Elsevier

NeuroImage

Volume 36, Issue 4, 15 July 2007, Pages 1074-1085
NeuroImage

Displacement of brain regions in preterm infants with non-synostotic dolichocephaly investigated by MRI

https://doi.org/10.1016/j.neuroimage.2007.04.011Get rights and content

Abstract

Regional investigations of newborn MRI are important to understand the appearance and consequences of early brain injury. Previously, regionalization in neonates has been achieved with a Talairach parcellation, using internal landmarks of the brain. Non-synostotic dolichocephaly defines a bi-temporal narrowing of the preterm infant’s head caused by pressure on the immature skull. The impact of dolichocephaly on brain shape and regional brain shift, which may compromise the validity of the parcellation scheme, has not yet been investigated. Twenty-four preterm and 20 fullterm infants were scanned at term equivalent. Skull shapes were investigated by cephalometric measurements and population registration. Brain tissue volumes were calculated to rule out brain injury underlying skull shape differences. The position of Talairach landmarks was evaluated. Cortical structures were segmented to determine a positional shift between both groups. The preterm group displayed dolichocephalic head shapes and had similar brain volumes compared to the mesocephalic fullterm group. In preterm infants, Talairach landmarks were consistently positioned relative to each other and to the skull base, but were displaced with regard to the calvarium. The frontal and superior region was enlarged; central and temporal gyri and sulci were shifted comparing preterm and fullterm infants. We found that, in healthy preterm infants, dolichocephaly led to a shift of cortical structures, but did not influence deep brain structures. We concluded that the validity of a Talairach parcellation scheme is compromised and may lead to a miscalculation of regional brain volumes and inconsistent parcel contents when comparing infant populations with divergent head shapes.

Introduction

Head circumference and skull shape are parameters that are used to examine brain and skull development in infants (Amin et al., 1997, Gutbrod et al., 2000). As the growing brain influences the growth and expansion of the skull, arrested or delayed brain growth leads to decreased head circumference (Hack et al., 1991, Bartholomeusz et al., 2002). In this case, the head circumference represents the size of the skull as an indirect measure of brain volume and growth. Since magnetic resonance imaging (MRI) became widely available, imaging of newborns has been used to assess brain volumes directly by means of tissue segmentation (Huppi et al., 1998). Information about the volume of certain brain tissues is used to draw conclusions about delayed brain development or brain injury (Toft et al., 1995; Inder, 1999 #32; Tolsa et al., 2004; Inder, 2005 #33).

Recently, there has been increasing effort to apply parcellation schemes in connection with tissue segmentation to allow regional investigation of brain tissue volumes in newborns (Peterson et al., 2003, Sowell et al., 2003). It appears that different perinatal factors directly or indirectly affect brain development in a regional manner (Kesler et al., 2004, Limperopoulos et al., 2005). Thus, a regional investigation of the newborn brain allows such insights. To date, in the investigation of newborns and especially preterm infants, regional investigation has concentrated on the application of a parcellation scheme in which planes set along landmarks defined by Talairach and Tournoux (1988) are used to partition the brain. This scheme relays on the identification of three landmarks, the anterior and posterior commissure and the genu of the corpus callosum (Peterson et al., 2003, Mewes et al., 2006). Imaging of newborns in general suffers from low image resolution, motion artifacts and low contrast intrinsic to the developing brain. In addition, gyral landmarks, which are being used to parcellate the adult brain (Meyer et al., 1999, Fischl et al., 2004, Makris et al., 2006), evolve and change rapidly during cortical development in the newborn period and thus posing additional challenges. This makes it difficult to identify congruent brain regions in newborn subjects by cortical parcellation. In contrast, the structural formation of the corpus callosum (CC) and adjacent commissures is complete by about 20 weeks of gestation, and they appear well defined in their position and shape on newborn MRI. Thus they can be reliably identified in MRI of preterm infants as landmarks for a Talairach parcellation scheme (Rakic and Yakovlev, 1968, Silver et al., 1982, Katz et al., 1983).

