No differential effect of beverages sweetened with fructose, high-fructose corn syrup, or glucose on systemic or adipose tissue inflammation in normal-weight to obese adults: A randomized controlled trial

American Journal of Clinical Nutrition

Volumn 104, Issue 2, 2016, Pages 306-314

  Kuzma, Jessica N ^a,d   Cromer, Gail ^a   Hagman, Derek K ^a   Breymeyer, Kara L ^b   Roth, Christian L ^e   Foster Schubert, Karen E ^c   Holte, Sarah E ^a   Weigle, David S ^c   Kratz, Mario ^a,c,d  

^a Division of Public Health Sciences   (United States)

^b USA   (United States)

^c Division of Metabolism Endocrinology and Nutrition   (United States)

^d Division of Epidemiology Human Genetics Environmental Sciences   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Adipose tissue inflammation; Fructose; Intestinal permeability; Sugar sweetened beverages; Systemic inflammation

Indexed keywords

ADIPONECTIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CORN SYRUP; FATTY ACID; FETUIN A; FRUCTOSE; GAMMA INTERFERON; GLUCOSE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTULOSE; LIPOPOLYSACCHARIDE BINDING PROTEIN; MANNITOL; MONOCYTE CHEMOTACTIC PROTEIN 1; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZONULIN; HEXOSE; IL6 PROTEIN, HUMAN; SWEETENING AGENT;

ABDOMINAL SUBCUTANEOUS FAT; ADIPOSE TISSUE; ADULT; AGED; ANALYTICAL PARAMETERS; ARTICLE; BEVERAGE; BODY WEIGHT; CALORIC INTAKE; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DRINKING; FEMALE; GENE EXPRESSION; GLUCOSE INTAKE; HEREDITARY FRUCTOSE INTOLERANCE; HUMAN; HUMAN TISSUE; INTESTINE MUCOSA PERMEABILITY; LACTULOSE MANNITOL RATIO; MALE; OBESITY; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SUGAR SWEETENED BEVERAGE; SYSTEMIC CIRCULATION; BLOOD; BODY MASS; DIET; DOUBLE BLIND PROCEDURE; FEEDING BEHAVIOR; INFLAMMATION; METABOLISM; MIDDLE AGED; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL; REFERENCE VALUE; YOUNG ADULT;

ADIPONECTIN; ADIPOSE TISSUE; ADULT; BEVERAGES; BODY MASS INDEX; C-REACTIVE PROTEIN; DIET; DOUBLE-BLIND METHOD; FEEDING BEHAVIOR; FEMALE; FRUCTOSE; GLUCOSE; HEXOSES; HIGH FRUCTOSE CORN SYRUP; HUMANS; INFLAMMATION; INTERLEUKIN-6; MALE; MIDDLE AGED; OBESITY; REFERENCE VALUES; SWEETENING AGENTS; YOUNG ADULT;

EID: 84980413778     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.115.129650     Document Type: Article

References (32)

