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Endocrine and Metabolic Effects of Consuming Beverages Sweetened with Fructose, Glucose, Sucrose, Or High-Fructose Corn Syrup1–5

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Endocrine and Metabolic Effects of Consuming Beverages Sweetened with Fructose, Glucose, Sucrose, Or High-Fructose Corn Syrup1–5 Endocrine and metabolic effects of consuming beverages sweetened with fructose, glucose, sucrose, or high-fructose corn syrup1–5 Kimber L Stanhope and Peter J Havel ABSTRACT systematic review of the relation between sugar-sweetened bev- Our laboratory has investigated 2 hypotheses regarding the effects of erage consumption and risk of weight gain and concluded that the fructose consumption: 1) the endocrine effects of fructose consump- evidence indicates that increased consumption of sugar- Downloaded from tion favor a positive energy balance, and 2) fructose consumption sweetened beverages is associated with weight gain. We have promotes the development of an atherogenic lipid profile. In previ- hypothesized that fructose consumption could promote weight ous short- and long-term studies, we showed that consumption of gain because it does not stimulate insulin secretion or leptin fructose-sweetened beverages with 3 meals results in lower 24-h production by adipose tissue (2, 3). Because leptin production is plasma concentrations of glucose, insulin, and leptin in humans than regulated by insulin-mediated glucose metabolism (6–8) and does consumption of glucose-sweetened beverages. We have also ingestion of fructose does not result in meal-related increases of www.ajcn.org tested whether prolonged consumption of high-fructose diets leads plasma glucose or insulin concentrations, we hypothesized that to increased caloric intake or decreased energy expenditure, thereby meals accompanied by fructose-sweetened beverages would re- contributing to weight gain and obesity. Results from a study con- sult in reduced circulating leptin concentrations when compared ducted in rhesus monkeys produced equivocal results. Carefully with glucose-sweetened beverages. We compared leptin concen- at Univ of California-Davis on December 8, 2008 controlled and adequately powered long-term studies are needed to trations over 2 separate 24-h periods in 12 normal-weight young address these hypotheses. In both short- and long-term studies, we women who consumed fructose- or glucose-sweetened bever- showed that consumption of fructose-sweetened beverages substan- ages with meals. Consumption of fructose-sweetened beverages tially increases postprandial triacylglycerol concentrations com- at 30% of energy requirements with 3 meals resulted in lower pared with glucose-sweetened beverages. In the long-term studies, 24-h circulating concentrations of glucose, insulin, and leptin apolipoprotein B concentrations were also increased in subjects con- and resulted in less postprandial suppression of ghrelin after each suming fructose, but not in those consuming glucose. Data from a meal compared with consumption of glucose-sweetened bever- short-term study comparing consumption of beverages sweetened ages (9). In a second short-term study comparing fructose- and with fructose, glucose, high-fructose corn syrup, and sucrose suggest glucose-sweetened beverages (30% of energy requirements), that high-fructose corn syrup and sucrose increase postprandial tri- acylglycerol to an extent comparable with that induced by 100% 1 From the Department of Molecular Biosciences, School of Veterinary fructose alone. Increased consumption of fructose-sweetened bever- Medicine, University of California, Davis, and the Department of Nutrition, ages along with increased prevalence of obesity, metabolic syndrome, University of California, Davis. and type 2 diabetes underscore the importance of investigating the 2 Presented at the American Society for Nutrition Public Information metabolic consequences of fructose consumption in carefully con- Committee symposium “High-Fructose Corn Syrup (HFCS): Everything trolled experiments. Am J Clin Nutr 2008;88(suppl):1733S–7S. You Wanted to Know, but Were Afraid to Ask,” held at Experimental Biol- ogy 2007 in Washington, DC, 30 April 2007. 3 The contents of this manuscript are solely the responsibility of the INTRODUCTION authors and do not necessarily represent the official view of the National Center for Research Resources (NCRR) or the National Institutes of Health Some investigators have proposed that increased fructose con- (NIH). Information on NCRR is available at http://www.ncrr.nih.gov/. In- sumption may be related to the current epidemics of obesity and formation on Re-engineering the Clinical Research Enterprise can be obtained metabolic syndrome (1–4). The purpose of this article is to re- from http://nihroadmap.nih.gov/clinicalresearch/overview-translational.asp. view some of our recent work investigating 2 hypotheses: 1) 4 Supported in part with research funding from the American Diabetes fructose consumption promotes a state of positive energy bal- Association; the US Department of Agriculture; the National Institutes of ance, and 2) fructose consumption favors the development of an Health (HL-075675, HL-091333, AT-002599, AT-002993, AT-003545, and atherogenic lipoprotein profile. DK-58108); Pepsico, Inc, Purchase, NY; the California National Primate Research Center (RR-00169); and the UC Davis Clinical and Translational Science Center (grant number UL1 RR024146) from the NCRR, a compo- FRUCTOSE CONSUMPTION AND ENERGY BALANCE nent of the NIH and the NIH Roadmap for Medical Research. 