Claire E Kelly1, Deanne K Thompson2, Sila Genc3, Jian Chen4, Joseph Ym Yang5, Chris Adamson4, Richard Beare4, Marc L Seal6, Lex W Doyle7, Jeanie Ly Cheong8, Peter J Anderson9. 1. Victorian Infant Brain Study (VIBeS), Murdoch Children's Research Institute, Melbourne, Australia; Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia. Electronic address: claire.kelly@mcri.edu.au. 2. Victorian Infant Brain Study (VIBeS), Murdoch Children's Research Institute, Melbourne, Australia; Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia; Department of Paediatrics, The University of Melbourne, Melbourne, Australia; Florey Institute of Neuroscience and Mental Health, Melbourne, Australia. 3. Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia; Cardiff University Brain Research Imaging Centre (CUBRIC), Cardiff University, Cardiff, UK. 4. Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia. 5. Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia; Department of Paediatrics, The University of Melbourne, Melbourne, Australia; Department of Neurosurgery, The Royal Children's Hospital, Melbourne, Australia; Neuroscience Research, Murdoch Children's Research Institute, Melbourne, Australia. 6. Developmental Imaging, Murdoch Children's Research Institute, Melbourne, Australia; Department of Paediatrics, The University of Melbourne, Melbourne, Australia. 7. Victorian Infant Brain Study (VIBeS), Murdoch Children's Research Institute, Melbourne, Australia; Department of Paediatrics, The University of Melbourne, Melbourne, Australia; Newborn Research, The Royal Women's Hospital, Melbourne, Australia; Department of Obstetrics and Gynaecology, The University of Melbourne, Melbourne, Australia. 8. Victorian Infant Brain Study (VIBeS), Murdoch Children's Research Institute, Melbourne, Australia; Newborn Research, The Royal Women's Hospital, Melbourne, Australia; Department of Obstetrics and Gynaecology, The University of Melbourne, Melbourne, Australia. 9. Victorian Infant Brain Study (VIBeS), Murdoch Children's Research Institute, Melbourne, Australia; Turner Institute for Brain and Mental Health, Monash University, Melbourne, Australia.
Abstract
BACKGROUND: It is well documented that infants born very preterm (VP) are at risk of brain injury and altered brain development in the neonatal period, however there is a lack of long-term, longitudinal studies on the effects of VP birth on white matter development over childhood. Most previous studies were based on voxel-averaged, non-fibre-specific diffusion magnetic resonance imaging (MRI) measures, such as fractional anisotropy. In contrast, the novel diffusion MRI analysis framework, fixel-based analysis (FBA), enables whole-brain analysis of microstructural and macrostructural properties of individual fibre populations at a sub-voxel level. We applied FBA to investigate the long-term implications of VP birth and associated perinatal risk factors on fibre development in childhood and adolescence. METHODS: Diffusion images were acquired for a cohort of VP (born <30 weeks' gestation) and full-term (FT, ≥37 weeks' gestation) children at two timepoints: mean (SD) 7.6 (0.2) years (n = 138 VP and 32 FT children) and 13.3 (0.4) years (n = 130 VP and 45 FT children). 103 VP and 21 FT children had images at both ages for longitudinal analysis. At every fixel (individual fibre population within an image voxel) across the white matter, we compared FBA metrics (fibre density (FD), cross-section (FC) and a combination of these properties (FDC)) between VP and FT groups cross-sectionally at each timepoint, and longitudinally between timepoints. We also examined associations between known perinatal risk factors and FBA metrics in the VP group. RESULTS: Compared with FT children, VP children had lower FD, FC and FDC throughout the white matter, particularly in the corpus callosum, tapetum, inferior fronto-occipital fasciculus, fornix and cingulum at ages 7 and 13 years, as well as the corticospinal tract and anterior limb of the internal capsule at age 13 years. VP children also had slower FDC development in the corpus callosum and corticospinal tract between ages 7 and 13 years compared with FT children. Within VP children, earlier gestational age at birth, lower birth weight z-score, and neonatal brain abnormalities were associated with lower FD, FC and FDC throughout the white matter at both ages. CONCLUSIONS: VP birth and concomitant perinatal risk factors are associated with fibre tract-specific alterations to axonal development in childhood and adolescence.
BACKGROUND: It is well documented that infants born very preterm (VP) are at risk of brain injury and altered brain development in the neonatal period, however there is a lack of long-term, longitudinal studies on the effects of VP birth on white matter development over childhood. Most previous studies were based on voxel-averaged, non-fibre-specific diffusion magnetic resonance imaging (MRI) measures, such as fractional anisotropy. In contrast, the novel diffusion MRI analysis framework, fixel-based analysis (FBA), enables whole-brain analysis of microstructural and macrostructural properties of individual fibre populations at a sub-voxel level. We applied FBA to investigate the long-term implications of VP birth and associated perinatal risk factors on fibre development in childhood and adolescence. METHODS: Diffusion images were acquired for a cohort of VP (born <30 weeks' gestation) and full-term (FT, ≥37 weeks' gestation) children at two timepoints: mean (SD) 7.6 (0.2) years (n = 138 VP and 32 FT children) and 13.3 (0.4) years (n = 130 VP and 45 FT children). 103 VP and 21 FT children had images at both ages for longitudinal analysis. At every fixel (individual fibre population within an image voxel) across the white matter, we compared FBA metrics (fibre density (FD), cross-section (FC) and a combination of these properties (FDC)) between VP and FT groups cross-sectionally at each timepoint, and longitudinally between timepoints. We also examined associations between known perinatal risk factors and FBA metrics in the VP group. RESULTS: Compared with FT children, VP children had lower FD, FC and FDC throughout the white matter, particularly in the corpus callosum, tapetum, inferior fronto-occipital fasciculus, fornix and cingulum at ages 7 and 13 years, as well as the corticospinal tract and anterior limb of the internal capsule at age 13 years. VP children also had slower FDC development in the corpus callosum and corticospinal tract between ages 7 and 13 years compared with FT children. Within VP children, earlier gestational age at birth, lower birth weight z-score, and neonatal brain abnormalities were associated with lower FD, FC and FDC throughout the white matter at both ages. CONCLUSIONS: VP birth and concomitant perinatal risk factors are associated with fibre tract-specific alterations to axonal development in childhood and adolescence.
Authors: Deanne K Thompson; Joseph Y M Yang; Jian Chen; Claire E Kelly; Christopher L Adamson; Bonnie Alexander; Courtney Gilchrist; Lillian G Matthews; Katherine J Lee; Rodney W Hunt; Jeanie L Y Cheong; Megan Spencer-Smith; Jeffrey J Neil; Marc L Seal; Terrie E Inder; Lex W Doyle; Peter J Anderson Journal: Neurology Date: 2021-12-22 Impact factor: 9.910
Authors: Courtney P Gilchrist; Deanne K Thompson; Claire E Kelly; Richard Beare; Christopher Adamson; Thijs Dhollander; Katherine Lee; Karli Treyvaud; Lillian G Matthews; Mary Tolcos; Jeanie L Y Cheong; Terrie E Inder; Lex W Doyle; Angela Cumberland; Peter J Anderson Journal: Biol Psychiatry Cogn Neurosci Neuroimaging Date: 2021-10-14
Authors: Aurore Menegaux; Dennis M Hedderich; Josef G Bäuml; Andrei Manoliu; Marcel Daamen; Ronja C Berg; Christine Preibisch; Claus Zimmer; Henning Boecker; Peter Bartmann; Dieter Wolke; Christian Sorg; Philipp Stämpfli Journal: Sci Rep Date: 2020-10-14 Impact factor: 4.379