Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth

Lucy Vanes; Sunniva Fenn-Moltu; Laila Hadaya; Sean P. Fitzgibbon; Lucilio Cordero-Grande; Anthony Price; Andrew Chew; Shona Falconer; Tomoki Arichi; Serena Counsell; Jo Hajnal; Dafnis Batalle; David Edwards; Chiara Nosarti

doi:https://doi.org/10.1016/j.dcn.2023.101250

Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth

Lucy Vanes, Sunniva Fenn-Moltu, Laila Hadaya, Sean P. Fitzgibbon, Lucilio Cordero-Grande, Anthony Price, Andrew Chew, Shona Falconer, Tomoki Arichi, Serena Counsell, Jo Hajnal, Dafnis Batalle, David Edwards, Chiara Nosarti

University of Oxford

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Abstract

Preterm birth results in premature exposure of the brain to the extrauterine environment during a critical period of neurodevelopment. Consequently, infants born preterm are at a heightened risk of adverse behavioural outcomes in later life. We characterise longitudinal development of neonatal regional brain volume and functional connectivity in the first weeks following preterm birth, sociodemographic factors, and their respective relationships to psychomotor outcomes and psychopathology in toddlerhood. We study 121 infants born preterm who underwent magnetic resonance imaging shortly after birth, at term-equivalent age, or both. Longitudinal regional brain volume and functional connectivity were modelled as a function of psychopathology and psychomotor outcomes at 18 months. Better psychomotor functioning in toddlerhood was associated with greater relative right cerebellar volume and a more rapid decrease over time of sensorimotor degree centrality in the neonatal period. In contrast, increased 18-month psychopathology was associated with a more rapid decrease in relative regional subcortical volume. Furthermore, while socio-economic deprivation was related to both psychopathology and psychomotor outcomes, cognitively stimulating parenting predicted psychopathology only. Our study highlights the importance of longitudinal imaging to better predict toddler outcomes following preterm birth, as well as disparate environmental influences on separable facets of behavioural development in this population.

Original language	English
Article number	101250
Journal	Developmental Cognitive Neuroscience
Volume	61
Early online date	5 May 2023
DOIs	https://doi.org/10.1016/j.dcn.2023.101250
Publication status	Published - Jun 2023

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Longitudinal neonatal brain_VANES_2023_GOLD VoR (CC BY)Final published version, 2.17 MBLicence: CC BY

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Vanes, L., Fenn-Moltu, S., Hadaya, L., Fitzgibbon, S. P., Cordero-Grande, L., Price, A., Chew, A., Falconer, S., Arichi, T., Counsell, S., Hajnal, J., Batalle, D., Edwards, D., & Nosarti, C. (2023). Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth. Developmental Cognitive Neuroscience, 61, Article 101250. https://doi.org/10.1016/j.dcn.2023.101250

@article{d2cfefd08f684a469a13a9721e50c581,

title = "Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth",

abstract = "Preterm birth results in premature exposure of the brain to the extrauterine environment during a critical period of neurodevelopment. Consequently, infants born preterm are at a heightened risk of adverse behavioural outcomes in later life. We characterise longitudinal development of neonatal regional brain volume and functional connectivity in the first weeks following preterm birth, sociodemographic factors, and their respective relationships to psychomotor outcomes and psychopathology in toddlerhood. We study 121 infants born preterm who underwent magnetic resonance imaging shortly after birth, at term-equivalent age, or both. Longitudinal regional brain volume and functional connectivity were modelled as a function of psychopathology and psychomotor outcomes at 18 months. Better psychomotor functioning in toddlerhood was associated with greater relative right cerebellar volume and a more rapid decrease over time of sensorimotor degree centrality in the neonatal period. In contrast, increased 18-month psychopathology was associated with a more rapid decrease in relative regional subcortical volume. Furthermore, while socio-economic deprivation was related to both psychopathology and psychomotor outcomes, cognitively stimulating parenting predicted psychopathology only. Our study highlights the importance of longitudinal imaging to better predict toddler outcomes following preterm birth, as well as disparate environmental influences on separable facets of behavioural development in this population.",

