Antioxidant supplements reduced oxidative stress and stabilized liver function tests but did not reduce inflammation in a randomized controlled trial in obese children and adolescents

Journal of Nutrition

Volumn 144, Issue 2, 2014, Pages 193-201

  Murer, Stefanie B ^a   Aeberli, Isabelle ^a,b   Braegger, Christian P ^c   Gittermann, Matthias ^d   Hersberger, Martin ^c   Leonard, Scott W ^e   Taylor, Alan W ^e   Traber, Maret G ^e   Zimmermann, Michael B ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^d Children's Hospital KSA   (Switzerland)

^e OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA TOCOPHEROL; ASCORBIC ACID; ASPARTATE AMINOTRANSFERASE; GAMMA GLUTAMYLTRANSFERASE; GLUCOSE; INSULIN; ISOPROSTANE DERIVATIVE; LIPID; LIVER ENZYME; PROSTAGLANDIN F2 ALPHA; SELENIUM;

ANTHROPOMETRY; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; FEMALE; HEPATITIS; HUMAN; LIFESTYLE MODIFICATION; LIVER FUNCTION; LIVER FUNCTION TEST; MALE; OBESITY; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; SCHOOL CHILD;

ADOLESCENT; ALANINE TRANSAMINASE; ALPHA-TOCOPHEROL; ANTIOXIDANTS; ASCORBIC ACID; ASPARTATE AMINOTRANSFERASES; BIOLOGICAL MARKERS; CHILD; DIETARY SUPPLEMENTS; FEMALE; GAMMA-GLUTAMYLTRANSFERASE; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; ISOPROSTANES; LIVER; LIVER FUNCTION TESTS; MALE; MICRONUTRIENTS; OBESITY; OXIDATIVE STRESS; SELENIUM; WEIGHT REDUCTION PROGRAMS;

EID: 84892637572     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.185561     Document Type: Article

References (84)

