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Metabolic and behavioural effects of sucrose and fructose/glucose drinks in the rat

Abstract

Purpose

Overconsumption of sugar-sweetened beverages, in particular carbonated soft drinks, promotes the development of overweight and obesity and is associated with metabolic disturbances, including intrahepatic fat accumulation and metabolic syndrome. One theory proposes that drinks sweetened with high-fructose corn syrup are particularly detrimental to health, as they contain fructose in its ‘free’ monosaccharide form. This experiment tested whether consuming ‘free’ fructose had a greater impact on body weight and metabolic abnormalities than when consumed ‘bound’ within the disaccharide sucrose.

Methods

Male Hooded Wistar rats were given free access for 56 days to 10% sucrose (Group Suc), 10%, 50/50 fructose/glucose (Group FrucGluc) or water control drinks (Group Control), plus chow. Caloric intake and body weights were measured throughout the protocol, and the following metabolic indices were determined between days 54 and 56: serum triglycerides, liver triglycerides, retroperitoneal fat and oral glucose tolerance.

Results

Animals with access to sugar beverages consumed 20% more calories, but did not show greater weight gain than controls. Nevertheless, they developed larger abdominal fat pads, higher triglyceride levels and exhibited impaired insulin/glucose homeostasis. Comparison of the two sugars revealed increased fasting glycaemia in the FrucGluc group, but not in Suc group, whereas the Suc group was more active in an open field.

Conclusions

A metabolic profile indicating increased risk of diabetes mellitus and cardiovascular disease was observed in animals given access to sugar-sweetened beverages. Notably, ‘free’ fructose disrupted glucose homeostasis more than did ‘bound’ fructose, thus posing a greater risk of progression to type 2 diabetes.

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References

  1. Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI, Kang DH et al (2007) Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr 86(4):899–906

    CAS  Google Scholar 

  2. Malik VS, Sculze MB, Hu FB (2006) Intake of sugar-sweetened beverages and weight gain: a systematic review. Am J Clin Nutr 84(2):274–288

    CAS  Google Scholar 

  3. Malik VS, Willett WC, Hu FB (2009) Sugar-sweetened beverages and BMI in children and adolescents: reanalyses of a meta-analysis. Am J Clin Nutr 89(1):438–439

    Article  CAS  Google Scholar 

  4. Vartanian LR, Schwartz MB, Brownell KD (2007) Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis. Am J Public Health 97(4):667–675

    Article  Google Scholar 

  5. Dhingra R (2007) Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community. Circulation 116(5):480–488

    Article  Google Scholar 

  6. Yoo S, Nicklas T, Baranowski T, Zakeri IF, Yang SJ, Srinivasan SR, Berenson GS et al (2004) Comparison of dietary intakes associated with metabolic syndrome risk factors in young adults: the Bogalusa heart study. Am J Clin Nutr 80(4):841–848

    CAS  Google Scholar 

  7. Montonen J, Jarvinen R, Knekt P, Heliovaara M, Reunanen A (2007) Consumption of sweetened beverages and intakes of fructose and glucose predict type 2 diabetes occurrence. J Nutr 137(6):1447–1454

    CAS  Google Scholar 

  8. Schulze MB, Manson JE, Ludwig DS, Colditz GA, Stampfer MJ, Willett WC et al (2004) Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. JAMA 292:927–934

    Article  CAS  Google Scholar 

  9. Assy N, Nasser G, Kamayse I, Nseir W, Nebiashvili Z, Djibre A et al (2008) Soft drink consumption linked with fatty liver in the absence of traditional risk factors. Can J Gastroenterol 22(10):811–816

    Google Scholar 

  10. Ouyang X, Cirillo P, Sautin Y, McCall S, Brushette JL, Diehl AM et al (2008) Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J Hepatol 48(6):993–999

    Article  CAS  Google Scholar 

  11. Fung TT, Malik V, Rexrode KM, Manson JE, Willett WC, Hu FB (2009) Sweetened beverage consumption and risk of coronary heart disease in women. Am J Clin Nutr 89(4):1037–1042

    Article  CAS  Google Scholar 

  12. Foreshee RA, Storey ML, Allison DB, Glinsmann WH, Hein GL, Lineback DR et al (2007) A critical examination of the evidence relating high fructose corn syrup and weight gain. Crit Rev Food Sci Nutr 47(6):561–582

