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Longitudinal growth of the basal ganglia and thalamus in very preterm children

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Abstract

The impact of very preterm (VP) birth on the development of individual basal ganglia nuclei and the thalamus during childhood remains unclear. We first aimed to compare (1a) the volumes of individual basal ganglia nuclei (nucleus accumbens, caudate nucleus, pallidum, putamen) and the thalamus at age 7 years, and (1b) their volumetric change from infancy to 7 years, in VP children with term-born children. Secondly, we aimed to (2a) determine whether basal ganglia and thalamic volumes at 7 years, or (2b) basal ganglia and thalamic growth rates from infancy to 7 years were associated with neurodevelopmental outcomes at 7 years, and whether these associations differed between the VP and term-born children. One hundred and fifty-four VP (<30 weeks’ gestational age or birth weight < 1250 g) and 35 term-born children had useable magnetic resonance imaging (MRI) scans that could be analyzed at 7 years. Of these, 149 VP and 30 term-born infants also had useable MRI scans at term-equivalent age. Volumes of the individual basal ganglia nuclei and the thalamus were automatically generated from the MRI scans. Compared with the term-born group, the VP group had smaller basal ganglia and thalamic volumes at 7 years and slower growth rates from birth to 7 years. After controlling for overall brain size, VP children still had smaller thalamic volumes but the deep grey matter volume growth rates from birth to 7 years were similar between groups. Reduced basal ganglia and thalamic volumes and slower growth rates in the VP group were associated with poorer cognition, academic achievement and motor function at 7 years. After controlling for overall brain size, the nucleus accumbens and pallidum were the deep grey matter structures most strongly associated with 7-year neurodevelopmental outcomes. In conclusion, basal ganglia and thalamic growth is delayed during early childhood in VP children, with delayed development contributing to poorer functional outcomes.

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Abbreviations

CNAcc:

Caudate nucleus/Nucleus accumbens complex

IQ:

Intelligence Quotient

M:

Mean

MABC-2:

Movement Assessment Battery for Children-2

MANTiS:

Morphologically Adaptive Neonatal Tissue Segmentation

MRI:

Magnetic Resonance Imaging

PSST:

Pediatric Subcortical Segmentation Technique

SD:

Standard Deviation

SDQ:

Strengths and Difficulties Questionnaire

TBV:

Total Brain Volume

VIBeS:

Victorian Infant Brain Studies

VP:

Very Preterm

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Acknowledgements

We are grateful for the help and support of the Victorian Infant Brain Studies (VIBeS) and Developmental Imaging groups, as well as the Melbourne Children’s MRI Centre at the Murdoch Childrens Research institute. We also thank the families and children who participated in this study.

Funding

This study was supported by Australia’s National Health & Medical Research Council: Centre for Clinical Research Excellence 546519 (L.W.D. and P.J.A.); Centre for Research Excellence 1060733 (L.W.D., P.J.A., J.L.Y.C., D.K.T., A.J.S. and W.Y.L.); Project Grant 491209 (P.J.A., L.W.D., T.E.I. and J.L.Y.C.; Senior Research Fellowship 628371 & 1081288 (P.J.A.); Career Development Fellowships 1108714 (A.J.S.), 1085754 (D.K.T.), 1053609 to (K.J.L.); Early Career Fellowship 1053787 (J.L.Y.C.). This study was also supported by the National Institutes of Health (HD058056), the Victorian Government’s Operational Infrastructure Support Program, and The Royal Children’s Hospital Foundation.

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Correspondence to Wai Yen Loh.

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Wai Yen Loh, Peter J Anderson, Jeanie LY Cheong, Alicia J Spittle, Jian Chen, Katherine J Lee, Charlotte Molesworth, Terrie E Inder, Alan Connelly, Lex W Doyle and Deanne K Thompson declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Loh, W.Y., Anderson, P.J., Cheong, J.L.Y. et al. Longitudinal growth of the basal ganglia and thalamus in very preterm children. Brain Imaging and Behavior 14, 998–1011 (2020). https://doi.org/10.1007/s11682-019-00057-z

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  • DOI: https://doi.org/10.1007/s11682-019-00057-z

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