author = "Lucy Vanes and Sunniva Fenn-Moltu and Laila Hadaya and Fitzgibbon, {Sean P.} and Lucilio Cordero-Grande and Anthony Price and Andrew Chew and Shona Falconer and Tomoki Arichi and Serena Counsell and Jo Hajnal and Dafnis Batalle and David Edwards and Chiara Nosarti",

note = "Funding Information: This work was supported by the European Research Council under the European Union's Seventh Framework Programme (FP7/20072013)/ERC grant agreement no. 319456 (dHCP project). The authors acknowledge infrastructure support from the National Institute for Health Research ( NIHR ) Mental Health Biomedical Research Centre ( BRC ) at South London, Maudsley NHS Foundation Trust and Institute of Psychiatry, Psychology and Neuroscience, King's College London and the NIHR-BRC at Guys and St Thomas{\textquoteright} Hospitals NHS Foundation Trust (GSTFT). The authors also acknowledge support in part from the Wellcome Engineering and Physical Sciences Research Council ( EPSRC ) Centre for Medical Engineering at Kings College London [ WT 203148/Z/16/Z ], and the Department of Health through an NIHR Comprehensive Biomedical Research Centre Award (to Guy{\textquoteright}s and St. Thomas{\textquoteright} National Health Service (NHS) Foundation Trust in partnership with King{\textquoteright}s College London and King{\textquoteright}s College Hospital NHS Foundation Trust). LDV is supported by a King{\textquoteright}s Prize Fellowship [Wellcome Trust Institutional Strategic Support Fund; 204823/Z/16/Z ] and the Medical Research Council [ MR/S026460/1 ]. SFM is supported by a grant from the UK Medical Research Council [ MR/N013700/1 ]. L.C-G. acknowledges funding from Spanish MICINN PID2021-129022OA-I00 and CAM-Spain under the line support for R&D projects for Beatriz Galindo researchers , and Project PID2021–129022OA-I00 funded by MCIN / AEI / 10.13039/501100011033 / FEDER , EU . TA and ADE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King{\textquoteright}s College London [ MR/N026063/1 ]. TA is supported by a MRC Clinician Scientist Fellowship [ MR/P008712/1 ] and Transition Support Award [ MR/V036874/1 ]. DB received support from a Wellcome Trust Seed Award in Science [ 217316/Z/19/Z ]. CN is supported by the Medical Research Council [ MR/S026460/1 ]. The views expressed are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = jun,

doi = "https://doi.org/10.1016/j.dcn.2023.101250",

language = "English",

volume = "61",

journal = "Developmental Cognitive Neuroscience",

issn = "1878-9293",

publisher = "Elsevier BV",

}

Vanes, L , Fenn-Moltu, S , Hadaya, L, Fitzgibbon, SP, Cordero-Grande, L , Price, A , Chew, A , Falconer, S , Arichi, T , Counsell, S , Hajnal, J , Batalle, D , Edwards, D & Nosarti, C 2023, 'Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth', Developmental Cognitive Neuroscience, vol. 61, 101250. https://doi.org/10.1016/j.dcn.2023.101250

TY - JOUR

T1 - Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth

AU - Vanes, Lucy

AU - Fenn-Moltu, Sunniva

AU - Hadaya, Laila

AU - Fitzgibbon, Sean P.