    Article  Google Scholar 

  13. Havel PJ (2005) Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr Rev 63(5):133–157

    Article  Google Scholar 

  14. Tappy L, Le KA (2010) Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 90(1):23–46

    Article  CAS  Google Scholar 

  15. Almiron-Roig E, Drewnowski A (2003) Hunger, thirst, and energy intakes following consumption of caloric beverages. Physiol Behav 79(4–5):767–773

    Article  CAS  Google Scholar 

  16. DellaValle DM, Roe LS, Rolls BJ (2005) Does the consumption of caloric and non-caloric beverages with a meal affect energy intake? Appetite 44(2):187–193

    Article  Google Scholar 

  17. DiMeglio DP, Mattes RD (2000) Liquid versus solid carbohydrate: effects on food intake and body weight. Int J Obes 24(6):794–800

    Article  CAS  Google Scholar 

  18. Bray GA (2004) The epidemic of obesity and changes in food intake: the fluoride hypothesis. Phys Behav 82(1):115–121

    Article  CAS  Google Scholar 

  19. Bocarsly ME, Powelle ES, Avena NM, Hoebel BG (2010) High-fructose corn syrup causes characteristics of obesity in rats: increased body weight, body fat and triglyceride levels. Pharmacol Biochem Behav 97(1):101–106

    Article  CAS  Google Scholar 

  20. Sanchez-Lozada LG, Mu W, Roncal C, Sautin YY, Abdelmalek M, Reungjui S et al (2010) Comparison of free fructose and glucose to sucrose in the ability to cause fatty liver. Eur J Nutr 49(1):1–9

    Article  CAS  Google Scholar 

  21. Cacho J, Sevillano J, Casto De, Herrera E, Ramos MP (2008) Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Spraque-Dawley rats. Am J Physiol-Endoc M 295(5):E1269–E1276

    CAS  Google Scholar 

  22. Van Nieuwenhuijzen PS, Li KM, Hunt GE, McGregor IS (2009) Weekly gamma-hydroxybutyrate exposure sensitizes locomotor hyperactivity to low-dose 3, 4-methylenedioxymethamphetamine in rats. Neuropsychobiology 60(3–4):195–203

    Article  Google Scholar 

  23. Moretti M, de Souza AG, de Andrade VM, Romao PRT, Gavioli EC (2010) Emotional behavior in middle-ages rats: implications for geriatric psychopathologies. Physiol Behav 102(1):115–120

    Article  Google Scholar 

  24. Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and it’s complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15:539–553

    Article  CAS  Google Scholar 

  25. Sclafani A (1987) Carbohydrate taste, appetite, and obesity—an overview. Neurosci Biobehav Rev 11:131–153

    Article  CAS  Google Scholar 

  26. Kumari D, Nair N, Ranveer SB (2011) Effect of dietary zinc deficiency on testes of Wistar rats: morphometric and cell quantification studies. J Trace Elem Med Bio 25(1):47–53

    Article  CAS  Google Scholar 

  27. Esteban-Pretel G, Marin MP, Cabezuelo F, Moreno V, Renau-Piqueras J, Timodena J et al (2010) Vitamin A deficiency increases protein catabolism and induces urea cycle enzymes in rats. J Nutr 140(4):792–798

    Article  CAS  Google Scholar 

  28. Landenburg L (2006) Feast or famine: the sympathetic nervous system response to nutrient intake. Cell Mol Neurobiol 26:497–508

    Google Scholar 

  29. Boakes RA, Boot B, Clarke JV, Carver A (2000) Comparing albino and hooded Wistar rats of both sexes on a range of behavioral and learning tasks. Psychobiology 28(3):339–359

    Google Scholar 

  30. Creel D (1980) Inappropriate use of albino animals as models in research. Pharmacol Biochem Behav 12(6):969–977

    Article  CAS  Google Scholar 

  31. Nakagawa T, Hu HB, Zharikov S, Tuttle KR, Short RA, Glushkova O et al (2006) A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol-Renal 290(3):F625–F631

    Article  CAS  Google Scholar 

  32. Stanhope KL, Schwarz JM, Keim NL, Griffen SC, Bremer AA, Graham JL et al (2009) Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest 119(5):1322–1334

