Microstructural brain development between 30 and 40 weeks corrected age in a longitudinal cohort of extremely preterm infants☆
Introduction
During the second half of gestation, the human brain undergoes major growth and development. In recent years, MRI, and more recently diffusion tensor imaging (DTI), has become an important tool to evaluate microstructural changes in vivo in preterm infants (Tournier et al., 2011).
DTI has shown significant changes in white matter tracts in the second trimester in post-mortem fetuses and large changes in fractional anisotropy (FA) and mean diffusivity (MD) values between 29 weeks and term age (Aeby et al., 2012, Berman et al., 2005, Huang et al., 2009, Huppi et al., 1998), which suggests an ongoing maturation of the brain. This maturational process continues after term equivalent age, with an ongoing organization of axons and myelination of tracts until childhood and adulthood (Lebel et al., 2008, Miller et al., 2003a).
In particular the FA measure has often been used to quantify brain maturation. It has been extensively shown that FA values in the posterior limb of the internal capsule (PLIC) are positively related to increasing gestational age (Bonifacio et al., 2010, Huppi et al., 1998, Neil et al., 1998). This FA increase with a simultaneous MD decrease is thought to be due to a combination of factors related to brain development, including a decrease in water content of the brain, greater cohesiveness and compactness of the fiber tracts, reduced extra-axonal space and an increase in myelination, restricting water diffusion perpendicular to the axons (Beaulieu, 2002).
Several methods have been applied to quantify diffusivity measures, of which the manual drawing of regions of interest (ROI), tractography and tract based spatial statistics (TBSS) are most commonly used (for a review, see (Deprez et al., 2013)). To avoid the subjective nature of manual ROI-based measurements and to provide the opportunity to study the entire brain within a manageable time frame, an automated, atlas based approach can be used. Because of the rapid development of the neonatal brain, adult brain atlases are not suitable for implementation in this population. Recently, Oishi and colleagues published a neonatal brain atlas for DTI, where they identified 122 brain regions according to the Talairach atlas (Oishi et al., 2011, Talairach and Tournoux, 1988).
The aim of our study was to gain more information about maturational changes of the preterm brain, by computing the main diffusivity measures (i.e., FA, MD, and also the radial (RD) and axial (AD) diffusivities) at 30 and 40 weeks and the change in these measures during this period in a unique group of longitudinally scanned, preterm born infants without brain injury and with a normal neurodevelopmental outcome at 15 months.
Section snippets
Clinical data
From a cohort of extremely preterm infants with a gestational age below 28 weeks, consecutively admitted to the neonatal intensive care unit of the Wilhelmina Children's Hospital between June 2008 and June 2011, all 59 infants with serial MR imaging and available outcome data at 15 months were selected for initial inclusion. According to the clinical protocol, these infants are scanned around 30 weeks gestational age, if clinically stable, and again at term equivalent age with DTI as part of the
Results
Clinical characteristics of the infants are shown in Table 1.
For each brain region, the average FA value of the 40 infants is shown at 30 and 40 weeks in Figs. 1 A and B, respectively. Fig. 2, Fig. 3, Fig. 4 show the equivalent maps for the MD, AD and RD, respectively.
Fig. 5 depicts the change in the average FA values across the 40 infants between the two scans. In 70 brain regions, a significant FA increase and in 14 brain regions, a significant FA decrease was seen between the first and the
Discussion
In this study, the longitudinal change of FA, MD, AD and RD in the preterm brain over the period of 30 to 40 weeks postmenstrual age has been analyzed for infants with a normal neurodevelopmental outcome at 15 months corrected age. FA changed significantly in 84 out of 122 atlas-based brain regions, with the largest increase in the central brain regions, up to 76% in a period of 10 weeks. In contrast, cortical brain regions showed a small decrease in FA. For the other diffusivity measures a
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This study includes infants participating in the Neobrain study (LSHM-CT-2006-036534), and infants from a study funded by the Wilhelmina Research Fund (OZF2008-19). The research of A.L. is supported by VIDI Grant 639.072.411 from the Netherlands Organisation for Scientific Research (NWO).