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.
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References
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: 1549–1555.
Survey CCH. Overweight Canadian children and adolescents, Canada 2004. Available at: http://www.statcan.gc.ca (accessed 5 September 2012).
Survey CCH. Adult obesity in Canada: measured height and weight, Canada 2004. Available at: http://www.statcan.gc.ca (accessed 5 September 2012).
Aronne LJ . Epidemiology, morbidity, and treatment of overweight and obesity. J Clin Psychiat 2001; 62 (Suppl 23): 13–22.
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: 1360.
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: 2406–2411.
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: 1572–1578.
Cserjesi R, Molnar D, Luminet O, Lenard L . Is there any relationship between obesity and mental flexibility in children? Appetite 2007; 49: 675–678.
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: 601–607.
Wajchenberg BL . Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697–738.
Votruba SB, Jensen MD . Regional fat deposition as a factor in FFA metabolism. Ann Rev Nutr 2007; 27: 149–163.
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: 54–59.
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: 572–579.
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: 1937–1942.
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: 75–80.
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: 1447–1451.
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: 1–8.
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: 463–467.
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: 1234–1241.
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: 453–461.
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: 502–518.
Peterson A, Crockett L, Richards M, Boxer A . A self-report measure of pubertal status. J Youth Adolesc 1988; 17: 117–133.
Schmitz KE, Hovell MF, Nichols JF et al. A validation study of early adolescents’ pubertal self-assessments. J Early Adolescence 2004; 24: 357–384.
Brooks-Gunn J, Warren MP, Rosso J, Gargiulo J . Validity of self-report measures of girls’ pubertal status. Child Dev 1987; 58: 829–841.
Shirtcliff EA, Dahl RE, Pollak SD . Pubertal development: correspondence between hormonal and physical development. Child Dev 2009; 80: 327–337.
Ruff RM, Allen CC . Ruff 2 and 7 Selective Attention Test professional manual. Psychological Assessment Resources: Odessa, FL, USA, 1996.
Wechsler D . Wechsler Intelligence Scale for Children 3rd edn. Psychological Corporation: San Antonio, TX, USA, 1991.
Strauss E, Sherman EMS, Spreen O . A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary 3rd edn. Oxford University Press: New York, NY, USA, 2006.
Petrides M, Milner B . Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 1982; 20: 249–262.
Archibald SJ, Kerns KA . Identification and description of new tests of executive functioning in children. Child Neuropsychol 1999; 5: 115–129.
Golden CJ . Stroop Color and Word Test: A Manual for Clinical and Experimental Uses. Stoelting Co.: Chicago, IL, USA, 1978.
Korkman M, Kirk U, Kemp SA . Development Neuropsychological Assessment Manual. Psychological Corporation: San Antonio, TX, USA, 1998.
Cohen MJ . Children’s Memory Scale. Psychological Corporation: San Antonio, TX, USA, 1997.
Aiken LS, West SG, Reno RR . Multiple Regression: Testing and Interpreting Interactions. Sage Publications, 1991.
Burnham KP, Anderson DR . Multimodel inference: understanding AIC and BIC in model selection. Sociol Method Res 2004; 33: 261–304.
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: 821–827.
McGill HC Jr, McMahan CA . Starting earlier to prevent heart disease. JAMA 2003; 290: 2320–2322.
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: 2255–2260.
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: 1217–1222.
Barrientos RM, Frank MG, Watkins LR, Maier SF . Aging-related changes in neuroimmune–endocrine function: Implications for hippocampal-dependent cognition. Horm Behav 2012; 62: 219–227.
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: 198–207.
Gimeno D, Marmot MG, Singh-Manoux A . Inflammatory markers and cognitive function in middle-aged adults: the Whitehall II study. Psychoneuroendocrinology 2008; 33: 1322–1334.
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: 582–592.
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: 706–714.
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. Proc Natl Acad Sci USA 2010; 107: 16988–16993.
Ruiz JR, Ortega FB, Castillo R, Martín-Matillas M, Kwak L, Vicente-Rodríguez G et al. Physical activity, fitness, weight status, and cognitive performance in adolescents. J Pediatr 2010; 157: 917–922.
Smith HA, Storti KL, Arena V, Kriska AM, Gabriel KK, Sutton-Tyrrell K et al. Associations between accelerometer-derived physical activity and regional adiposity in young men and women. Obesity 2013 doi:10.1002/oby.20308.
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: 1068–1075.
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: 1263–1271.
Acknowledgements
We thank all families who took part in the Saguenay Youth Study and the following individuals for their contributions in designing the protocol, acquiring and analyzing the data: psychometricians (Chantale Belleau, Mélanie Drolet, Catherine Harvey, Stéphane Jean, Hélène Simard, Mélanie Tremblay, Patrick Vachon), ÉCOBES team (Nadine Arbour, Julie Auclair, Marie-Ève Blackburn, Marie-Ève Bouchard, Annie Gautier, Annie Houde, Catherine Lavoie), laboratory technicians (Denise Morin and Nadia Mior), nutritionists (Caroline Benoit and Henriette Langlais), MR team (Sylvie Masson, Suzanne Castonguay, Marie-Josée Morin, Caroline Mérette) and cardio nurses (Jessica Blackburn, Mélanie Gagné, Jeannine Landry, Catherine Lavoie, Lisa Pageau, Réjean Savard, France Tremblay, Jacynthe Tremblay). We also thank Dr Jean Mathieu for the medical follow-up of participants in whom we detected any medically relevant abnormalities; Manon Bernard for designing and managing our online database; Dr Rosanne Aleong for her assistance in coordinating the project; Dr Elizabeth Page-Gould and Dr Melissa Pangelinan for their assistance on statistical analyses and Ms Katie Goodwin for her assistance in semiautomated delineations of visceral fat. TP, ZP and DHS had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. This work was supported by the Saguenay Youth Study project, which is funded by the Canadian Institutes of Health Research (TP, ZP), Heart and Stroke Foundation of Quebec (ZP) and the Canadian Foundation for Innovation (ZP). DHS is supported by a doctoral grant from the Alzheimer Society of Canada.
Author contributions
Study concept and design: Paus and Pausova; acquisition of data: Leonard, Perron, Richer, Syme, Veillette, Pausova and Paus; analysis and interpretation of data: Schwartz, Paus and Pausova; drafting of the manuscript: Schwartz; critical revision of the manuscript for important intellectual content: Paus and Pausova; obtained funding: Paus and Pausova; administrative, technical or material support: Leonard, Perron, Richer, Syme, Veillette, Pausova and Paus; and study supervision: Paus and Pausova.
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Schwartz, D., Leonard, G., Perron, M. et al. Visceral fat is associated with lower executive functioning in adolescents. Int J Obes 37, 1336–1343 (2013). https://doi.org/10.1038/ijo.2013.104
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DOI: https://doi.org/10.1038/ijo.2013.104
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