Fructose decreases physical activity and increases body fat without affecting hippocampal neurogenesis and learning relative to an isocaloric glucose diet

Catarina Rendeiro; Ashley M. Masnik; Jonathan G. Mun; Kristy Du; Diana Clark; Ryan N. Dilger; Anna C. Dilger; Justin S. Rhodes

doi:10.1038/srep09589

journal article Open Access Apr 20, 2015

Fructose decreases physical activity and increases body fat without affecting hippocampal neurogenesis and learning relative to an isocaloric glucose diet

Catarina Rendeiro Ashley M. Masnik Jonathan G. Mun

Kristy Du Diana Clark Ryan N. Dilger Anna C. Dilger Justin S. Rhodes

Scientific Reports Vol. 5 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep09589

Abstract

AbstractRecent evidence suggests that fructose consumption is associated with weight gain, fat deposition and impaired cognitive function. However it is unclear whether the detrimental effects are caused by fructose itself or by the concurrent increase in overall energy intake. In the present study we examine the impact of a fructose diet relative to an isocaloric glucose diet in the absence of overfeeding, using a mouse model that mimics fructose intake in the top percentile of the USA population (18% energy). Following 77 days of supplementation, changes in body weight (BW), body fat, physical activity, cognitive performance and adult hippocampal neurogenesis were assessed. Despite the fact that no differences in calorie intake were observed between groups, the fructose animals displayed significantly increased BW, liver mass and fat mass in comparison to the glucose group. This was further accompanied by a significant reduction in physical activity in the fructose animals. Conversely, no differences were detected in hippocampal neurogenesis and cognitive/motor performance as measured by object recognition, fear conditioning and rotorod tasks. The present study suggests that fructoseper se, in the absence of excess energy intake, increases fat deposition and BW potentially by reducing physical activity, without impacting hippocampal neurogenesis or cognitive function.

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References

60

[1]

Bray, G. A., Nielsen, S. J. & Popkin, B. M. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr 79, 537–543 (2004). 10.1093/ajcn/79.4.537

[2]

Vos, M. B., Kimmons, J. E., Gillespie, C., Welsh, J. & Blanck, H. M. Dietary fructose consumption among US children and adults: the Third National Health and Nutrition Examination Survey. Medscape J Med 10, 160 (2008).

[3]

Marriott, B. P., Cole, N. & Lee, E. National estimates of dietary fructose intake increased from 1977 to 2004 in the United States. J Nutr 139, 1228S–1235S (2009). 10.3945/jn.108.098277

[4]

Sun, S. Z., Anderson, G. H., Flickinger, B. D., Williamson-Hughes, P. S. & Empie, M. W. Fructose and non-fructose sugar intakes in the US population and their associations with indicators of metabolic syndrome. Food Chem Toxicol 49, 2875–2882 (2011). 10.1016/j.fct.2011.07.068

[5]

Rizkalla, S. W. Health implications of fructose consumption: A review of recent data. Nutr Metab (Lond) 7, 82 (2010). 10.1186/1743-7075-7-82

[6]

Stanhope, K. L., Schwarz, J. M. & Havel, P. J. Adverse metabolic effects of dietary fructose: results from the recent epidemiological, clinical and mechanistic studies. Curr Opin Lipidol 24, 198–206 (2013). 10.1097/mol.0b013e3283613bca

[7]

Metabolic Effects of Fructose and the Worldwide Increase in Obesity

Luc Tappy, Kim-Anne Lê

Physiological Reviews 2010 10.1152/physrev.00019.2009

[8]

Ebbeling, C. B. et al. A randomized trial of sugar-sweetened beverages and adolescent body weight. N Engl J Med 367, 1407–1416 (2012). 10.1056/nejmoa1203388

[9]

de Ruyter, J. C., Katan, M. B., Kuijper, L. D., Liem, D. G. & Olthof, M. R. The effect of sugar-free versus sugar-sweetened beverages on satiety, liking and wanting: an 18 month randomized double-blind trial in children. PLoS One 8, e78039 (2013). 10.1371/journal.pone.0078039

[10]

Stanhope, K. L. et al. Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest 119, 1322–1334 (2009). 10.1172/jci37385

[11]

Marques-Lopes, I., Ansorena, D., Astiasaran, I., Forga, L. & Martinez, J. A. Postprandial de novo lipogenesis and metabolic changes induced by a high-carbohydrate, low-fat meal in lean and overweight men. Am J Clin Nutr 73, 253–261 (2001). 10.1093/ajcn/73.2.253

[12]

Silbernagel, G. et al. Effects of 4-week very-high-fructose/glucose diets on insulin sensitivity, visceral fat and intrahepatic lipids: an exploratory trial. Br J Nutr 106, 79–86 (2011). 10.1017/s000711451000574x

