Research Article: Volumetric gray matter measures of amygdala and accumbens in childhood overweight/obesity

Date Published: October 18, 2018

Publisher: Public Library of Science

Author(s): Gabor Perlaki, Denes Molnar, Paul A. M. Smeets, Wolfgang Ahrens, Maike Wolters, Gabriele Eiben, Lauren Lissner, Peter Erhard, Floor van Meer, Manfred Herrmann, Jozsef Janszky, Gergely Orsi, Francisco J. Esteban.

http://doi.org/10.1371/journal.pone.0205331

Abstract

Neuroimaging data suggest that pediatric overweight and obesity are associated with morphological alterations in gray matter (GM) brain structures, but previous studies using mainly voxel-based morphometry (VBM) showed inconsistent results. Here, we aimed to examine the relationship between youth obesity and the volume of predefined reward system structures using magnetic resonance (MR) volumetry. We also aimed to complement volumetry with VBM-style analysis.

Fifty-one Caucasian young subjects (32 females; mean age: 13.8±1.9, range: 10.2–16.5 years) were included. Subjects were selected from a subsample of the I.Family study examined in the Hungarian center. A T1-weighted 1 mm3 isotropic resolution image was acquired. Age- and sex-standardized body mass index (zBMI) was assessed at the day of MRI and ~1.89 years (mean±SD: 689±188 days) before the examination. Obesity related GM alterations were investigated using MR volumetry in five predefined brain structures presumed to play crucial roles in body weight regulation (hippocampus, amygdala, accumbens, caudate, putamen), as well as whole-brain and regional VBM.

The volumes of accumbens and amygdala showed significant positive correlations with zBMI, while their GM densities were inversely related to zBMI. Voxel-based GM mass also showed significant negative correlation with zBMI when investigated in the predefined amygdala region, but this relationship was mediated by GM density.

Overweight/obesity related morphometric brain differences already seem to be present in children/adolescents. Our work highlights the disparity between volume and VBM-derived measures and that GM mass (combination of volume and density) is not informative in the context of obesity related volumetric changes. To better characterize the association between childhood obesity and GM morphometry, a combination of volumetric segmentation and VBM methods, as well as future longitudinal studies are necessary. Our results suggest that childhood obesity is associated with enlarged structural volumes, but decreased GM density in the reward system.

Partial Text

Overweight and obese children and adolescents represent a major public health problem in many countries, including Hungary [1–3]. The rate of overweight (including obesity) among Hungarian children and adolescents aged 5–17 years is over 25% (28% and 23% for boys and girls respectively) [4]. Obesity in this age range is associated with increased risk for cardiovascular disease [5], type 2 diabetes [6] as well as other adverse conditions [7–9]. Moreover, obese youths are more likely to become obese adults [10] and as adults are more likely to develop adverse health effects [11–13].

BMI z-score T4 and T3 were not different between sexes (P = 0.650; t = 0.456 and P = 0.953; t = -0.060 respectively, two-tailed independent samples t tests) and puberty stages (P = 0.776; t = -0.286 and P = 0.929; t = -0.090 respectively, two-tailed independent samples t tests) nor were associated with ICV (P = 0.709; r = 0.053 and P = 0.900; r = 0.018 respectively, two-tailed Pearson correlations) and age (P = 0.795; ρ = -0.037 and P = 0.830; ρ = -0.031 respectively, two-tailed Spearman correlations). Table 1 shows the demographic and obesity related characteristics of our subjects.

In conclusion, the present study shows that overweight/obesity related brain differences may already be present in children/adolescents. Our results suggest that a higher degree of obesity in children/adolescents is associated with greater volumes of amygdala and accumbens; both regions involved in motivated behavior related to food intake regulation. Future longitudinal studies should clarify the causality and whether these early brain differences are reversible or not. Somewhat unexpectedly, the GMD of both amygdala and accumbens was negatively correlated with obesity, although currently it is not clear whether this pattern is a consequence of histological alterations or the methodological limitations specific to VBM analysis. The disparity found between VBM-derived measures and volume in the context of obesity in children/adolescents may inspire new volumetry studies and warrants cautious interpretation of VBM studies in obesity.

 

Source:

http://doi.org/10.1371/journal.pone.0205331

 

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