Visceral fat is associated with lower executive functioning in adolescents

D H Schwartz, G Leonard, M Perron, L Richer, C Syme, S Veillette, Z Pausova, T Paus, D H Schwartz, G Leonard, M Perron, L Richer, C Syme, S Veillette, Z Pausova, T Paus

Abstract

Background: Obesity, a major risk factor for cardiometabolic disease, is associated with lower cognitive performance from childhood to senescence, especially on tasks of executive function. In the cardiovascular domain, fat stored viscerally rather than elsewhere in the body carries particularly high risk. It is unknown whether this is also true in case of obesity-cognition relationships. The aim of this study was to assess the cross-sectional relationship between visceral fat (VF) and cognitive performance in a community sample of healthy adolescents.

Methods: In a community-based sample of 983 adolescents (12-18 years old, 480 males), VF was quantified using magnetic resonance imaging, total body fat was measured using a multifrequency bioimpedance, and cognitive performance was assessed using a battery of cognitive tests measuring executive function and memory.

Results: We found that larger volumes of VF were associated with lower performance on six measures of executive function (P=0.0001-0.02). We also found that the association of VF with executive function was moderated by sex for a subset of measures, such that relationship was present mainly in female subjects and not in male subjects (sex-by-VF interaction: P=0.001-0.04). These relationships were independent of the quantity of total body fat and a number of potential confounders, including age, puberty stage and household income.

Conclusions: Our results suggest that the adverse association between obesity and executive function may be attributed to fat stored viscerally and not to fat stored elsewhere in the body. They also suggest that female subjects compared with male subjects may be more sensitive to the potentially detrimental effects of VF on cognition.

Conflict of interest statement

We declare no conflicts of interest.

Figures

Figure 1
Figure 1
The role of sex in moderating the impact of visceral fat (VF) and total body fat (TBF) on cognitive performance for five neuropsychological outcomes. Interactions quantified using continuous variables in multilevel models as detailed in Table 2. For significant interactions, post hoc tests were calculated for simple slopes at one standard deviation above and below the means of both predictors, as graphed here. A. Symbol Search – total number of search targets correctly identified, B. Digit-span Forwards –total number of correctly repeated forward digit strings C. Digit-span Backwards – total number of correctly repeated backward digit strings D. Stroop Interference – performance on color-word incongruent trial (Color-Word Score) controlled for overall speed of naming (Predicted score), see Supplementary Appendix for calculation details. E. Phonemic Fluency – total number of words reported. Low VF/TBF – dark gray, High VF/TBF – light gray, *p<.05, **p<.01, ***p<.001

