Automatic quantification of normal cortical folding patterns from fetal brain MRI
Open accessAbstract
We automatically quantify patterns of normal cortical folding in the developing fetus from in utero MR images (N=80) over a wide gestational age (GA) range (21.7 to 38.9weeks). This work on data from healthy subjects represents a first step towards characterising abnormal folding that may be related to pathology, facilitating earlier diagnosis and intervention. The cortical boundary was delineated by automatically segmenting the brain MR image into a number of key structures. This utilised a spatio-temporal atlas as tissue priors in an expectation-maximization approach with second order Markov random field (MRF) regularization to improve the accuracy of the cortical boundary estimate. An implicit high resolution surface was then used to compute cortical folding measures. We validated the automated segmentations with manual delineations and the average surface discrepancy was of the order of 1mm. Eight curvature-based folding measures were computed for each fetal cortex and used to give summary shape descriptors. These were strongly correlated with GA (R(2)=0.99) confirming the close link between neurological development and cortical convolution. This allowed an age-dependent non-linear model to be accurately fitted to the folding measures. The model supports visual observations that, after a slow initial start, cortical folding increases rapidly between 25 and 30weeks and subsequently slows near birth. The model allows the accurate prediction of fetal age from an observed folding measure with a smaller error where growth is fastest. We also analysed regional patterns in folding by parcellating each fetal cortex using a nine-region anatomical atlas and found that Gompertz models fitted the change in lobar regions. Regional differences in growth rate were detected, with the parietal and posterior temporal lobes exhibiting the fastest growth, while the cingulate, frontal and medial temporal lobes developed more slowly.
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Cites
Image quality assessment: from error visibility to structural similarity
Wang, Z., Bovik, A. C., Sheikh, H. R., & Simoncelli, E. P. (2004) · IEEE Transactions on Image Processing · doi:10.1109/tip.2003.819861 · Cited by 57,892 · see citing works
Fast robust automated brain extraction
Smith, S. M. (2002) · Human Brain Mapping · doi:10.1002/hbm.10062 · Cited by 10,496 · see citing works
Marching cubes: A high resolution 3D surface construction algorithm
Lorensen, W. E., & Cline, H. E. (1987) · ACM SIGGRAPH Conference (SIGGRAPH) · doi:10.1145/37401.37422 · Cited by 10,143 · see citing works
N4ITK: Improved N3 Bias Correction
Tustison, N. J., Avants, B., Cook, P. A., Zheng, Y., Egan, A., Yushkevich, P. A., & Gee, J. C. (2010) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2010.2046908 · Cited by 6,119 · see citing works
Nonrigid registration using free-form deformations: application to breast mr images
Rueckert, D., Sonoda, L. I., Hayes, C., Hill, D. L. G., Leach, M. O., & Hawkes, D. J. (1999) · IEEE Transactions on Medical Imaging · doi:10.1109/42.796284 · Cited by 5,265 · see citing works
Self-citationDevelopment and Evolution of the Human Neocortex
Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2011) · Cell · doi:10.1016/j.cell.2011.06.030 · Cited by 1,342 · see citing works
Automated model-based tissue classification of MR images of the brain
Van Leemput, K., Maes, F., Vandermeulen, D., & Suetens, P. (1999) · IEEE Transactions on Medical Imaging · doi:10.1109/42.811270 · Cited by 1,024 · see citing works
Laird, A. K. (1964) · British Journal of Cancer · doi:10.1038/bjc.1964.55 · Cited by 880 · see citing works
BEaST: Brain extraction based on nonlocal segmentation technique
Eskildsen, S. F., Pierrick Coupé, A., Fonov, V., Manjón, J. V., Leung, K. K., Guizard, N., Wassef, S. N., Østergaard, L. R., & Collins, D. L. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.012 · Cited by 475 · see citing works
Reconstruction of fetal brain MRI with intensity matching and complete outlier removal
Deprez, M., Quaghebeur, G., Rutherford, M., Hajnal, J. V., & Schnabel, J. A. (2012) · Medical Image Analysis · doi:10.1016/j.media.2012.07.004 · Cited by 428 · see citing works
Self-citationWilde, J. P. D., Rivers, A. W., & Price, D. L. (2004) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2004.08.010 · Cited by 351 · see citing works
Gholipour, A., Estroff, J. A., & Warfield, S. K. (2010) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2010.2051680 · Cited by 351 · see citing works
Johnson, S. J., Hennessy, E., Smith, R., Trikic, R., Dieter Wolke, C., & Marlow, N. (2009) · Archives of Disease in Childhood Fetal & Neonatal · doi:10.1136/adc.2008.152793 · Cited by 345 · see citing works
A dynamic 4D probabilistic atlas of the developing brain
Deprez, M., Aljabar, P., Srinivasan, L., Counsell, S. J., Doria, V., Serag, A., Gousias, I. S., Boardman, J. P., Rutherford, M., Edwards, A. D., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.10.019 · Cited by 287 · see citing works
Self-citationFetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging.
