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Pediatrics

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

International Journal of Obesity volume 47, pages 590–605 (2023)Cite this article

Subjects

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.

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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Author notes

  1. These authors contributed equally: Skylar J. Brooks, Calli Smith.

Authors and Affiliations

  1. Boston Children’s Hospital, Department of Pediatrics, Division of Adolescent Medicine, Boston, MA, USA

    Skylar J. Brooks, Calli Smith & Catherine Stamoulis

  2. University of California Berkeley, Helen Wills Neuroscience Institute, Berkeley, CA, USA

    Skylar J. Brooks

  3. Harvard Medical School, Department of Pediatrics, Boston, MA, USA

    Catherine Stamoulis

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  3. Catherine Stamoulis
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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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  • DOI: https://doi.org/10.1038/s41366-023-01303-7

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