[13]

Le, K. A. & Tappy, L. Metabolic effects of fructose. Curr Opin Clin Nutr Metab Care 9, 469–475 (2006). 10.1097/01.mco.0000232910.61612.4d

[14]

Chong, M. F., Fielding, B. A. & Frayn, K. N. Mechanisms for the acute effect of fructose on postprandial lipemia. Am J Clin Nutr 85, 1511–1520 (2007). 10.1093/ajcn/85.6.1511

[15]

Stanhope, K. L. et al. Consumption of fructose and high fructose corn syrup increase postprandial triglycerides, LDL-cholesterol and apolipoprotein-B in young men and women. J Clin Endocrinol Metab 96, E1596–1605 (2011). 10.1210/jc.2011-1251

[16]

Samuel, V. T. Fructose induced lipogenesis: from sugar to fat to insulin resistance. Trends Endocrinol Metab 22, 60–65 (2011). 10.1016/j.tem.2010.10.003

[17]

Tappy, L., Le, K. A., Tran, C. & Paquot, N. Fructose and metabolic diseases: new findings, new questions. Nutrition 26, 1044–1049 (2010). 10.1016/j.nut.2010.02.014

[18]

Mayes, P. A. Intermediary metabolism of fructose. Am J Clin Nutr 58, 754S–765S (1993). 10.1093/ajcn/58.5.754s

[19]

Havel, P. J. Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr Rev 63, 133–157 (2005). 10.1111/j.1753-4887.2005.tb00132.x

[20]

Sievenpiper, J. L. et al. Effect of fructose on body weight in controlled feeding trials: a systematic review and meta-analysis. Ann Intern Med 156, 291–304 (2012). 10.7326/0003-4819-156-4-201202210-00007

[21]

Te Morenga, L., Mallard, S. & Mann, J. Dietary sugars and body weight: systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ 346, e7492 (2013). 10.1136/bmj.e7492

[22]

Dolan, L. C., Potter, S. M. & Burdock, G. A. Evidence-based review on the effect of normal dietary consumption of fructose on blood lipids and body weight of overweight and obese individuals. Crit Rev Food Sci Nutr 50, 889–918 (2010). 10.1080/10408398.2010.512990

[23]

Heterogeneous Effects of Fructose on Blood Lipids in Individuals With Type 2 Diabetes

John L. Sievenpiper, Amanda J. Carleton, Sheena Chatha et al.

Diabetes Care 2009 10.2337/dc09-0619

[24]

David Wang, D. et al. Effect of fructose on postprandial triglycerides: a systematic review and meta-analysis of controlled feeding trials. Atherosclerosis 232, 125–133 (2014). 10.1016/j.atherosclerosis.2013.10.019

[25]

Effect of Fructose on Blood Pressure

Vanessa Ha, John L. Sievenpiper, Russell J. de Souza et al.

Hypertension 2012 10.1161/hypertensionaha.111.182311

[26]

Chiu, S. et al. Effect of fructose on markers of non-alcoholic fatty liver disease (NAFLD): a systematic review and meta-analysis of controlled feeding trials. Eur J Clin Nutr 68, 416–423 (2014). 10.1038/ejcn.2014.8

[27]

Stranahan, A. M. et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18, 1085–1088 (2008). 10.1002/hipo.20470

[28]

Sievenpiper, J. L., de Souza, R. J., Kendall, C. W. & Jenkins, D. J. Is fructose a story of mice but not men? J Am Diet Assoc 111, 219–220 (2011). 10.1016/j.jada.2010.12.001

[29]

Ye, X., Gao, X., Scott, T. & Tucker, K. L. Habitual sugar intake and cognitive function among middle-aged and older Puerto Ricans without diabetes. Br J Nutr 106, 1423–1432 (2011). 10.1017/s0007114511001760

[30]

Lakhan, S. E. & Kirchgessner, A. The emerging role of dietary fructose in obesity and cognitive decline. Nutr J 12, 114 (2013). 10.1186/1475-2891-12-114

[31]

Mielke, J. G. et al. A biochemical and functional characterization of diet-induced brain insulin resistance. J Neurochem 93, 1568–1578 (2005). 10.1111/j.1471-4159.2005.03155.x

[32]

Costello, D. A. et al. Brain deletion of insulin receptor substrate 2 disrupts hippocampal synaptic plasticity and metaplasticity. PLoS One 7, e31124 (2012). 10.1371/journal.pone.0031124

[33]

Ross, A. P., Bartness, T. J., Mielke, J. G. & Parent, M. B. A high fructose diet impairs spatial memory in male rats. Neurobiol Learn Mem 92, 410–416 (2009). 10.1016/j.nlm.2009.05.007