After birth the configuration of the neonate’s head changes. Besides significant deviation from the norm indicating serious clinical conditions such as premature closure of the skull sutures (Huang et al., 1998) or hydrocephalus, the infants’ head in general adjusts to its new environment. External forces compress the skull transmitted from the padding the infant rests on. This procedure affects the head shape of term and preterm infants similarly, but to a different extent (Largo and Duc, 1978). The resulting shape is correlated to the head and sleep position, which lead to either parietal or occipital flattening of the head (Baum and Searls, 1971, Largo and Duc, 1978, Argenta et al., 1996). Certain secondary conditions, which are common in preterm infants, promote the effect of the external compression, such as neurological deficits or immaturity, which reduces the muscle tone to spontaneously change head position, lack of full bone mineralization and prolonged time periods in the same position (Cartlidge and Rutter, 1988, Hemingway and Oliver, 2000, Hummel and Fortado, 2005). As preterm infants are mostly positioned with their heads sideways, often in a fixed position to facilitate respiratory support (Hummel and Fortado, 2005), their heads frequently show a pronounced elongation and temporal narrowing of the head, called non-synostotic dolichocephaly (NSD) (Cartlidge and Rutter, 1988, Hemingway and Oliver, 2000). NSD is correlated to the degree of prematurity. It is more pronounced in the preterm infants born less mature and with low or very low birth weight for gestational age (Largo and Duc, 1978, Elliman et al., 1986). Although studies have investigated preterm infants head shapes and found dolichocephalic head configurations in all study infants (Elliman et al., 1986), NSD is not inevitable in preterm infants and can be avoided with special care. Water pillows (Marsden, 1980, Schwirian et al., 1986), air mattresses (Cartlidge and Rutter, 1988), frequent positional changes and special positioning techniques have been successfully tested (Hummel and Fortado, 2005), but are not part of the standard intensive care. The impact of NSD on the shape of the brain parenchyma and a possible subsequent shift of the brain tissue has not yet been investigated. In the context of a landmark-based parcellation scheme, a displacement of brain structures subsequent to NSD might introduce a systematic error and influence the reliability of the parcellation method.

In this study, we aimed to investigate whether a dolichocephalic skull shape in a group of preterm infants without brain injury led to a displacement of deep or superficial brain structures in comparison to fullterm infants with mesocephalic skulls. We first evaluated whether internal landmarks as defined by Talairach and Tournoux were consistently positioned between the preterm and fullterm study infants (Talairach and Tournoux, 1988). Second, we determined whether specific sulci and gyri were consistently positioned with respect to the deep brain landmarks of the Talairach parcellation scheme.

Section snippets

Subjects

The scans of forty-four infants born at one of three collaborating medical centers were analyzed in this study. Seven preterm and fourteen fullterm infants were inborn patients at the Royal Women’s Hospital in Melbourne, Australia; ten preterm and six fullterm infants were born at the Brigham and Women’s Hospital, Boston MA, USA; seven preterm infants were born at the Children’s Hospital, Geneva, Switzerland.

Infants enrolled in the study were appropriate for gestational age with head

Validation

Repeated measurements of two distances, the CC length and the diameter of the superior ICC, as well as two angles, the angle ε and angle δ were analyzed for the intra-observer variability. The mean coefficient of variation was 0.99% for the two distances and 3.6% for the two angles. The ratio of the distribution of repeated segmentations of the central sulcus over the central and occipital parcel was analyzed for the intra-observer variability as well. The mean coefficient of variation was 4.1%

Discussion

During infancy, the growing skull and the developing brain interact with each other and eventually achieve the adult shape and size of the head and brain. Brain injury may interfere with skull growth (Hack et al., 1991) and skull growth that diverges from its normal trajectory may lead to a dysmorphology of the brain (Aldridge et al., 2002). The preterm infants in this study demonstrated an occipito-frontal and inferior–superior elongation and a temporal narrowing of the skull together with a

Acknowledgments

This study was supported in part by NIH grants P30 HD18655, P41RR13218, R01 RR021885, R01 HD046855, R01 HD047730, R03 CA126466, R21 MH067054 and U41RR019703-01A2; by research grant RG 3478A2/2 from the NMSS; by the US Department of Education Grants H023C70032 and R305T990294, and in part by the Swiss National Foundation Grants SNF 32-56927.99 and 3200-102127, the Murdoch Children’s Research Institute, Royal Women’s Hospital (Melbourne) and the National Health and Medical Research Council of

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