1. Sies H. Introductory remarks. In: Oxidative stress. London: Academic Press; 1985. p. 1-8.
2. Ortega RM, Rodriguez-Rodriguez E, Aparicio A, Jimenez-Ortega AI, Palmeros C, Perea JM, Navia B, Lopez-Sobaler AM. Young children with excess of weight show an impaired selenium status. Int J Vitam Nutr Res. 2012;82:121-9.
3. Puchau B, Ochoa MC, Zulet MA, Marti A, Martinez JA, Members G. Dietary total antioxidant capacity and obesity in children and adolescents. Int J Food Sci Nutr. 2010;61:713-21.
4. Beydoun MA, Canas JA, Beydoun HA, Chen X, ShroffMR, Zonderman AB. Serum antioxidant concentrations and metabolic syndrome are associated among U.S. adolescents in recent national surveys. J Nutr. 2012; 142:1693-704.
5. de Souza Valente da Silva L, Valeria da Veiga G, Ramalho RA. Association of serum concentrations of retinol and carotenoids with overweight in children and adolescents. Nutrition. 2007;23:392-7.
6. Decsi T, Molnar D, Koletzko B. Reduced plasma concentrations of alpha-tocopherol and beta-carotene in obese boys. J Pediatr. 1997;130: 653-5.
7. Kuno T, Hozumi M, Morinobu T, Murata T, Mingci Z, Tamai H. Antioxidant vitamin levels in plasma and low density lipoprotein of obese girls. Free Radic Res. 1998;28:81-6.
8. Molnár D, Decsi T, Koletzko B. Reduced antioxidant status in obese children with multimetabolic syndrome. Int J Obes Relat Metab Disord. 2004;28:1197-202.
9. Morinobu T, Murata T, Takaya R, Tamai H. Nutritional status of betacarotene, alpha-tocopherol and retinol in obese children. Int J Vitam Nutr Res. 2002;72:119-23.
10. Sarni RO, Suano de Souza FI, Ramalho RA, Schoeps Dde O, Kochi C, Catherino P, Dias MC, Pessotti CF, Mattoso LC, Colugnat FA. Serum retinol and total carotene concentrations in obese pre-school children. Med Sci Monit. 2005;11:CR510-4.
11. Strauss RS. Comparison of serum concentrations of alpha-tocopherol and beta-carotene in a cross-sectional sample of obese and nonobese children (NHANES III). National Health and Nutrition Examination Survey. J Pediatr. 1999;134:160-5.
12. Codoñer-Franch P, Boix-Garcia L, Simo-Jorda R, Del Castillo-Villaescusa C, Maset-Maldonado J, Valls-Belles V. Is obesity associated with oxidative stress in children?. Int J Pediatr Obes. 2010;5:56-63.
13. Codoñer-Franch P, Valls-Belles V, Arilla-Codoner A, Alonso-Iglesias E. Oxidant mechanisms in childhood obesity: the link between inflammation and oxidative stress. Transl Res. 2011;158:369-84.
14. Sinaiko AR, Steinberger J,Moran A, Prineas RJ, Vessby B, Basu S, Tracy R, Jacobs DR, Jr. Relation of body mass index and insulin resistance to cardiovascular risk factors, inflammatory factors, and oxidative stress during adolescence. Circulation. 2005;111:1985-91.
15. Araki S, Dobashi K, Yamamoto Y, Asayama K, Kusuhara K. Increased plasma isoprostane is associated with visceral fat, high molecular weight adiponectin, and metabolic complications in obese children. Eur J Pediatr. 2010;169:965-70.
16. Kelly AS, Jacobs DR Jr, Sinaiko AR, Moran A, Steffen LM, Steinberger J. Relation of circulating oxidized LDL to obesity and insulin resistance in children. Pediatr Diabetes. 2010;11:552-5.
17. Codoñer-Franch P, Tavarez-Alonso S,Murria-Estal R, Tortajada-GirbesM, Simo-Jorda R, Alonso-Iglesias E. Elevated advanced oxidation protein products (AOPPs) indicate metabolic risk in severely obese children. Nutr Metab Cardiovasc Dis. 2012;22:237-43.
18. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stressactivated signaling pathways mediators of insulin resistance and betacell dysfunction?. Diabetes. 2003;52:1-8.
19. Day CP, James OF. Steatohepatitis: a tale of two "hits"?. Gastroenterology. 1998;114:842-5.
20. Higdon JV, Frei B. Obesity and oxidative stress: a direct link to CVD?. Arterioscler Thromb Vasc Biol. 2003;23:365-7.
21. Nemet D, Wang P, Funahashi T, Matsuzawa Y, Tanaka S, Engelman L, Cooper DM. Adipocytokines, body composition, and fitness in children. Pediatr Res. 2003;53:148-52.
22. Moon YS, Kim DH, Song DK. Serum tumor necrosis factor-alpha levels and components of the metabolic syndrome in obese adolescents. Metabolism. 2004;53:863-7.
23. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Lowgrade systemic inflammation in overweight children. Pediatrics. 2001; 107:E13.
24. Ford ES, Galuska DA, Gillespie C, Will JC, Giles WH, Dietz WH. C-reactive protein and body mass index in children: findings from the Third National Health and Nutrition Examination Survey, 1988-1994. J Pediatr. 2001;138:486-92.
25. Tilg H, Moschen AR. Inflammatory mechanisms in the regulation of insulin resistance. Mol Med. 2008;14:222-31.
26. Zhang C. The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol. 2008;103:398-406.
27. Bondia-Pons I, Ryan L, Martinez JA. Oxidative stress and inflammation interactions in human obesity. J Physiol Biochem. 2012;68:701-11.
28. Kelly AS, Steinberger J, Kaiser DR, Olson TP, Bank AJ, Dengel DR. Oxidative stress and adverse adipokine profile characterize the metabolic syndrome in children. J Cardiometab Syndr. 2006;1:248-52.
29. Ustundag B, Gungor S, Aygun AD, Turgut M, Yilmaz E. Oxidative status and serum leptin levels in obese prepubertal children. Cell Biochem Funct. 2007;25:479-83.
30. Codoñer-Franch P, Tavarez-Alonso S, Murria-Estal R, Megias-Vericat J, Tortajada-Girbes M, Alonso-Iglesias E. Nitric oxide production is increased in severely obese children and related to markers of oxidative stress and inflammation. Atherosclerosis. 2011;215:475-80.
31. Holt EM, Steffen LM,Moran A, Basu S, Steinberger J, Ross JA, Hong CP, Sinaiko AR. Fruit and vegetable consumption and its relation to markers of inflammation and oxidative stress in adolescents. J Am Diet Assoc. 2009;109:414-21.
32. Helmersson J, Arnlov J, Larsson A, Basu S. Low dietary intake of betacarotene, alpha-tocopherol and ascorbic acid is associated with increased inflammatory and oxidative stress status in a Swedish cohort. Br J Nutr. 2009;101:1775-82.
33. Sutherland WH, Manning PJ, Walker RJ, de Jong SA, Ryalls AR, Berry EA. Vitamin E supplementation and plasma 8-isoprostane and adiponectin in overweight subjects. Obesity (Silver Spring). 2007;15: 386-91.
34. Block G, Jensen CD, Morrow JD, Holland N, Norkus EP, Milne GL, Hudes M, Dalvi TB, Crawford PB, Fung EB, et al. The effect of vitamins C and E on biomarkers of oxidative stress depends on baseline level. Free Radic Biol Med. 2008;45:377-84.
35. Devaraj S, Leonard S, Traber MG, Jialal I. Gamma-tocopherol supplementation alone and in combination with alpha-tocopherol alters biomarkers of oxidative stress and inflammation in subjects with metabolic syndrome. Free Radic Biol Med. 2008;44:1203-8.
36. Vincent HK, Bourguignon CM, Weltman AL, Vincent KR, Barrett E, Innes KE, Taylor AG. Effects of antioxidant supplementation on insulin sensitivity, endothelial adhesion molecules, and oxidative stress in normal-weight and overweight young adults. Metabolism. 2009;58: 254-62.
37. Devaraj S, Jialal I. Alpha tocopherol supplementation decreases serum C-reactive protein and monocyte interleukin-6 levels in normal volunteers and type 2 diabetic patients. Free Radic Biol Med. 2000;29:790-2.
38. Peairs AT, Rankin JW. Inflammatory response to a high-fat, lowcarbohydrate weight loss diet: effect of antioxidants. Obesity (Silver Spring). 2008;16:1573-8.
39. Block G, Jensen CD, Dalvi TB, Norkus EP, Hudes M, Crawford PB, Holland N, Fung EB, Schumacher L, Harmatz P. Vitamin C treatment reduces elevated C-reactive protein. Free Radic Biol Med. 2009;46:70-7.
40. Manning PJ, Sutherland WH, Walker RJ, Williams SM, De Jong SA, Ryalls AR, Berry EA. Effect of high-dose vitamin E on insulin resistance and associated parameters in overweight subjects. Diabetes Care. 2004;27:2166-71.
41. Codoñer-Franch P, Lopez-Jaen AB, De La Mano-Hernandez A, Sentandreu E, Simo-Jorda R, Valls-Belles V. Oxidative markers in children with severe obesity following low-calorie diets supplemented with mandarin juice. Acta Paediatr. 2010;99:1841-6.