[34]

Ross, A. P., Bruggeman, E. C., Kasumu, A. W., Mielke, J. G. & Parent, M. B. Non-alcoholic fatty liver disease impairs hippocampal-dependent memory in male rats. Physiol Behav 106, 133–141 (2012). 10.1016/j.physbeh.2012.01.008

[35]

Hsu, T. M. et al. Effects of sucrose and high fructose corn syrup consumption on spatial memory function and hippocampal neuroinflammation in adolescent rats. Hippocampus [Epub ahead of print] (2014). 10.1002/hipo.22368

[36]

van der Borght, K. et al. Reduced neurogenesis in the rat hippocampus following high fructose consumption. Regul Pept 167, 26–30 (2011). 10.1016/j.regpep.2010.11.002

[37]

AIN-93 Purified Diets for Laboratory Rodents: Final Report of the American Institute of Nutrition Ad Hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet

Philip G Reeves, Forrest H Nielsen, George C Fahey

The Journal of Nutrition 1993 10.1093/jn/123.11.1939

[38]

Zombeck, J. A., Deyoung, E. K., Brzezinska, W. J. & Rhodes, J. S. Selective breeding for increased home cage physical activity in collaborative cross and Hsd:ICR mice. Behav Genet 41, 571–582 (2011). 10.1007/s10519-010-9425-2

[39]

Koteja, P., Swallow, J. G., Carter, P. A. & Garland, T. Jr. Energy cost of wheel running in house mice: implications for coadaptation of locomotion and energy budgets. Physiol Biochem Zool 72, 238–249 (1999). 10.1086/316653

[40]

Koteja, P., Carter, P. A., Swallow, J. G. & Garland, T. Jr. Food wasting by house mice: variation among individuals, families and genetic lines. Physiol Behav 80, 375–383 (2003). 10.1016/j.physbeh.2003.09.001

[41]

Starr, M. E. & Saito, H. Age-related increase in food spilling by laboratory mice may lead to significant overestimation of actual food consumption: implications for studies on dietary restriction, metabolism and dose calculations. J Gerontol A Biol Sci Med Sci 67, 1043–1048 (2012). 10.1093/gerona/gls009

[42]

Ravussin, Y., Gutman, R., LeDuc, C. A. & Leibel, R. L. Estimating energy expenditure in mice using an energy balance technique. Int J Obes (Lond) 37, 399–403 (2013). 10.1038/ijo.2012.105

[43]

Guo, J. & Hall, K. D. Predicting changes of body weight, body fat, energy expenditure and metabolic fuel selection in C57BL/6 mice. PLoS One 6, e15961 (2011). 10.1371/journal.pone.0015961

[44]

Clark, P. J. et al. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 155, 1048–1058 (2008). 10.1016/j.neuroscience.2008.06.051

[45]

van Praag, H., Kempermann, G. & Gage, F. H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2, 266–270 (1999). 10.1038/6368

[46]

White, J. S. Challenging the fructose hypothesis: new perspectives on fructose consumption and metabolism. Adv Nutr 4, 246–256 (2013). 10.3945/an.112.003137

[47]

Laughlin, M. R. et al. Clinical research strategies for fructose metabolism. Adv Nutr 5, 248–259 (2014). 10.3945/an.113.005249

[48]

Kaiser, K. A., Shikany, J. M., Keating, K. D. & Allison, D. B. Will reducing sugar-sweetened beverage consumption reduce obesity? Evidence supporting conjecture is strong, but evidence when testing effect is weak. Obes Rev 14, 620–633 (2013). 10.1111/obr.12048

[49]

Ervin, R. B., Kit, B. K., Carroll, M. D. & Ogden, C. L. Consumption of added sugar among U.S. children and adolescents, 2005–2008. NCHS Data Brief 87, 1–8 (2012).

[50]

Bremer, A. A. et al. Fructose-fed rhesus monkeys: a nonhuman primate model of insulin resistance, metabolic syndrome and type 2 diabetes. Clin Transl Sci 4, 243–252 (2011). 10.1111/j.1752-8062.2011.00298.x

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Published: Apr 20, 2015
Vol/Issue: 5(1)
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Catarina Rendeiro, Ashley M. Masnik, Jonathan G. Mun, et al. (2015). Fructose decreases physical activity and increases body fat without affecting hippocampal neurogenesis and learning relative to an isocaloric glucose diet. Scientific Reports, 5(1). https://doi.org/10.1038/srep09589

Fructose decreases physical activity and increases body fat without affecting hippocampal neurogenesis and learning relative to an isocaloric glucose diet

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