Garel, C., Chantrel, E., Brisse, H. J., Elmaleh, M., Luton, D., Oury, J., Sebag, G. H., & Hassan, M. (2001) · PubMed Central · Cited by 286 · see citing works
Early Folding Patterns and Asymmetries of the Normal Human Brain Detected from in Utero MRI
Habas, P. A., Scott, J. A., Roosta, A., Rajagopalan, V., Kim, K., Rousseau, F., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr053 · Cited by 256 · see citing works
Characterizing white matter with magnetization transfer andT2
Stanisz, G. J., Kecojević, A., Bronskill, M. J., & Henkelman, R. M. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199912)42:6 · Cited by 249 · see citing works
Medical Image Computing and Computer-Assisted Intervention – MICCAI 2010
(2010) · Lecture notes in computer science · doi:10.1007/978-3-642-15705-9 · Cited by 246 · see citing works
Registration-Based Approach for Reconstruction of High-Resolution In Utero Fetal MR Brain Images
Rousseau, F., Glenn, O. A., Iordanova, B. E., Rodriguez-Carranza, C. E., Vigneron, D. B., Barkovich, A. J., & Studholme, C. (2006) · Academic Radiology · doi:10.1016/j.acra.2006.05.003 · Cited by 240 · see citing works
Gousias, I. S., Edwards, A. D., Rutherford, M., Counsell, S. J., Hajnal, J. V., Rueckert, D., & Hammers, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.05.083 · Cited by 219 · see citing works
Self-citationAutomatic segmentation and reconstruction of the cortex from neonatal MRI
Xue, H., Srinivasan, L., Jiang, S., Rutherford, M., Edwards, A. D., Rueckert, D., & Hajnal, J. V. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.030 · Cited by 204 · see citing works
Self-citationJiang, S., Xue, H., Glover, A., Rutherford, M., Rueckert, D., & Hajnal, J. V. (2007) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2007.895456 · Cited by 200 · see citing works
Self-citationIntersection Based Motion Correction of Multislice MRI for 3-D in Utero Fetal Brain Image Formation
Kim, K., Habas, P. A., Rousseau, F., Glenn, O. A., Barkovich, A. J., & Studholme, C. (2009) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2009.2030679 · Cited by 171 · see citing works
Local Tissue Growth Patterns Underlying Normal Fetal Human Brain Gyrification QuantifiedIn Utero
Rajagopalan, V., Scott, J. A., Habas, P. A., Kim, K., Corbett-Detig, J., Rousseau, F., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5458-10.2011 · Cited by 166 · see citing works
Fetal MRI: techniques and protocols
Prayer, D., Brugger, P., & Prayer, L. M. (2004) · Pediatric Radiology · doi:10.1007/s00247-004-1246-0 · Cited by 163 · see citing works
Prenatal US and MR Imaging Findings of Lissencephaly: Review of Fetal Cerebral Sulcal Development
Ghai, S., Fong, K. W., Toi, A., Chitayat, D. A., Pantazi, S., & Blaser, S. E. (2006) · Radiographics · doi:10.1148/rg.262055059 · Cited by 126 · see citing works
Egaña‐Ugrinovic, G., Cortés, M. S., Figueras, F., Bargalló, N., & Gratacós, E. (2013) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2013.04.008 · Cited by 121 · see citing works
Scott, J. A., Habas, P. A., Kim, K., Rajagopalan, V., Hamzelou, K. S., Corbett‐Detig, J. M., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.04.001 · Cited by 119 · see citing works
Hand, J. W., Li, Y., & Hajnal, J. V. (2010) · Physics in Medicine and Biology · doi:10.1088/0031-9155/55/4/001 · Cited by 114 · see citing works
Self-citationHabas, P. A., Kim, K., Rousseau, F., Glenn, O. A., Barkovich, A. J., & Studholme, C. (2010) · Human Brain Mapping · doi:10.1002/hbm.20935 · Cited by 92 · see citing works
Gholipour, A., Akhondi‐Asl, A., Estroff, J. A., & Warfield, S. K. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.128 · Cited by 83 · see citing works
On Super-Resolution for Fetal Brain MRI
Rousseau, F., Kim, K., Studholme, C., Koob, M., & Dietemann, J. (2010) · Lecture notes in computer science · doi:10.1007/978-3-642-15745-5_44 · Cited by 72 · see citing works
Cortical Overgrowth in Fetuses With Isolated Ventriculomegaly
Kyriakopoulou, V., Vatansever, D., Elkommos, S., Dawson, S., McGuinness, A., Allsop, J. R., Molnár, Z., Hajnal, J. V., & Rutherford, M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht062 · Cited by 70 · see citing works
Self-citationA framework for in vivo quantification of regional brain folding in premature neonates
Rodriguez-Carranza, C. E., Mukherjee, P., Vigneron, D. B., Barkovich, J., & Studholme, C. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.01.008 · Cited by 56 · see citing works
Segmentation of Brain MRI in Young Children
Murgasova, M., Dyet, L., Edwards, A., Rutherford, M., Hajnal, J., & Rueckert, D. (2007) · International Conference on Medical Image Computing and Computer-Assisted Intervention · doi:10.1016/j.acra.2007.07.020 · Cited by 53 · see citing works