42. Kelishadi R, Hashemipour M, Adeli K, Tavakoli N, Movahedian-Attar A, Shapouri J, Poursafa P, Rouzbahani A. Effect of zinc supplementation on markers of insulin resistance, oxidative stress, and inflammation among prepubescent children with metabolic syndrome. Metab Syndr Relat Disord. 2010;8:505-10.
43. D'Adamo E, Marcovecchio ML, Giannini C, de Giorgis T, Chiavaroli V, Chiarelli F, Mohn A. Improved oxidative stress and cardio-metabolic status in obese prepubertal children with liver steatosis treated with lifestyle combined with Vitamin E. Free Radic Res. 2013;47:146-53.
44. Mencin AA, Lavine JE. Advances in pediatric nonalcoholic fatty liver disease. Pediatr Clin North Am. 2011;58:1375-92.
45. Schwimmer JB, Pardee PE, Lavine JE, Blumkin AK, Cook S. Cardiovascular risk factors and the metabolic syndrome in pediatric nonalcoholic fatty liver disease. Circulation. 2008;118:277-83.
46. Barshop NJ, Francis CS, Schwimmer JB, Lavine JE. Nonalcoholic fatty liver disease as a comorbidity of childhood obesity. Ped Health. 2009;3: 271-81.
47. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010; 52:1836-46.
48. Alisi A, Feldstein AE, Villani A, Raponi M, Nobili V. Pediatric nonalcoholic fatty liver disease: a multidisciplinary approach. Nat Rev Gastroenterol Hepatol. 2012;9:152-61.
49. Lavine JE, Schwimmer JB, Van Natta ML, Molleston JP, Murray KF, Rosenthal P, Abrams SH, Scheimann AO, Sanyal AJ, Chalasani N, et al. Effect of vitamin E or metformin for treatment of nonalcoholic fatty liver disease in children and adolescents: the TONIC randomized controlled trial. JAMA. 2011;305:1659-68.
50. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, Neuschwander-Tetri BA, Lavine JE, Tonascia J, Unalp A, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010;362:1675-85.
51. Harrison SA, Torgerson S, Hayashi P, Ward J, Schenker S. Vitamin E and vitamin C treatment improves fibrosis in patients with nonalcoholic steatohepatitis. Am J Gastroenterol. 2003;98:2485-90.
52. Nobili V, Manco M, Devito R, Ciampalini P, Piemonte F, Marcellini M. Effect of vitamin E on aminotransferase levels and insulin resistance in children with non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2006;24:1553-61.
53. Nobili V, Manco M, Devito R, Di Ciommo V, Comparcola D, Sartorelli MR, Piemonte F, Marcellini M, Angulo P. Lifestyle intervention and antioxidant therapy in children with nonalcoholic fatty liver disease: a randomized, controlled trial. Hepatology. 2008;48:119-28.
54. Ogden CL, Kuczmarski RJ, Flegal KM, Mei Z, Guo S, Wei R, Grummer-Strawn LM, Curtin LR, Roche AF, Johnson CL. Centers for Disease Control and Prevention 2000 growth charts for the United States: improvements to the 1977 National Center for Health Statistics version. Pediatrics. 2002;109:45-60.
55. Institute of Medicine. Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids. A Report of the Panel on Dietary Antioxidants and Related Compounds, Subcommittees on Upper Reference Levels of Nutrients and Interpretation and Uses of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. Washington, DC: National Academy Press; 2000.
56. Bruno RS, Leonard SW, Park SI, Zhao Y, Traber MG. Human vitamin E requirements assessed with the use of apples fortified with deuterium-labeled alpha-tocopheryl acetate. Am J Clin Nutr. 2006; 83:299-304.
57. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser. 1995;854:1-452.
58. Gibson R. Nutritional assessment: a laboratory manual. Oxford: Oxford University Press; 1993.
59. Deurenberg P, Pieters JJ, Hautvast JG. The assessment of the body fat percentage by skinfold thickness measurements in childhood and young adolescence. Br J Nutr. 1990;63:293-303.
60. Frei B, England L, Ames BN. Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci USA. 1989;86:6377-81.
61. Podda M, Weber C, Traber MG, Packer L. Simultaneous determination of tissue tocopherols, tocotrienols, ubiquinols, and ubiquinones. J Lipid Res. 1996;37:893-901.
62. Traber MG, Jialal I. Measurement of lipid-soluble vitamins-further adjustment needed?. Lancet. 2000;355:2013-4.
