Roles of diet, physical activity, sedentary time and the gut-microbiome in cognitive and executive functioning development during early life

McMath, Arden Lee

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https://hdl.handle.net/2142/122199 Copy

Description

Title

Roles of diet, physical activity, sedentary time and the gut-microbiome in cognitive and executive functioning development during early life

Author(s)

McMath, Arden Lee

Issue Date

2023-09-08

Director of Research (if dissertation) or Advisor (if thesis)

• Donovan, Sharon
• Khan, Naiman

Doctoral Committee Chair(s)

Dilger, Ryan

Committee Member(s)

Woods, Jeffery

Department of Study

Nutritional Sciences

Discipline

Nutritional Sciences

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• cognitive development
• diet
• microbiome

Abstract

Executive function (EF), defined as cognitive processes pertinent to the regulation of goal-directed behaviors, may have immediate consequences for academic achievement and lasting consequences for success in adulthood 1,2. Early childhood is a key time for development of EF3, and may be impacted by diet4 and physical activity 4, and the transition towards an adult-like gastrointestinal microbiome 5. The objective of this research is to define how diet (Studies 2, 3, 4), physical activity (Study 2), screen time (a proxy for sedentary time) (Study 2), and gastrointestinal microbiome composition (Studies 1 and 5) influence EF development. Parents from the STRONG Kids 2 cohort study (n= 468) completed surveys about their child’s EF, physical activity, diet and screen time at 24, 36 and 48-mo. Child fecal samples were also collected as these timepoints for microbiota analyses. Children were recruited for sub-study at 4 or 5-yo (n= 94), involving objective assessments of EF and academic achievement. Study 1. Evidence from animal models or children with neurodevelopmental disorders has implicated the gut microbiome in neurocognitive development. However, even subclinical impairment of cognition can have negative consequences, as cognition serves as the foundation for skills necessary to succeed in school, vocation and socially. Study 1 aimed to identify gut microbiome characteristics or changes in gut microbiome characteristics that consistently associate with cognitive outcomes in healthy, neurotypical infants and children. Of the 1,520 articles identified in the search, 23 were included in qualitative synthesis after applying exclusion criteria. Most studies were cross-sectional and focused on behavior or motor and language skills. Bifidobacterium, Bacteroides, Clostridia, Prevotella, and Roseburia were related to these aspects of cognition across several studies. While these results support the role of gut microbiome in cognitive development, higher quality studies focused on more complex cognition are needed to understand the extent to which the gut microbiome contributes to cognitive development. Study 2. The aim of this study was to test the hypothesis that healthy weight status and adherence to American Academy of Pediatrics (AAP) guidelines for diet and physical activity would extend to greater EF at age 24 months. Parents of 24-month-old children from the STRONG Kids 2 cohort study (n = 352) completed the Behavioral Rating Inventory of Executive Function for Preschoolers (BRIEF-P) and reported physical activities, diet, and screen time. Toddlers met AAP guidelines if they consumed at least 5 servings of fruits and vegetables, were physically active, refrained from sugar-sweetened beverages, and limited daily screen time to <60 minutes. Relationships between EF, 24-month weight status, and meeting AAP guidelines were tested independent of child sex, ethnicity, socioeconomic status, weight status at birth, and maternal pregnancy weight status. Weight-for-length Z-score was not directly related to EF, nor did it mediate relationships between AAP guidelines and EF. Toddlers meeting the screen time guideline had greater EF (β= −0.125; 95% CI= 0.234 to −0.008), inhibitory self-control (β= −0.142; 95% CI= −0.248 to −0.029), and emergent metacognition (β= −0.111; 95% CI= −0.221 to 0.002), indicated by lower BRIEF-P scores. Those with more minutes of screen time had poorer overall EF (β= 0.257; 95% CI= 0.118-0.384), inhibitory self-control (β= 0.231; 95% CI= 0.099-0.354), cognitive flexibility (β= 0.217; 95% CI= 0.082-0.342), and emergent metacognition (β= 0.257; 95% CI= 0.120-0.381). Daily physical activity was associated with greater emergent metacognition (β= −0.116; 95% CI= −0.225 to −0.005). Meeting AAP guidelines for physical activity and screen time was related to greater EF in a demographically homogenous sample of toddlers. Future randomized control trials and more diverse samples are needed to confirm the directionality of this relationship. Study 3. This study aimed to identify and describe diet patterns of children during early childhood using confirmatory factor analysis (CFA). Longitudinal data were drawn from the STRONG Kids2 program. Mothers were surveyed about their child’s diet at 24 (n = 337), 36 (n = 317), and 48 (n = 289) months. The Block Food Frequency Questionnaire (FFQ) for Ages 2-7 was used to derive diet patterns; 23 food groups were created for analyses. Principal component analysis (PCA) was used to obtain preliminary factor loadings and loadings were used to form a priori hypotheses for CFA-derived diet patterns. Independent samples t-tests were used to compare food groups, nutrient intakes, child and family characteristics by CFA pattern scores above versus at/below the median. Three diet patterns consistently emerged: 1) processed meats, fried and sweet foods, 2) vegetables, legumes, and starchy