Quantitative Folding Pattern Analysis of Early Primary Sulci in Human Fetuses with Brain Abnormalities

Abstract

Background and Purpose Aberrant gyral folding is a key feature in the diagnosis of many cerebral malformations. However, in fetal life it is particularly challenging to confidently diagnose aberrant folding due to the rapid spatiotemporal changes of gyral development. Currently, there is no resource to measure how an individual fetal brain compares to normal spatiotemporal variations. In this study we assess the potential for automatic analysis of early sulcal patterns to detect individual fetal brains with cerebral abnormalities. Materials and Methods Triplane MR images were aligned to create a motion-corrected volume for each individual fetal brain and cortical plate surfaces were extracted. Sulcal basins were automatically identified on the cortical plate surface and compared with a combined set generated from 9 normal fetal brain templates. Sulcal pattern similarities to the templates were quantified using multivariate geometric features and inter-sulcal relationships for 14 normal fetal brains and 5 fetal brains proven abnormal on postnatal MRI. Results were compared to gyrifixation index. Results Significantly reduced sulcal pattern similarities to normal templates were found in all abnormal individual fetuses compared to normal fetuses (mean similarity [normal, abnormal], left: 0.818, 0.752; P < .001, right: 0.810, 0.753; P < .01). Altered location and depth patterns of sulcal basins were the primary distinguishing features. Gyrification index was not significantly different between the normal and abnormal groups. Conclusion Automated analysis of interrelated patterning of early primary sulci could outperform traditional gyrification index and has the potential to quantitatively detect individual fetuses with emerging abnormal sulcal patterns.

Disorganized Patterns of Sulcal Position in Fetal Brains with Agenesis of Corpus Callosum

“…The 3D inner cortical plate surface was then reconstructed using the isosurface function with the isovalue of 0.5 from the Matlab software ( Fig. 1) (Im et al 2017). Although small folds of the similar size with a voxel might be eliminated, our smoothing was necessary and effective to avoid noise and voxelized representation of the brain surface.…”

“…A minimum bounding box for a given surface model was created, and an average 3D relative position (x: left-right [0-1], y: posterior-anterior [0-1], z: inferior-superior [0-1]) was calculated for each sulcal basin. We also computed the normalized surface area (s) and mean sulcal depth (d) of sulcal basins to capture their geometry (Im et al 2017).…”

“…2). For each fetus, the patterns of sulcal similarity to the normal templates ranged from 0 to 1, reflecting the deviation from the normal sulcal pattern (Im et al 2013(Im et al , 2016(Im et al , 2017. However, sulcal basins on the cingulate cortical area were excluded from the SI measurement because the cortical plate surfaces from several ACC cases showed anatomically meaningless folding on the medial area due to the absence of corpus callosum and associated absence of the cingulate gyrus.…”

“…Another study showed atypical global sulcal patterns in parieto-temporal and occipito-temporal cortical regions in children with developmental dyslexia (Im et al 2016) where decreased fractional anisotropy in diffusion tensor MR imaging suggests altered white matter organization (Rimrodt et al 2010;Vandermosten et al 2012). Recently, atypical early sulcal pattern was revealed in human fetuses with brain abnormalities using this method (Im et al 2017). To our knowledge, cortical folding patterns associated with ACC have not been previously measured.…”

Quantitative MRI Analyses of Regional Brain Growth in Living Fetuses with Down Syndrome

“…One of its advantages over sonography is that post-acquisition quantitative analyses can be performed, such as volumetric and cerebral surface-based analyses Studholme 2015). Analysis of fetal brain MRIs has successfully detected subtle developmental aberrations in regional structural growth and cerebral sulcal development in fetuses with brain malformations such as cerebral ventriculomegaly (Biegon and Hoffmann 2014;Benkarim et al 2018), polymicrogyria (Im et al 2017), and agenesis of corpus callosum (Tarui et al 2018). One of its advantages over fetopsy is that MRI can be applied safely to living fetuses also allows a study of inter-individual variations at various time points during development.…”