Longitudinal Evidence of a Vicious Cycle Between Nucleus Accumbens Microstructure and Childhood Weight Gain

Rapuano, Kristina M.; Berrian, Nia; Baskin‐Sommers, Arielle; Décarie-Spain, Léa; Sharma, Sandeep; Fulton, Stephanie; Casey, B. J.; Watts, Richard

doi:10.1016/j.jadohealth.2022.01.002

Cited by 17 publications

(28 citation statements)

References 57 publications

(73 reference statements)

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“…In our study, it may be that a lack of social/economic resources in the environment facilitate continued weight gain, and that weight gain itself caused structural changes in the brain in the caudate (a reward region) that facilitate overeating. This is in line with other studies using the ABCD Study ® data showing that neighborhood resources are related to weight gain ( 23 ) and, that weight gain is associated with changes in brain structure ( 54 , 55 ). Others postulate that social/economic resource advocacy may play a role in determining how much funding is available for neighborhoods ( 56 ), while other studies suggests that decreased social/economic neighborhood resources are detrimental to healthy development of children and adolescents ( 57 ), that have long-lasting (and even lifetime) effects ( 58 ).…”

Section: Discussionsupporting

confidence: 92%

Access to quality health resources and environmental toxins affect the relationship between brain structure and BMI in a sample of pre and early adolescents

Adise

Marshall

Kan

2022

Front. Public Health

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BackgroundEnvironmental resources are related to childhood obesity risk and altered brain development, but whether these relationships are stable or if they have sustained impact is unknown. Here, we utilized a multidimensional index of childhood neighborhood conditions to compare the influence of various social and environmental disparities (SED) on body mass index (BMI)-brain relationships over a 2-year period in early adolescence.MethodsData were gathered the Adolescent Brain Cognitive Development Study® (n = 2,970, 49.8% female, 69.1% White, no siblings). Structure magnetic resonance imaging (sMRI), anthropometrics, and demographic information were collected at baseline (9/10-years-old) and the 2-year-follow-up (11/12-years-old). Region of interest (ROIs; 68 cortical, 18 subcortical) estimates of cortical thickness and subcortical volume were extracted from sMRI T1w images using the Desikan atlas. Residential addresses at baseline were used to obtain geocoded estimates of SEDs from 3 domains of childhood opportunity index (COI): healthy environment (COIHE), social/economic (COISE), and education (COIED). Nested, random-effects mixed models were conducted to evaluate relationships of BMI with (1) ROI * COI[domain] and (2) ROI * COI[domain]* Time. Models controlled for sex, race, ethnicity, puberty, and the other two COI domains of non-interest, allowing us to estimate the unique variance explained by each domain and its interaction with ROI and time.ResultsYouth living in areas with lower COISE and COIED scores were heavier at the 2-year follow-up than baseline and exhibited greater thinning in the bilateral occipital cortex between visits. Lower COISE scores corresponded with larger volume of the bilateral caudate and greater BMI at the 2-year follow-up. COIHE scores showed the greatest associations (n = 20 ROIs) with brain-BMI relationships: youth living in areas with lower COIHE had thinner cortices in prefrontal regions and larger volumes of the left pallidum and Ventral DC. Time did not moderate the COIHE x ROI interaction for any brain region during the examined 2-year period. Findings were independent of family income (i.e., income-to-needs).ConclusionCollectively our findings demonstrate that neighborhood SEDs for health-promoting resources play a particularly important role in moderating relationships between brain and BMI in early adolescence regardless of family-level financial resources.

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Section: Discussionsupporting

confidence: 92%

Access to quality health resources and environmental toxins affect the relationship between brain structure and BMI in a sample of pre and early adolescents

Adise

Marshall

Kan

2022

Front. Public Health

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“…Indeed, our observation of DBSI-assessed cellularity (DBSI-RF) in the striatum in children with obesity is consistent with diet-induced reactive gliosis in the nucleus accumbens of juvenile and adult rodents (Décarie-Spain et al, 2018;Molina et al, 2020). Furthermore, the association between baseline nucleus accumbens cellularity and future weight gain, as observed by us and others (Rapuano et al, 2020(Rapuano et al, , 2022, relates to striatal neuroinflammation-mediated overfeeding in rodent studies (Décarie-Spain et al, 2018). Interestingly, we previously found that putative neuroinflammation in the nucleus accumbens mediates the relationship between obesity and greater self-reported emotional eating in adults (Samara et al, 2021) and Rapuano et al (2022) recently observed that greater putative cellular density in this region mediates the relationship between greater dietary fat intake and higher waist circumference and BMI in children.…”

