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Pediatrics

Excess BMI in early adolescence adversely impacts maturating functional circuits supporting high-level cognition and their structural correlates

Abstract

Background/Objectives

Adverse effects of excess BMI (affecting 1 in 5 children in the US) on brain circuits during neurodevelopmentally vulnerable periods are incompletely understood. This study investigated BMI-related alterations in maturating functional networks and their underlying brain structures, and high-level cognition in early adolescence.

Subjects/Methods

Cross-sectional resting-state fMRI, structural sMRI, neurocognitive task scores, and BMI from 4922 youth [median (IQR) age = 120.0 (13.0) months, 2572 females (52.25%)] from the Adolescent Brain Cognitive Development (ABCD) cohort were analyzed. Comprehensive topological and morphometric network properties were estimated from fMRI and sMRI, respectively. Cross-validated linear regression models assessed correlations with BMI. Results were reproduced across multiple fMRI datasets.

Results

Almost 30% of youth had excess BMI, including 736 (15.0%) with overweight and 672 (13.7%) with obesity, and statistically more Black and Hispanic compared to white, Asian and non-Hispanic youth (p < 0.01). Those with obesity or overweight were less physically active, slept less than recommended, snored more frequently, and spent more time using an electronic device (p < 0.01). They also had lower topological efficiency, resilience, connectivity, connectedness and clustering in Default-Mode, dorsal attention, salience, control, limbic, and reward networks (p ≤ 0.04, Cohen’s d: 0.07-0.39). Lower cortico-thalamic efficiency and connectivity were estimated only in youth with obesity (p < 0.01, Cohen’s d: 0.09-0.19). Both groups had lower cortical thickness, volume and white matter intensity in these networks’ constituent structures, particularly anterior cingulate, entorhinal, prefrontal, and lateral occipital cortices (p < 0.01, Cohen’s d: 0.12-0.30), which also mediated inverse relationships between BMI and regional functional topologies. Youth with obesity or overweight had lower scores in a task measuring fluid reasoning - a core aspect of cognitive function, which were partially correlated with topological changes (p ≤ 0.04).

Conclusions

Excess BMI in early adolescence may be associated with profound aberrant topological alterations in maturating functional circuits and underdeveloped brain structures that adversely impact core aspects of cognitive function.

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Fig. 1: Network plots showing regions and connections that are correlated with excess BMI (with overweight or obesity) relative to normal BMI.
Fig. 2: Significant negative correlations between BMI status (with overweight—top plot, with obesity—bottom plot), relative to normal BMI, and regional node properties, including node degree and clustering.

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Data availability

All analyzed data are publicly available through the National Institute of Mental Health Data Archive (NDA) https://nda.nih.gov/. All computer codes associated with neuroimaging data analyses are part of the publicly shared Next-Generation Neural Data Analysis-NGNDA https://github.com/cstamoulis1/Next-Generation-Neural-Data-Analysis-NGNDA- platform. Codes associated with statistical analyses are available in: https://github.com/cstamoulis1/Brain-BMI-Analyses.git.

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Acknowledgements

This work was supported by the National Science Foundation, through awards #1940094, #1649865 and #2116707.

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CSt conceived and designed the study. SB and CSm conducted the data analyses. All three authors wrote, reviewed and approved the manuscript.

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Correspondence to Catherine Stamoulis.

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Brooks, S.J., Smith, C. & Stamoulis, C. Excess BMI in early adolescence adversely impacts maturating functional circuits supporting high-level cognition and their structural correlates. Int J Obes 47, 590–605 (2023). https://doi.org/10.1038/s41366-023-01303-7

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