    Article  CAS  Google Scholar 

  33. Swarbrick MM, Stanhope KL, Elliott SS, Graham JL, Krauss RM, Christiansen MP et al (2008) Consumption of fructose-sweetened beverages for 10 weeks increases postprandial triacylglycerol and apolipoprotein-B concentrations in overweight and obese women. BJN 100(5):947–952

    Article  CAS  Google Scholar 

  34. Teff KL, Grudziak J, Townsend RR, Dunn TN, Grant RW, Adams SH et al (2009) Endocrine and metabolic effects of consuming fructose and glucose-sweetened beverages with meals in obese men and women: influence of insulin resistance on plasma triglyceride responses. J Clin Endocr Metab 94:1562–1569

    Article  CAS  Google Scholar 

  35. Despres JP, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444(7121):881–887

    Article  CAS  Google Scholar 

  36. Abdul-Ghani MA, Tripathy D, DeFronzo RA (2006) Contributions of beta-cell dysfunction and insulin resistance to the pathogenesis of impaired glucose tolerance and impaired fasting glucose. Diabetes Care 29(5):1130–1139

    Article  CAS  Google Scholar 

  37. Unwin N, Shaw J, Zimmet P, Alberti KGMM (2002) Impaired glucose tolerance and impaired fasting glycaemia: the current status on definition and intervention. Diabet Med 19:708–723

    Article  CAS  Google Scholar 

  38. Faeh D, Minehira K, Schwarz JM, Periasami R, Seongsu P, Tappy L (2005) Effect of fructose overfeeding and fish oil administration on hepatic de novo lipogenesis and insulin sensitivity in healthy men. Diabetes 54(7):1907–1913

    Article  CAS  Google Scholar 

  39. Le KA, Ith M, Kreis R, Faeh D, Bortolotti M, Tan C et al (2009) Fructose overconsumption causes dyslipidemia and ectopic lipid deposition in healthy subjects with and without a family history of type 2 diabetes. Am J Clin Nutr 89(6):1760–1765

    Article  CAS  Google Scholar 

  40. Ellwood KC, Michaelis OE, Hallfrisch JG, Odorisio TM, Cataland S (1983) Blood insulin, glucose, fructose and gastric-inhibitory polypeptide levels in carbohydrate-sensitive and normal men given a sucrose or invert sugar tolerance-test. J Nutr 113(9):1732–1736

    CAS  Google Scholar 

  41. Shreeve WW, Hoshi M, Kikkawa R (1971) Insulin responses to ingested sucrose vs fructose in obese patients. Diabetes 20(suppl):377

    Google Scholar 

  42. Lee VM, Szepesi B, Hansen RJ (1986) Absence of a generalized disaccharide effect in adult female rats. J Nutr 116(8):1555–1560

    CAS  Google Scholar 

  43. Michaelis OE, Nace CS, Szepesi B (1975) Demonstration of a specific metabolic effect of dietary disaccharides in rat. J Nutr 105(9):1186–1191

    CAS  Google Scholar 

  44. Lim SJ, Mietus-Snyder M, Valente A, Schwarz J, Lustig RH (2010) The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol 7(5):251–264

    Article  CAS  Google Scholar 

  45. Ruxton CHS, Gardner EJ, McNulty HM (2010) Is sugar consumption detrimental to health? A review of the evidence 1995–2006. Crit Rev Food Sci 50(1):1–19

    Article  CAS  Google Scholar 

  46. Prinz RJ, Riddle DB (1986) Associations between nutrition and behavior in 5-year-old children. Nurt rev 44 (S3):151–158

    Google Scholar 

  47. Prinz RJ, Roberts WA, Hantman E (1980) Dietary correlates of hyperactive behavior in children. J Consult Clin Psychol 48(6):760–769

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Iain McGregor for his advice on behavioural testing and for generously allowing us to use his equipment for this purpose.

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Correspondence to Robert A. Boakes.

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Sheludiakova, A., Rooney, K. & Boakes, R.A. Metabolic and behavioural effects of sucrose and fructose/glucose drinks in the rat. Eur J Nutr 51, 445–454 (2012). https://doi.org/10.1007/s00394-011-0228-x

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  • DOI: https://doi.org/10.1007/s00394-011-0228-x

Keywords

  • Metabolic syndrome
  • Sucrose
  • Fructose
  • Glucose
  • High-fructose corn syrup
  • Insulin resistance
  • Glucose tolerance
  • Triglycerides
  • Behaviour