63. Sieniawska CE, Mensikov R, Delves HT. Determination of total selenium in serum, whole blood and erythrocytes by ICP-MS. J Anal Atomic Spectrom. 1999;14:109-12.
64. Erhardt JG, Estes JE, Pfeiffer CM, Biesalski HK, Craft NE. Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique. J Nutr. 2004;134:3127-32.
65. Hong YL, Yeh SL, Chang CY, Hu ML. Total plasma malondialdehyde levels in 16 Taiwanese college students determined by various thiobarbituric acid tests and an improved high-performance liquid chromatographybased method. Clin Biochem. 2000;33:619-25.
66. Young IS, Trimble ER. Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem. 1991;28:504-8.
67. Taylor AW, Bruno RS, Traber MG. Women and smokers have elevated urinary F(2)-isoprostane metabolites: a novel extraction and LC-MS methodology. Lipids. 2008;43:925-36.
68. Leonard SW, Traber MG. Measurement of the vitamin E metabolites, carboxyethyl hydroxychromans (CEHCs), in biological samples. Curr Protoc Toxicol. 2006;Chapter 7:Unit 7.8.
69. Li YJ, Luo SC, Lee YJ, Lin FJ, Cheng CC,Wein YS, Kuo YH, Huang CJ. Isolation and identification of alpha-CEHC sulfate in rat urine and an improved method for the determination of conjugated alpha-CEHC. J Agric Food Chem. 2008;56:11105-13.
70. Hervey GR. Determination of creatinine by the Jaffe reaction. Nature. 1953;171:1125.
71. Jacob S. Swiss nutrient database V1.0. Bern (Switzerland): Swiss Nutrition Society, Bern; Federal Office of Public Health, Bern; Swiss Federal Institute of Technology, Zurich; 2005.
72. Bandini LG, Schoeller DA, Cyr HN, Dietz WH. Validity of reported energy intake in obese and nonobese adolescents. Am J Clin Nutr. 1990;52:421-5.
73. Aeberli I, Molinari L, Spinas G, Lehmann R, l'Allemand D, Zimmermann MB. Dietary intakes of fat and antioxidant vitamins are predictors of subclinical inflammation in overweight Swiss children. Am J Clin Nutr. 2006;84:748-55.
74. Mohn A, Catino M, Capanna R, Giannini C, Marcovecchio M, Chiarelli F. Increased oxidative stress in prepubertal severely obese children: effect of a dietary restriction restriction-weight loss program. J Clin Endocrinol Metab. 2005;90:2653-8.
75. Morrow JD, Harris TM, Roberts LJ 2nd. Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Anal Biochem. 1990;184:1-10.
76. Basu S. Isoprostanes: novel bioactive products of lipid peroxidation. Free Radic Res. 2004;38:105-22.
77. Musiek ES, Yin H, Milne GL, Morrow JD. Recent advances in the biochemistry and clinical relevance of the isoprostane pathway. Lipids. 2005;40:987-94.
78. Dorjgochoo T, Gao YT, Chow WH, Shu XO, Yang G, Cai Q, Rothman N, Cai H, Li H, Deng X, et al. Major metabolite of F2-isoprostane in urine may be a more sensitive biomarker of oxidative stress than isoprostane itself. Am J Clin Nutr. 2012;96:405-14.
79. Block G, Jensen C, Dietrich M, Norkus EP, Hudes M, Packer L. Plasma C-reactive protein concentrations in active and passive smokers: influence of antioxidant supplementation. J Am Coll Nutr. 2004;23:141-7.
80. Bruunsgaard H, Poulsen HE, Pedersen BK, Nyyssonen K, Kaikkonen J, Salonen JT. Long-term combined supplementations with alpha-tocopherol and vitamin C have no detectable anti-inflammatory effects in healthy men. J Nutr. 2003;133:1170-3.
81. Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C. Prevalence of fatty liver in children and adolescents. Pediatrics. 2006;118: 1388-93.
82. Schindhelm RK, Diamant M, Dekker JM, Tushuizen ME, Teerlink T, Heine RJ. Alanine aminotransferase as a marker of non-alcoholic fatty liver disease in relation to type 2 diabetes mellitus and cardiovascular disease. Diabetes Metab Res Rev. 2006;22:437-43.
83. Lebold KM, Ang A, Traber MG, Arab L. Urinary alpha-carboxyethyl hydroxychroman can be used as a predictor of alpha-tocopherol adequacy, as demonstrated in the Energetics Study. Am J Clin Nutr. 2012;96: 801-9.
84. Patton HM, Lavine JE, Van Natta ML, Schwimmer JB, Kleiner D, Molleston J; Nonalcoholic Steatohepatitis Clinical Research Network. Clinical correlates of histopathology in pediatric nonalcoholic steatohepatitis. Gastroenterology. 2008;135:1961-71.e2.