References

    1. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA. 2006;295(13):1549–55.
    1. Survey CCH. Overweight Canadian children and adolescnets. Vol. 2004. Canada: 2004. [Accessed September 5, 2012]. Available at .
    1. Survey CCH. Adult obesity in Canada: Measured height and weight. Vol. 2004. Canada: 2004. [Accessed September 5, 2012]. Available at .
    1. Aronne LJ. Epidemiology, morbidity, and treatment of overweight and obesity. J Clin Psychiat. 2001;62(Suppl 23):13–22.
    1. Whitmer RA, Gunderson EP, Barrett-Connor E, Quesenberry CP, Jr, Yaffe K. Obesity in middle age and future risk of dementia: a 27 year longitudinal population based study. BMJ. 2005;330(7504):1360.
    1. Kamijo K, Khan NA, Pontifex MB, Scudder MR, Drollette ES, Raine LB, et al. The relation of adiposity to cognitive control and scholastic achievement in preadolescent children. Obesity. 2012;20(12):2406–11.
    1. Verdejo-Garcia A, Perez-Exposito M, Schmidt-Rio-Valle J, Fernandez-Serrano MJ, Cruz F, Perez-Garcia M, et al. Selective Alterations Within Executive Functions in Adolescents With Excess Weight. Obesity. 2010;18(8):1572–8.
    1. Cserjesi R, Molnar D, Luminet O, Lenard L. Is there any relationship between obesity and mental flexibility in children? Appetite. 2007;49(3):675–8.
    1. Sabia S, Kivimaki M, Shipley MJ, Marmot MG, Singh-Manoux A. Body mass index over the adult life course and cognition in late midlife: the Whitehall II Cohort Study. Am J Clin Nutr. 2009;89(2):601–7.
    1. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev. 2000;21(6):697–738.
    1. Votruba SB, Jensen MD. Regional fat deposition as a factor in FFA metabolism. Ann Rev Nutr. 2007;27:149–63.
    1. Fujioka S, Matsuzawa Y, Tokunaga K, Tarui S. Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism. 1987;36(1):54–9.
    1. Pausova Z, Mahboubi A, Abrahamowicz M, Leonard GT, Perron M, Richer L, et al. Sex differences in the contributions of visceral and total body fat to blood pressure in adolescence. Hypertension. 2012;59(3):572–9.
    1. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology. 1999;53(9):1937–42.
    1. Solomon A, Kivipelto M, Wolozin B, Zhou J, Whitmer RA. Midlife serum cholesterol and increased risk of Alzheimer’s and vascular dementia three decades later. Dement Geriatr Cogn. 2009;28(1):75–80.
    1. Kivipelto M, Helkala EL, Laakso MP, Hanninen T, Hallikainen M, Alhainen K, et al. Midlife vascular risk factors and Alzheimer’s disease in later life: longitudinal, population based study. BMJ. 2001;322(7300):1447–51.
    1. Isaac V, Sim S, Zheng H, Zagorodnov V, Tai SE, Chee M. Adverse associations between visceral adiposity, brain structure, and cognitive performance in healthy elderly. Front Ag Neurosci. 2011;3(12):1–8.
    1. Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Despres JP. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr. 1993;58(4):463–7.
    1. Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation. 2007;116(11):1234–41.
    1. Syme C, Abrahamowicz M, Leonard GT, Perron M, Pitiot A, Qiu X, et al. Intra-abdominal adiposity and individual components of the metabolic syndrome in adolescence: sex differences and underlying mechanisms. Arch Pediat Adol Med. 2008;162(5):453–61.
    1. Pausova Z, Paus T, Abrahamowicz M, Almerigi J, Arbour N, Bernard M, et al. Genes, maternal smoking, and the offspring brain and body during adolescence: Design of the Saguenay Youth Study. Hum Brain Mapp. 2007;28(6):502–18.
    1. Peterson A, Crockett L, Richards M, Boxer A. A self-report measure of pubertal status. J Youth Adolescence. 1988;17(2):117–33.
    1. Schmitz KE, Hovell MF, Nichols JF, et al. A validation study of early adolescents’ pubertal self-assessments. J Early Adolescence. 2004;24(4):357–384.
    1. Brooks-Gunn J, Warren MP, Rosso J, Gargiulo J. Validity of self-report measures of girls’ pubertal status. Child Dev. 1987;58(3):829–841.
    1. Shirtcliff EA, Dahl RE, Pollak SD. Pubertal development: correspondence between hormonal and physical development. Child Dev. 2009;80(2):327–337.
    1. Ruff RM, Allen CC. Ruff 2 and 7 Selective Attention Test professional manual. Odessa, Florida: Psychological Assessment Resources; 1996.
    1. Wechsler D. Wechsler Intelligence Scale for Children. 3. San Antonio, Texas: Psychological Corporation; 1991.
    1. Strauss E, Sherman EMS, Spreen O. A Compendium of Neuropsychological tests: Administration, norms, and commentary. 3. New York: Oxford University Press; 2006.
    1. Petrides M, Milner B. Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia. 1982;20(3):249–62.
    1. Archibald SJ, Kerns KA. Identification and Description of New Tests of Executive Functioning in Children. Child Neuropsychol. 1999;5(2):115–129.
    1. Golden CJ. Stroop Color and Word Test: A manual for clinical and experimental uses. Chicago, Illinois: Stoelting, Co; 1978.
    1. Korkman M, Kirk U, Kemp S. A Development Neuropsychological Assessment Manual. San Antonio, Texas: Psychological Corporation; 1998.
    1. Cohen MJ. Children’s Memory Scale. San Antonio, Texas: Psychological Corporation; 1997.
    1. Aiken LS, West SG, Reno RR. Multiple regression: testing and interpreting interactions. Sage Publications; 1991.
    1. Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociol Method Res. 2004;33:261–304.
    1. Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH. Prevalence of a metabolic syndrome phenotype in adolescents: findings from the third National Health and Nutrition Examination Survey, 1988–1994. Arch Pediat Adol Med. 2003;157(8):821–7.
    1. McGill HC, Jr, McMahan CA. Starting earlier to prevent heart disease. JAMA. 2003;290(17):2320–2.
    1. Kalmijn S, Foley D, White L, Burchfiel CM, Curb JD, Petrovitch H, et al. Metabolic cardiovascular syndrome and risk of dementia in Japanese-American elderly men. The Honolulu-Asia aging study. Arterioscl Throm Vas. 2000;20(10):2255–60.
    1. Vohl MC, Sladek R, Robitaille J, Gurd S, Marceau P, Richard D, et al. A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obesity Res. 2004;12(8):1217–22.
    1. Barrientos RM, Frank MG, Watkins LR, Maier SF. Aging-related changes in neuroimmune-endocrine function: Implications for hippocampal-dependent cognition. Horm Behav. 2012;62(3):219–27.
    1. Sweat V, Starr V, Bruehl H, Arentoft A, Tirsi A, Javier E, et al. C-reactive protein is linked to lower cognitive performance in overweight and obese women. Inflammation. 2008;31(3):198–207.
    1. Gimeno D, Marmot MG, Singh-Manoux A. Inflammatory markers and cognitive function in middle-aged adults: the Whitehall II study. Psychoneuroendocrino. 2008;33(10):1322–34.
    1. Kishinevsky FI, Cox JE, Murdaugh DL, Stoeckel LE, Cook EW, 3rd, Weller RE. fMRI reactivity on a delay discounting task predicts weight gain in obese women. Appetite. 2012;58(2):582–92.
    1. Pausova Z, Abrahamowicz M, Mahboubi A, Syme C, Leonard GT, Perron M, et al. Functional variation in the androgen-receptor gene is associated with visceral adiposity and blood pressure in male adolescents. Hypertension. 2010;55(3):706–14.
    1. Raznahan A, Lee Y, Stidd R, Long R, Greenstein D, Clasen L, et al. Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. PNAS. 2010;107(39):16988–93.
    1. Ruiz JR, Ortega FB, Castillo R, et al. Physical activity, fitness, weight status, and cognitive performance in adolescents. J Pediatr. 2010;157(6):917–922.
    1. Smith HA, Storti KL, Arena V, et al. Associations between accelerometer-derived physical activity and regional adiposity in young men and women. Obesity. doi: 10.1002/oby.20308. Accepted Article.
    1. Porter SA, Massaro JM, Hoffmann U, Vasan RS, O’Donnel CJ, Fox CS. Abdominal subcutaneous adipose tissue: a protective fat depot? Diabetes Care. 2009;32(6):1068–75.
    1. Demerath EW, Reed D, Rogers N, Sun SS, Lee M, Choh AC, et al. Visceral adiposity and its anatomical distribution as predictors of the metabolic syndrome and cardiometabolic risk factor levels. Am J Clin Nutr. 2008;88(5):1263–71.

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