maturation has not been previously studied in healthy preterm children. The purpose of this study was to evaluate the age dependency of GM development in 116 GM areas in preterm subjects. Sixty one preterm infants (corrected age: 13.7 ± 9.92 months, gestational age: 33.4 ± 1.9 weeks) with normal structural appearance on MRI were included in the study. Using a T1-weighted high resolution 3D spoiled gradient echo sequence, volumes of 116 GM areas were calculated after their segmentation using the Voxel Based Morphometry Toolboxes and the Individual Brain Atlas Statistical Parametric Mapping (IBASPM) software packages. Non linear regression analysis assessed age dependency of volume data for every GM area using the monoexponential function y = A  B  exp(− x/C). All supratentorial GM areas followed the monoexponential function model reasonably well. Cerebellar structures had a poor goodness of fit. Volume increase of the individual GM areas followed an inferior to superior and a posterior to anterior pattern. The putamen, thalamus, and caudate nucleus reached 99% of the final volume earlier than most cortical GM areas. The visual cortex and the postcentral and precentral cortices matured earlier than the parietal, frontal and temporal cortices. The fronto-occipital asymmetry or torque seen in adults was observed in the preterm infants; the left occipital areas reached maturation earlier than the right, while the right prefrontal and frontal areas matured earlier than the left. To conclude, GM development progresses in a region-specific manner coinciding with functional, phylogenetical and regional white matter (WM) maturation.

Introduction

Brain maturation follows a dynamic course, starting during fetal life and is a lifelong process (Dekaban, 1978, Dobbing and Sands, 1973, Kretschmann et al., 1986). Most of the progressive and regressive events (e.g. neuronal migration, synaptic reorganization, myelin deposition and cell death) that contribute to brain maturation take place during the perinatal period and the first years of life (Dobbing and Sands, 1973). Brain volume increases with age and by the age of 2 years it reaches 75% of its adult weight (Dekaban, 1978, Kretschmann et al., 1986). Development of both grey (GM) and white matter (WM) accounts for the brain volume increase. Premature birth has been associated with complicated neonatal events resulting in increased central nervous system (CNS) morbidity, and in particular periventricular leukomalacia (PVL) (Wood et al., 2000). Preterm infants, even those with an uncomplicated neonatal course, may manifest long-term neurodevelopmental deficits, including cognitive and behavioural problems (Hack et al., 2000, Marlow, 2004). Evaluation of brain development, in terms of myelination progress and GM and WM volume changes, would permit the relating of developmental outcomes to changes in specific anatomic structures. Magnetization Transfer Imaging (MTI) evaluating Magnetization Transfer Ratio (MTR) has been used to study the progress of myelination in both preterm babies with an uneventful perinatal history and those with findings of PVL (Xydis et al., 2006a, Xydis et al., 2006b). Those studies demonstrated that myelination follows a monoexponential function model. Volumetric studies evaluating GM maturation and age-related changes in full-term children included mainly subjects aged older than 2 years (Caviness et al., 1996, Giedd et al., 1999, Giedd et al., 1996, Reiss et al., 1996, Sowell et al., 2003). There are only few reports of studies assessing GM age-related changes during the first 2 years of life in full-term babies (Gilmore et al., 2007, Matsuzawa et al., 2001, Pfefferbaum et al., 1994). Using semi-automated techniques of image segmentation the researchers calculated either total cortical GM volume or GM volume of certain lobes and demonstrated that GM volume in full-term infants increases following an exponential function model (Matsuzawa et al., 2001, Pfefferbaum et al., 1994). There are no normative data regarding normal GM development in preterm babies.

Volumetric MRI studies assessing GM development have been based either on the region-of-interest (ROI) approach or more recently on modern techniques of image segmentation and automatic volume calculation (Caviness et al., 1996, Giedd et al., 1996, Matsuzawa et al., 2001, Peterson et al., 2000, Pfefferbaum et al., 1994, Reiss et al., 1996). Individual Brain Atlases using Statistical Parametric Mapping (IBASPM) is a toolbox used for brain segmentation, individual atlas generation, labelling of 116 individual GM areas and volume computation that permits objective measurements of regional brain volume (Alemán-Gómez et al., 2006). This tool has not been used previously for the quantification of maturational brain changes in infants and children.

The purpose of this study was to conduct a volumetric assessment, using IBASPM that would provide normative data on the volume of 116 individual GM areas in preterm infants and to investigate the age-related changes in total GM volume and in the 116 GM areas in particular.

Section snippets

Materials and methods

The study population consisted of 61 preterm infants (32 males, 29 females) with a mean gestational age (GA) of 33.4 ± 1.9 weeks (range 30–36 weeks), investigated at mean corrected age of 13.7 ± 9.92 months (range 0.4–49.23 months). They had all had an uncomplicated neonatal course, and had neurological evaluation during regular follow up (Amiel-Tison, 2001) and had no major neurological problem. Subjects with postnatal steroid exposure, or bronchopulmonary dysplasia and brain abnormalities on MRI

Results

Figs. 1a,b demonstrate the quality of our data and the accuracy of our registration using as example the caudate nucleus in an 8 months old subject.

Total GM volume increased asymptotically, reaching 99% of the final value at corrected age: 64.5 months (5.3 years, R2 = 0.774) (Fig. 2). All supratentorial GM areas followed the monoexponential function model reasonably as indicated by the R2 values (Table 1). Cerebellar structures had a poor goodness of fit.

Fig. 3, Fig. 4 encode with colour t(99%)

Discussion

In this study an automated method for brain segmentation and volume calculation was used in order to evaluate normal GM development in preterm infants. The main finding was an increase in total and regional GM volume in preterm babies that followed a monoexponential function model. Regional GM maturation took place in order from inferior to superior and from posterior to anterior. The basal ganglia matured earlier than the cortex while the motor, sensory and visual cortices matured before the

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