Preterm birth alters the development of cortical microstructure and morphology at term-equivalent age
Ralica Dimitrova,
Maximilian Pietsch,
Judit Ciarrusta,
Sean P. Fitzgibbon,
Logan Z.J. Williams,
Daan Christiaens,
Lucilio Cordero-Grande,
Dafnis Batalle,
Antonios Makropoulos,
Andreas Schuh,
Anthony N. Price,
Jana Hutter,
Rui PAG Teixeira,
Emer Hughes,
Andrew Chew,
Shona Falconer,
Olivia Carney,
Alexia Egloff,
J-Donald Tournier,
Grainne McAlonan,
Mary A. Rutherford,
Serena J. Counsell,
Emma C. Robinson,
Joseph V. Hajnal,
Daniel Rueckert,
A. David Edwards,
Jonathan O'Muircheartaigh
Affiliations
Ralica Dimitrova
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom
Maximilian Pietsch
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Judit Ciarrusta
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom
Sean P. Fitzgibbon
Centre for Functional MRI of the Brain (FMRIB), Welcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
Logan Z.J. Williams
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Daan Christiaens
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Department of Electrical Engineering, ESAT/PSI, KU Leuven, Belgium
Lucilio Cordero-Grande
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Biomedical Image Technologies, ETSI Telecomunicación, Universidad Politécnica de Madrid and CIBER-BBN, Madrid, Spain
Dafnis Batalle
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom
Antonios Makropoulos
Biomedical Image Analysis Group, Department of Computing, Imperial College London, London, United Kingdom
Andreas Schuh
Biomedical Image Analysis Group, Department of Computing, Imperial College London, London, United Kingdom
Anthony N. Price
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Jana Hutter
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Rui PAG Teixeira
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Emer Hughes
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Andrew Chew
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Shona Falconer
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Olivia Carney
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Alexia Egloff
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
J-Donald Tournier
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Grainne McAlonan
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom; MRC Centre for Neurodevelopmental Disorders, King's College London, London, United Kingdom; South London and Maudsley NHS Foundation Trust, London, United Kingdom
Mary A. Rutherford
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Serena J. Counsell
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Emma C. Robinson
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Joseph V. Hajnal
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom
Daniel Rueckert
Biomedical Image Analysis Group, Department of Computing, Imperial College London, London, United Kingdom; Faculty of Informatics and Medicine, Klinikum rechts der Isar, Technical University of Munich, Munich, Germany
A. David Edwards
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; MRC Centre for Neurodevelopmental Disorders, King's College London, London, United Kingdom
Jonathan O'Muircheartaigh
Centre for the Developing Brain, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom; Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom; MRC Centre for Neurodevelopmental Disorders, King's College London, London, United Kingdom; Corresponding author.
Introduction: The dynamic nature and complexity of the cellular events that take place during the last trimester of pregnancy make the developing cortex particularly vulnerable to perturbations. Abrupt interruption to normal gestation can lead to significant deviations to many of these processes, resulting in atypical trajectory of cortical maturation in preterm birth survivors. Methods: We sought to first map typical cortical micro- and macrostructure development using invivo MRI in a large sample of healthy term-born infants scanned after birth (n = 259). Then we offer a comprehensive characterization of the cortical consequences of preterm birth in 76 preterm infants scanned at term-equivalent age (37–44 weeks postmenstrual age). We describe the group-average atypicality, the heterogeneity across individual preterm infants, and relate individual deviations from normative development to age at birth and neurodevelopment at 18 months. Results: In the term-born neonatal brain, we observed heterogeneous and regionally specific associations between age at scan and measures of cortical morphology and microstructure, including rapid surface expansion, greater cortical thickness, lower cortical anisotropy and higher neurite orientation dispersion. By term-equivalent age, preterm infants had on average increased cortical tissue water content and reduced neurite density index in the posterior parts of the cortex, and greater cortical thickness anteriorly compared to term-born infants. While individual preterm infants were more likely to show extreme deviations (over 3.1 standard deviations) from normative cortical maturation compared to term-born infants, these extreme deviations were highly variable and showed very little spatial overlap between individuals. Measures of regional cortical development were associated with age at birth, but not with neurodevelopment at 18 months. Conclusion: We showed that preterm birth alters cortical micro- and macrostructural maturation near the time of full-term birth. Deviations from normative development were highly variable between individual preterm infants.