5 Address reprint requests to PJ Havel, Department of Molecular Bio- Consumption of dietary fructose has increased in conjunction sciences, School of Veterinary Medicine, University of California, Davis, with rising intake of fructose-containing sugars, largely in the One Shields Avenue, Davis, CA 95616. E-mail: [email protected]. form of sugar-sweetened beverages. Malik et al (5) conducted a doi: 10.3945/ajcn.2008.25825D. Am J Clin Nutr 2008;88(suppl):1733S–7S. Printed in USA. © 2008 American Society for Nutrition 1733S 1734S STANHOPE AND HAVEL A B 0.0 Glucose 4 Fructose * -2.5 3 * -5.0 2 * ** * -7.5 1 * Body Weight (kg) ** ∆ 0 -10.0 ** in energy expenditure (%) -1 ∆ -12.5 ** -3 mo 0 mo 3 mo 6 mo 9 mo 12 mo 3 mo 6 mo 12 mo 3 mo 6 mo 12 mo Weeks Glucosea Fructose b FIGURE 1. (A) Changes (⌬) in body weight from baseline in male rhesus monkeys consuming 380 kcal/d of fructose- or glucose-sweetened beverage for 1y(n ҃ 8/group). Baseline body weights were not significantly different. Data are mean Ȁ SEM (analysis described in Figure 2). Responses to each sugar over Downloaded from time were analyzed by repeated-measures ANOVA (SAS version 9.1; SAS Institute Inc, Cary, NC) with contrasts comparing weights at 3, 6, and 12 mo to baseline weights (*P 0.05, **P 0.01). Comparison of fructose and glucose response analyzed by 2-factor repeated measures ANOVA: sugar ҂ time interaction ҃ NS. (B) Percentage change in energy expenditure (measured by indirect calorimetry) from baseline in rhesus monkeys after 3, 6, and 12 mo of consuming 380 kcal/d of fructose- or glucose-sweetened beverages. Baseline energy expenditure was not significantly different between groups. Data are mean Ȁ SEM. Responses to each sugar over time were analyzed by repeated-measures, one-factor ANOVA (aP 0.05; bP 0.01 with Greenhouse-Geisser Epsilon correction with contrasts comparing energy expenditure at 3, 6, and 12 mo to baseline energy expenditure (*P 0.05, **P 0.01). Comparison of fructose and glucose response analyzed by two-factor repeated measure ANOVA: sugar ҂ time interaction ҃ NS. n ҃ 6/group. www.ajcn.org meal-induced insulin secretion was attenuated and 24-h circu- FRUCTOSE AND LONG-TERM ENERGY BALANCE IN lating leptin profiles were reduced in both overweight and obese RHESUS MONKEYS at Univ of California-Davis on December 8, 2008 men and overweight and obese women (10). Fructose-sweetened We conducted a 12-mo study in 16 adult male rhesus monkeys beverage consumption also reduced the percent (proportional) (Macaca mulatta) to determine whether prolonged consumption change of leptin concentrations between the morning nadir and of a diet high in energy from fructose would lead to greater the late night peak (9, 10). Results from a clinical study investi- weight gain via increased caloric intake, decreased energy ex- gating weight and body fat loss during an ad libitum, low-fat, penditure, or both compared with a diet high in glucose. Monkeys high-carbohydrate diet suggest an association between the am- (n ҃ 8/group) were fed an ad libitum standard chow diet supple- plitude of the diurnal leptin pattern and long-term energy balance mented with either glucose- or fructose-sweetened beverages (11). (100 g sugar/d). The 2 groups of monkeys consumed an average In long-term comparisons of fructose- and glucose-sweetened of 43.8 Ȁ 4.1% and 41.5 Ȁ 2.7% of total energy as glucose and beverages (25% of energy requirements consumed with meals), fructose consumption resulted in significant reductions in the fructose, respectively, during the 12-mo intervention period. 24-h areas under the curve for glucose, insulin, and leptin (12), Monkeys fed fructose beverages gained significant amounts of whereas consumption of glucose did not. These results indicate weight at 3 and 6 mo compared with their baseline weights, that reductions of insulin secretion and attenuated 24-h leptin whereas the animals consuming glucose did not. However, profiles observed in the short-term studies are not transient, but weight gain was not significantly different between the 2 groups are maintained during long-term fructose consumption. by the end of the study at 12 mo (Figure 1A). Insulin and leptin function as key endocrine signals to the Food and beverage intake was measured daily, and differences central nervous system in the long-term regulation of energy in energy intake did not account for the weight gain in monkeys balance (13, 14). Therefore, prolonged consumption of diets high fed fructose-sweetened beverages during the first 6 mo of the in energy from fructose could lead to increased caloric intake or study. Differences in energy expenditure between the 2 groups of decreased caloric expenditure, contributing to weight gain and animals may have explained the early differences in body weight obesity as a result of reduced insulin and leptin signaling in the gain (Figure 1B).
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