vegetables, and 3) grains, nuts/seeds and condiments (only 24 and 36 months). These patterns were related to differences in added sugars, dietary fiber and potassium intakes, and maternal education status and household income. These findings suggest a promising avenue for improving methodological approaches for deriving diet patterns and exploring their reproducibility throughout childhood: combining PCA and CFA allows for confirmation and refinement of data-driven diet pattern models. Study 4. The role of diet patterns on cognitive abilities in preschool ages is sparsely explored, focusing primarily on older children. Study 4 aimed to define how diet patterns throughout early childhood influence development of EF and academic skills using data from the longitudinal STRONGKids2 cohort. The parent-survey, Behavioral Inventory of Executive Functions (BRIEF-P), was used to assess overall EFs at 24 and 48-months, while a sub-sample of children completed a modified Eriksen flanker to measure attentional inhibition, a hearts and flowers switch task to assess cognitive flexibility, the Woodcock Johnson’s Early Cognitive and Academic Development tests (ECAD) to assess academic abilities during preschool ages (48 and 72-months). Block Food Frequency Questionnaire items were grouped into 23 food groups, and inputted into PCA and CFA to derive patterns. Diet pattern scores were implemented into multivariable linear regressions for EFs at 24- (n=217) and 48-months (n=250-266), as well as performance metrics on an attentional inhibition (n=53-56) and cognitive flexibility (n=50-59) tasks, cognitive (n=65-71) and academic (n=55-57) scores in preschooler sub-sample. A 36-month diet pattern characterized by higher intakes of processed meats, sweet, and fried foods was related to lower ECAD scores in preschoolers (all >-.351, R2>.115, FDR-adjusted p-value=0.028). A diet pattern higher in grains, nuts/seeds, and condiments at 24-months was related to greater incongruent Flanker accuracy (=-.380, R2=.132, FDR-adjusted p-value=0.030). Diet patterns that tracked from 2 to 4-years were related to academic achievement and attentional inhibition, suggesting importance of early diet interventions to promote cognitive development. Study 5. Current studies exploring the impact of gut microbiome on cognitive development focus primarily on infant temperament, behavior, language skills and motor skills. Few studies are conducted in preschool age children, and even fewer focus on EFs or academic skills. Study 5 aimed to investigate the impact of gut microbiota diversity and microbial-derived volatile fatty acids (VFAs) on development of EFs on EFs and academic achievement using data from the longitudinal STRONGKids2 cohort. Overall EF was measured via 24 and 48-mo BRIEF-P surveys, and attentional inhibition via modified Eriksen flanker, cognitive flexibility via hearts and flowers switch task, and academic skills via the ECAD during preschool ages (48 and 72-months). Child fecal samples were collected for gut microbiota analysis via 16S rRNA sequencing (24 and 48-mo) and VFA analysis via gas chromatography (24-mo and between 48 and 60-mo). Principle coordinates analysis (PCoA) was performed with weighted and unweighted UniFrac distance measures to describe beta diversity. Multiple linear regressions were used to assess relationships between VFA concentrations (n= 23 to 38) and alpha diversity metrics (n = 48 to 80) with cognitive functions. PERMANOVAs were utilized to assess differences in beta diversity based on cognitive performance (n = 48 to 80). All analyses were corrected for multiple comparisons using Benjamini-Hocheberg correction (BH). In models adjusted for maternal education, child sex, breastfeeding exclusivity at 6-wo, presence of siblings, being in school at time of cognitive assessments and dietary fiber intake, greater 24 and 48-mo alpha diversity were related to higher congruent condition accuracy of switch ( = 0.28 to 0.44, p = 0.001 to 0.026, q = 0.056 to 0.345) and Flanker tasks ( = 0.29 to 0.30, p = 0.0237 to 0.033, q = 0.345). Adjusted beta diversity analyses revealed that earlier (24-mo) community structure was associated with higher homogenous switch hearts (F = 1.35 to 2.75, p = 0.001 to 0.006, q = 0.030 to 0.090) and heterogenous switch accuracy (F = 1.23, p = 0.027, q = 0.270). Children with higher 48/60-mo acetate and butyrate concentrations had faster reaction times for both congruent conditions of the switch ( = -0.49 to -0.50, p = 0.006 to 0.007) and Flanker tasks ( = -0.45 to -0.51, p = 0.023 to 0.048). After BH, only relationships of cognitive outcomes with 24-mo community structure and relative abundances remained. Performance on homogenous hearts condition of the hearts and flowers task is likely a reflection of working memory, while the heterogenous task condition is intended to target cognitive flexibility skill. Therefore, the present study demonstrates the potential importance of 1) higher preschool-age alpha diversity and microbial-derived butyrate and acetate on working memory and 2) early (24-mo) gut microbiota composition on working memory and cognitive flexibility in preschool aged children. Limiting screen time, consuming a more healthful diet pattern, and the relative abundance of age-specific gut microbiome are related to better EF and cognition. These findings could inform future preventative and interventional efforts to ultimately improve success in school, vocational productivity, mental and physical health, and quality of life throughout childhood.

Graduation Semester

2023-12

Type of Resource

Thesis

Copyright and License Information

Copyright 2023 Arden McMath

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