Self-citationVolumetric and surface-based 3D MRI analyses of fetal isolated mild ventriculomegaly
Scott, J. A., Habas, P. A., Rajagopalan, V., Kim, K., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0418-1 · Cited by 51 · see citing works
Hosny, I. A., & Elghawabi, H. S. (2010) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2010.06.024 · Cited by 51 · see citing works
Curvature and Bending Energy in Digitized 2D and 3D Images
Verbeek, P. W., & van Vliet, L. J. (1993) · Research Repository (Delft University of Technology) · Cited by 51 · see citing works
Voxel-based surface area estimation: from theory to practice
Windreich, G., Kiryati, N., & Lohmann, G. (2003) · Pattern Recognition · doi:10.1016/s0031-3203(03)00173-0 · Cited by 46 · see citing works
Fetal Hippocampal Development: Analysis by Magnetic Resonance Imaging Volumetry
Jacob, F. D., Habas, P. A., Kim, K., Corbett-Detig, J., Xu, D., Studholme, C., & Glenn, O. A. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e318211dd7f · Cited by 44 · see citing works
Rieger, B., Timmermans, F. J., van Vliet, L. J., et al. (2004) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/tpami.2004.50 · Cited by 43 · see citing works
IEEE International Symposium on Biomedical Imaging (ISBI)
(2015) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2015.2398792 · Cited by 36 · see citing works
Fetal Magnetic Resonance Imaging at 3.0 T
Welsh, R. C., Nemec, U., & Thomason, M. E. (2011) · Topics in Magnetic Resonance Imaging · doi:10.1097/rmr.0b013e318267f932 · Cited by 27 · see citing works
Glastonbury, C. M., & Kennedy, A. (2002) · Australasian Radiology · doi:10.1046/j.1440-1673.2001.00990.x · Cited by 22 · see citing works
Segmentation of the cortex in fetal MRI using a topological model
Caldairou, B., Passat, N., Habas, P. A., Studholme, C., Koob, M., Dietemann, J., & Rousseau, F. (2011) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi.2011.5872814 · Cited by 15 · see citing works
Research on gompertz curve model used for mobile user growth
Tao, J. (2010) · International Conference on Educational and Network Technology (ICENT) · doi:10.1109/icent.2010.5532100 · Cited by 11 · see citing works
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Moeskops, P., Viergever, M. A., Mendrik, A. M., de Vries, L. S., Benders, M. J. N. L., & Isgum, I. (2016) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2016.2548501 · Cited by 861 · see citing works
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Paredes, M. F., James, D., Gil-Perotin, S., Kim, H., Cotter, J. A., Ng, C., Sandoval, K., Rowitch, D. H., Xu, D., McQuillen, P. S., et al. (2016) · Science · doi:10.1126/science.aaf7073 · Cited by 391 · see citing works
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Wheelock, M. D., Hect, J. L., Hernandez-Andrade, E., Hassan, S. S., Romero, R., Eggebrecht, A. T., & Thomason, M. E. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100632 · Cited by 126 · see citing works
Wu, Y., De Asis-Cruz, J., & Limperopoulos, C. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02449-0 · Cited by 124 · see citing works
Lefèvre, J., Germanaud, D., Dubois, J., Rousseau, F., de Macedo Santos, I., Angleys, H., Mangin, J.-F., Hüppi, P. S., Girard, N., & De Guio, F. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv123 · Cited by 102 · see citing works
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- Authors
- Wright, R., Kyriakopoulou, V., Ledig, C., Rutherford, M. A., Hajnal, J. V., Rueckert, D., & Aljabar, P.
- Affiliations
- Imperial College London (GB)
- St Thomas' Hospital (GB)
- Corresponding author
- Wright, R.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2014-05
- Volume
- 91
- Pages
- 21-32
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1987353801
- Cited by
- 134
- References
- 47
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 9 · 2023: 11 · 2022: 10 · 2021: 20 · 2020: 12 · 2019: 14 · 2018: 11 · 2017: 10 · 2016: 12 · 2015: 12 · 2014: 2
- FWCI
- 10.72
- Type
- journal article
- Language
- en
- Open access
- green
- kclpure.kcl.ac.uk
- Licence
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (publishedVersion, other-oa)
- Funders
- National Institute for Health Research (NIHR) Biomedical Research Centre at Guy's and St Thomas' NHS Foundation Trust and King's College London
- Topics
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- fetal brain MRI, gestational age estimation, Gompertz model, cortical parcellation, fetal brain development
- MeSH terms
- Adult, Algorithms, Atlases as Topic, Cerebral Cortex, Data Interpretation, Statistical, Female, Fetus, Gestational Age, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Pregnancy, Reproducibility of Results, Linear Models
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