AU - Cordero-Grande, Lucilio

AU - Price, Anthony

AU - Chew, Andrew

AU - Falconer, Shona

AU - Arichi, Tomoki

AU - Counsell, Serena

AU - Hajnal, Jo

AU - Batalle, Dafnis

AU - Edwards, David

AU - Nosarti, Chiara

N1 - Funding Information: This work was supported by the European Research Council under the European Union's Seventh Framework Programme (FP7/20072013)/ERC grant agreement no. 319456 (dHCP project). The authors acknowledge infrastructure support from the National Institute for Health Research ( NIHR ) Mental Health Biomedical Research Centre ( BRC ) at South London, Maudsley NHS Foundation Trust and Institute of Psychiatry, Psychology and Neuroscience, King's College London and the NIHR-BRC at Guys and St Thomas’ Hospitals NHS Foundation Trust (GSTFT). The authors also acknowledge support in part from the Wellcome Engineering and Physical Sciences Research Council ( EPSRC ) Centre for Medical Engineering at Kings College London [ WT 203148/Z/16/Z ], and the Department of Health through an NIHR Comprehensive Biomedical Research Centre Award (to Guy’s and St. Thomas’ National Health Service (NHS) Foundation Trust in partnership with King’s College London and King’s College Hospital NHS Foundation Trust). LDV is supported by a King’s Prize Fellowship [Wellcome Trust Institutional Strategic Support Fund; 204823/Z/16/Z ] and the Medical Research Council [ MR/S026460/1 ]. SFM is supported by a grant from the UK Medical Research Council [ MR/N013700/1 ]. L.C-G. acknowledges funding from Spanish MICINN PID2021-129022OA-I00 and CAM-Spain under the line support for R&D projects for Beatriz Galindo researchers , and Project PID2021–129022OA-I00 funded by MCIN / AEI / 10.13039/501100011033 / FEDER , EU . TA and ADE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King’s College London [ MR/N026063/1 ]. TA is supported by a MRC Clinician Scientist Fellowship [ MR/P008712/1 ] and Transition Support Award [ MR/V036874/1 ]. DB received support from a Wellcome Trust Seed Award in Science [ 217316/Z/19/Z ]. CN is supported by the Medical Research Council [ MR/S026460/1 ]. The views expressed are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Publisher Copyright: © 2023 The Authors

PY - 2023/6

Y1 - 2023/6

N2 - Preterm birth results in premature exposure of the brain to the extrauterine environment during a critical period of neurodevelopment. Consequently, infants born preterm are at a heightened risk of adverse behavioural outcomes in later life. We characterise longitudinal development of neonatal regional brain volume and functional connectivity in the first weeks following preterm birth, sociodemographic factors, and their respective relationships to psychomotor outcomes and psychopathology in toddlerhood. We study 121 infants born preterm who underwent magnetic resonance imaging shortly after birth, at term-equivalent age, or both. Longitudinal regional brain volume and functional connectivity were modelled as a function of psychopathology and psychomotor outcomes at 18 months. Better psychomotor functioning in toddlerhood was associated with greater relative right cerebellar volume and a more rapid decrease over time of sensorimotor degree centrality in the neonatal period. In contrast, increased 18-month psychopathology was associated with a more rapid decrease in relative regional subcortical volume. Furthermore, while socio-economic deprivation was related to both psychopathology and psychomotor outcomes, cognitively stimulating parenting predicted psychopathology only. Our study highlights the importance of longitudinal imaging to better predict toddler outcomes following preterm birth, as well as disparate environmental influences on separable facets of behavioural development in this population.

AB - Preterm birth results in premature exposure of the brain to the extrauterine environment during a critical period of neurodevelopment. Consequently, infants born preterm are at a heightened risk of adverse behavioural outcomes in later life. We characterise longitudinal development of neonatal regional brain volume and functional connectivity in the first weeks following preterm birth, sociodemographic factors, and their respective relationships to psychomotor outcomes and psychopathology in toddlerhood. We study 121 infants born preterm who underwent magnetic resonance imaging shortly after birth, at term-equivalent age, or both. Longitudinal regional brain volume and functional connectivity were modelled as a function of psychopathology and psychomotor outcomes at 18 months. Better psychomotor functioning in toddlerhood was associated with greater relative right cerebellar volume and a more rapid decrease over time of sensorimotor degree centrality in the neonatal period. In contrast, increased 18-month psychopathology was associated with a more rapid decrease in relative regional subcortical volume. Furthermore, while socio-economic deprivation was related to both psychopathology and psychomotor outcomes, cognitively stimulating parenting predicted psychopathology only. Our study highlights the importance of longitudinal imaging to better predict toddler outcomes following preterm birth, as well as disparate environmental influences on separable facets of behavioural development in this population.

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U2 - https://doi.org/10.1016/j.dcn.2023.101250

DO - https://doi.org/10.1016/j.dcn.2023.101250

M3 - Article

SN - 1878-9293

VL - 61

JO - Developmental Cognitive Neuroscience

JF - Developmental Cognitive Neuroscience

M1 - 101250

ER -

Longitudinal neonatal brain development and socio-demographic correlates of infant outcomes following preterm birth

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