1. Xi B, Huang Y, Reilly KH, Li S, Zheng R, Barrio-Lopez MT, Martinez-Gonzalez MA, Zhou D. Sugar-sweetened beverages and risk of hypertension and CVD: a dose-response meta-analysis. Br J Nutr 2015;113:709-17.
2. Fung TT, Malik V, Rexrode KM, Manson JE, Willett WC, Hu FB. Sweetened beverage consumption and risk of coronary heart disease in women. Am J Clin Nutr 2009;89:1037-42.
3. Malik VS, Popkin BM, Bray GA, Despres JP, Willett WC, Hu FB. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care 2010;33:2477-83.
4. Kosova EC, Auinger P, Bremer AA. The relationships between sugarsweetened beverage intake and cardiometabolic markers in young children. J Acad Nutr Diet 2013;113:219-27.
5. Schulze MB, Hoffmann K, Manson JE, Willett WC, Meigs JB, Weikert C, Heidemann C, Colditz GA, Hu FB. Dietary pattern, inflammation, and incidence of type 2 diabetes in women. Am J Clin Nutr 2005;82:675-84.
6. Kavanagh K, Wylie AT, Tucker KL, Hamp TJ, Gharaibeh RZ, Fodor AA, Cullen JM. Dietary fructose induces endotoxemia and hepatic injury in calorically controlled primates. Am J Clin Nutr 2013;98:349-57.
7. Bergheim I, Weber S, Vos M, Kramer S, Volynets V, Kaserouni S, McClain CJ, Bischoff SC. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol 2008;48:983-92.
8. Aeberli I, Hochuli M, Gerber PA, Sze L, Murer SB, Tappy L, Spinas GA, Berneis K. Moderate amounts of fructose consumption impair insulin sensitivity in healthy young men: a randomized controlled trial. Diabetes Care 2013;36:150-6.
9. Stanhope KL, Schwarz JM, Keim NL, Griffen SC, Bremer AA, Graham JL, Hatcher B, Cox CL, Dyachenko A, Zhang W, 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 2009;119:1322-34.
10. Spruss A, Kanuri G, Wagnerberger S, Haub S, Bischoff SC, Bergheim I. Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology 2009;50:1094-104.
11. EkstromM, HalleM, Bjessmo S, Liska J, Kolak M, Fisher R, Eriksson P, Tornvall P. Systemic inflammation activates the nuclear factor-kappaB regulatory pathway in adipose tissue. Am J Physiol Endocrinol Metab 2010;299:E234-40.
12. Schwarz JM, Noworolski SM, Wen MJ, Dyachenko A, Prior JL, Weinberg ME, Herraiz LA, Tai VW, Bergeron N, Bersot TP, et al. Effect of a high-fructose weight-maintaining diet on lipogenesis and liver fat. J Clin Endocrinol Metab 2015;100:2434-42.
13. Stefan N, Hennige AM, Staiger H, Machann J, Schick F, Krober SM, Machicao F, Fritsche A, Haring HU. Alpha2-Heremans-Schmid glycoprotein/fetuin-A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care 2006;29:853-7.
14. Haukeland JW, Dahl TB, Yndestad A, Gladhaug IP, Loberg EM, Haaland T, Konopski Z, Wium C, Aasheim ET, Johansen OE, et al. Fetuin A in nonalcoholic fatty liver disease: in vivo and in vitro studies. Eur J Endocrinol 2012;166:503-10.
15. Pal D, Dasgupta S, Kundu R, Maitra S, Das G, Mukhopadhyay S, Ray S, Majumdar SS, Bhattacharya S. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat Med 2012;18:1279-85.
16. Kuzma JN, Cromer G, Hagman DK, Breymeyer KL, Roth CL, Foster-Schubert KE, Holte SE, Callahan HS, Weigle DS, Kratz M. No difference in ad libitum energy intake in healthy men and women consuming beverages sweetened with fructose, glucose, or high-fructose corn syrup: a randomized trial. Am J Clin Nutr 2015;102:1373-80.
17. Keller J, Franke A, Storr M, Wiedbrauck F, Schirra J. [Clinically relevant breath tests in gastroenterological diagnostics-recommendations of the German Society for Neurogastroenterology and Motility as well as the German Society for Digestive and Metabolic Diseases.] Z Gastroenterol 2005;43:1071-90.
18. Mifflin MD, St Jeor ST, Hill LA, Scott BJ, Daugherty SA, Koh YO. A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr 1990;51:241-7.
19. Blair SN, Haskell WL, Ho P, Paffenbarger RS Jr., Vranizan KM, Farquhar JW, Wood PD. Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. Am J Epidemiol 1985;122:794-804.
20. Dastych M, Dastych M Jr., Novotna H, Cihalova J. Lactulose/mannitol test and specificity, sensitivity, and area under curve of intestinal permeability parameters in patients with liver cirrhosis and Crohn's disease. Dig Dis Sci 2008;53:2789-92.
21. Campbell KL, Makar KW, Kratz M, Foster-Schubert KE, McTiernan A, Ulrich CM. A pilot study of sampling subcutaneous adipose tissue to examine biomarkers of cancer risk. Cancer Prev Res (Phila) 2009;2:37-42.
22. Farhadi A, Keshavarzian A, Fields JZ, Sheikh M, Banan A. Resolution of common dietary sugars from probe sugars for test of intestinal permeability using capillary column gas chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 2006;836:63-8.
23. Hagman DK, Kuzma JN, Larson I, Foster-Schubert KE, Kuan LY, Cignarella A, Geamanu E, Makar KW, Gottlieb JR, Kratz M. Characterizing and quantifying leukocyte populations in human adipose tissue: impact of enzymatic tissue processing. J Immunol Methods 2012;386:50-9.
24. Catalán V, Gomez-Ambrosi J, Rotellar F, Silva C, Rodriguez A, Salvador J, Gil MJ, Cienfuegos JA, Fruhbeck G. Validation of endogenous control genes in human adipose tissue: relevance to obesity and obesity-associated type 2 diabetes mellitus. Horm Metab Res 2007;39:495-500.
25. Streiner DL. Best (but oft-forgotten) practices: the multiple problems of multiplicity-whether and how to correct for many statistical tests. Am J Clin Nutr 2015;102:721-8.
26. Smecuol E, Sugai E, Niveloni S, Vazquez H, Pedreira S, Mazure R, Moreno ML, Label M, Maurino E, Fasano A, et al. Permeability, zonulin production, and enteropathy in dermatitis herpetiformis. Clin Gastroenterol Hepatol 2005;3:335-41.
27. Cox CL, Stanhope KL, Schwarz JM, Graham JL, Hatcher B, Griffen SC, Bremer AA, Berglund L, McGahan JP, Keim NL, et al. Circulating concentrations of monocyte chemoattractant protein-1, plasminogen activator inhibitor-1, and soluble leukocyte adhesion molecule-1 in overweight/obese men and women consuming fructose-or glucosesweetened beverages for 10 weeks. J Clin Endocrinol Metab 2011;96: E2034-8.
28. Shimomura I, Funahashi T, Takahashi M, Maeda K, Kotani K, Nakamura T, Yamashita S, Miura M, Fukuda Y, Takemura K, et al. Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity. Nat Med 1996;2:800-3.
29. Bruun JM, Lihn AS, Pedersen SB, Richelsen B.Monocyte chemoattractant protein-1 release is higher in visceral than subcutaneous human adipose tissue (AT): implication of macrophages resident in the AT. J Clin Endocrinol Metab 2005;90:2282-9.
30. Silbernagel G, Machann J, Haring HU, Fritsche A, Peter A. Plasminogen activator inhibitor-1, monocyte chemoattractant protein-1, e-selectin and C-reactive protein levels in response to 4-week very-high-fructose or-glucose diets. Eur J Clin Nutr 2014;68:97-100.
31. Aeberli I, Gerber PA, Hochuli M, Kohler S, Haile SR, Gouni-Berthold I, Berthold HK, Spinas GA, Berneis K. Low to moderate sugar-sweetened beverage consumption impairs glucose and lipid metabolism and promotes inflammation in healthy young men: a randomized controlled trial. Am J Clin Nutr 2011;94:479-85.
32. Stefan N, Haring HU. The role of hepatokines in metabolism. Nat Rev Endocrinol 2013;9:144-52.