Section: Links Between Obesity Neuroinflammation and Brain Functionsupporting

confidence: 89%

“…Furthermore, the association between baseline nucleus accumbens cellularity and future weight gain, as observed by us and others (Rapuano et al, 2020(Rapuano et al, , 2022, relates to striatal neuroinflammation-mediated overfeeding in rodent studies (Décarie-Spain et al, 2018). Interestingly, we previously found that putative neuroinflammation in the nucleus accumbens mediates the relationship between obesity and greater self-reported emotional eating in adults (Samara et al, 2021) and Rapuano et al (2022) recently observed that greater putative cellular density in this region mediates the relationship between greater dietary fat intake and higher waist circumference and BMI in children. Taken together, the MRI-based assessments of the hypothalamus and striatum by our lab and others are consistent and report putative neuroinflammation in these regions in childhood obesity, in agreement with studies in rodent models and human adults.…”

Section: Links Between Obesity Neuroinflammation and Brain Functionsupporting

confidence: 65%

“…Our smaller sample size was powered to determine whether DBSI could detect the robust effects found using RSI in Rapuano et al (2020), specifically, obesity-related putative cellularity (DBSI-RF) in striatal regions. In Rapuano et al (2020, 2022), effect sizes were noticeably smaller for the prediction of future waist circumference and BMI metrics by RSI restricted component in nucleus accumbens compared to baseline results. It should be noted that all data from the children in the current study were included in that of Rapuano et al (2020), making up 5% of the previous study’s baseline sample size.…”

Section: Discussionmentioning

confidence: 73%

“…DBSI has not yet been used to assess obesity-related putative neuroinflammation in children. However, Rapuano et al (2020) used the diffusion-based MRI technique restriction spectrum imaging (RSI), which, in contrast to DBSI, models isotropic water diffusion components based on the ratio of radial and axial anisotropic water diffusivities (Palmer et al, 2022;White et al, 2013), and observed that greater purported cellular density in striatal and limbic regions relates to greater baseline and future waist circumference and BMI metrics in children enrolled in the Adolescent Brain Cognitive Development SM Study (ABCD Study ® ) (Casey et al, 2018;Rapuano et al, 2020Rapuano et al, , 2022. Also, using a non-diffusion MRI-based method of assessing putative neuroinflammation, namely quantitative T2-weighted MRI, studies have reported that longer hypothalamic T2 relaxation times and greater T2 signal intensity, both suggestive of reactive microglial and astrocytic gliosis normally seen in response to brain injury, relate to higher BMI in adults (Schur et al, 2015;Thaler et al, 2012) and children, including a subset enrolled in the ABCD Study ® (Sewaybricker et al, 2019;Sewaybricker, Kee, et al, 2021;.…”

Section: Introductionmentioning

confidence: 99%

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Childhood obesity is linked to putative neuroinflammation in brain white matter, hypothalamus, and striatum

Samara

Ray

et al. 2022

Preprint

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Introduction Childhood obesity is increasingly prevalent and confers elevated risk of developing medical complications across the lifespan. Given the brain's prominent involvement in homeostatic and hedonic eating, it is crucial to understand brain health in obesity. Recent studies using quantitative T2-weighted MRI and diffusion-weighted MRI showed obesity-related putative neuroinflammation in human brain. To assess convergent validity across diffusion-based MRI techniques and extend these findings, this study characterized tissue microstructure of white matter (WM) tracts and energy regulation and reward processing brain regions in children across levels of obesity-related measures, using diffusion basis spectrum imaging (DBSI). Methods Using data from the Adolescent Brain Cognitive Development Study (ABCD Study®), DBSI metrics indicative of putative neuroinflammation were computed for WM tracts, hypothalamus, nucleus accumbens, caudate nucleus, and putamen. DBSI metrics were compared between children with normal-weight vs. obesity. DBSI metrics were also correlated to baseline and one- and two-year change in continuous obesity-related measures (waist circumference, BMI, and BMI z-scores). Striatal DBSI findings were compared to those of restriction spectrum imaging (RSI). Results A total of 263 nine- and ten-year old children from the ABCD Study® 2.0.1 data release (5 underweight; 126 with normal-weight; 64 with over-weight; 68 with obesity) who met inclusion and exclusion criteria were randomly selected. Relative to children with normal-weight, children with obesity had lower DBSI fiber fraction (FF; reflects apparent axonal/dendritic density) and higher DBSI restricted fraction (RF; reflects cellularity) in WM tracts throughout the brain (voxel-wise FWE-corrected p < 0.05), as well as higher DBSI-RF in the hypothalamus, nucleus accumbens, and caudate nucleus (Cohen's d's ≥ 0.28, p's ≤ 0.05). Across all children, greater baseline waist circumference was related to higher DBSI-RF in the hypothalamus (standardized β = 0.17, p = 0.0033), nucleus accumbens (standardized β = 0.21, p = 0.0001), and caudate nucleus (standardized β = 0.14, p = 0.013). Gain in waist circumference over one and two years related to higher baseline DBSI-RF in nucleus accumbens (standardized β = 0.12, p = 0.08) and in hypothalamus (standardized β = 0.15, p = 0.03), respectively. Overall, results were consistent for BMI and BMI z-scores. Similar results were observed using RSI metrics. Conclusion Novel findings include demonstration that, as in adults, childhood obesity is associated with DBSI-assessed putative neuroinflammation in WM tracts and hypothalamus. In addition, our results support the reproducibility of previous findings that MRI-assessed putative neuroinflammation in striatum and hypothalamus is related to obesity in children, contributing to a growing understanding of the role of adiposity in brain health across the lifespan.

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Associations Between Socioeconomic Status, Obesity, Cognition, and White Matter Microstructure in Children

Cai

Taylor

et al. 2023

JAMA Netw Open

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ImportanceLower neighborhood and household socioeconomic status (SES) are associated with negative health outcomes and altered brain structure in children. It is unclear whether such findings extend to white matter and via what mechanisms.ObjectiveTo assess whether and how neighborhood and household SES are independently associated with children’s white matter microstructure and examine whether obesity and cognitive performance (reflecting environmental cognitive and sensory stimulation) are plausible mediators.Design, Setting, and ParticipantsThis cross-sectional study used baseline data from participants in the Adolescent Brain Cognitive Development (ABCD) study. Data were collected at 21 US sites, and school-based recruitment was used to represent the US population. Children aged 9 to 11 years and their parents or caregivers completed assessments between October 1, 2016, and October 31, 2018. After exclusions, 8842 of 11 875 children in the ABCD study were included in the analyses. Data analysis was conducted from July 11 to December 19, 2022.ExposuresNeighborhood disadvantage was derived from area deprivation indices at participants’ primary residence. Household SES factors were total income and highest parental educational attainment.Main Outcomes and MeasuresA restriction spectrum imaging (RSI) model was used to quantify restricted normalized directional (RND; reflecting oriented myelin organization) and restricted normalized isotropic (RNI; reflecting glial and neuronal cell bodies) diffusion in 31 major white matter tracts. The RSI measurements were scanner harmonized. Obesity was assessed through body mass index (BMI; calculated as weight in kilograms divided by height in meters squared), age- and sex-adjusted BMI z scores, and waist circumference, and cognition was assessed through the National Institutes of Health Toolbox Cognition Battery. Analyses were adjusted for age, sex, pubertal development stage, intracranial volume, mean head motion, and twin or siblingship.ResultsAmong 8842 children, 4543 (51.4%) were boys, and the mean (SD) age was 9.9 (0.7) years. Linear mixed-effects models revealed that greater neighborhood disadvantage was associated with lower RSI-RND in the left superior longitudinal fasciculus (β = −0.055; 95% CI, −0.081 to −0.028) and forceps major (β = −0.040; 95% CI, −0.067 to −0.013). Lower parental educational attainment was associated with lower RSI-RND in the bilateral superior longitudinal fasciculus (eg, right hemisphere: β = 0.053; 95% CI, 0.025-0.080) and bilateral corticospinal or pyramidal tract (eg, right hemisphere: β = 0.042; 95% CI, 0.015-0.069). Structural equation models revealed that lower cognitive performance (eg, lower total cognition score and higher neighborhood disadvantage: β = −0.012; 95% CI, −0.016 to −0.009) and greater obesity (eg, higher BMI and higher neighborhood disadvantage: β = −0.004; 95% CI, −0.006 to −0.001) partially accounted for the associations between SES and RSI-RND. Lower household income was associated with higher RSI-RNI in most tracts (eg, right inferior longitudinal fasciculus: β = −0.042 [95% CI, −0.073 to −0.012]; right anterior thalamic radiations: β = −0.045 [95% CI, −0.075 to −0.014]), and greater neighborhood disadvantage had similar associations in primarily frontolimbic tracts (eg, right fornix: β = 0.046 [95% CI, 0.019-0.074]; right anterior thalamic radiations: β = 0.045 [95% CI, 0.018-0.072]). Lower parental educational attainment was associated with higher RSI-RNI in the forceps major (β = −0.048; 95% CI, −0.077 to −0.020). Greater obesity partially accounted for these SES associations with RSI-RNI (eg, higher BMI and higher neighborhood disadvantage: β = 0.015; 95% CI, 0.011-0.020). Findings were robust in sensitivity analyses and were corroborated using diffusion tensor imaging.Conclusions and RelevanceIn this cross-sectional study, both neighborhood and household contexts were associated with white matter development in children, and findings suggested that obesity and cognitive performance were possible mediators in these associations. Future research on children’s brain health may benefit from considering these factors from multiple socioeconomic perspectives.

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Longitudinal Evidence of a Vicious Cycle Between Nucleus Accumbens Microstructure and Childhood Weight Gain

Cited by 17 publications

References 57 publications

Access to quality health resources and environmental toxins affect the relationship between brain structure and BMI in a sample of pre and early adolescents

Access to quality health resources and environmental toxins affect the relationship between brain structure and BMI in a sample of pre and early adolescents

Childhood obesity is linked to putative neuroinflammation in brain white matter, hypothalamus, and striatum

Associations Between Socioeconomic Status, Obesity, Cognition, and White Matter Microstructure in Children

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