Low-Fat milk ingestion prevents postprandial hyperglycemia-mediated impairments in vascular endothelial function in obese individuals with metabolic syndrome1-3

Journal of Nutrition

Volumn 143, Issue 10, 2013, Pages 1602-1610

  Ballard, Kevin D ^a   Mah, Eunice ^c   Guo, Yi ^c   Pei, Ruisong ^c   Volek, Jeff S ^b   Bruno, Richard S ^c  

^a Departments of Nutritional Sciences   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ARGININE; ASCORBIC ACID; BIOLOGICAL MARKER; GAMMA TOCOPHEROL; GLUCOSE; GLUTATHIONE DISULFIDE; MALONALDEHYDE; MILK FAT; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; THIOL;

ADULT; AREA UNDER THE CURVE; ARTICLE; BIOAVAILABILITY; BRACHIAL ARTERY; CARDIOVASCULAR PARAMETERS; CLINICAL ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; ENDOTHELIAL DYSFUNCTION; FEMALE; FLOW MEDIATED DILATATION; GLUCOSE BLOOD LEVEL; HUMAN; HYPERGLYCEMIA; LIPID PEROXIDATION; MALE; METABOLIC SYNDROME X; NITRATIVE STRESS; OBESITY; OXIDATIVE STRESS; POSTPRANDIAL STATE; RANDOMIZED CONTROLLED TRIAL; VASCULAR ENDOTHELIUM;

ADULT; ANIMALS; AREA UNDER CURVE; ARGININE; BLOOD GLUCOSE; BRACHIAL ARTERY; CROSS-OVER STUDIES; DIET; DIETARY FATS; DOUBLE-BLIND METHOD; ENDOTHELIUM, VASCULAR; FASTING; FEMALE; HUMANS; HYPERGLYCEMIA; LIPID PEROXIDATION; MALE; MALONDIALDEHYDE; METABOLIC SYNDROME X; MILK; NITRIC OXIDE; OBESITY; ORYZA SATIVA; OXIDATIVE STRESS; PLANT PREPARATIONS; POSTPRANDIAL PERIOD; VASCULAR DISEASES; VASODILATION;

EID: 84885703275     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.179465     Document Type: Article

References (55)

1. Kris-Etherton PM, Grieger JA, Hilpert KF, West SG. Milk products, dietary patterns and blood pressure management. J Am Coll Nutr. 2009;28 Suppl 1:S103-19.
2. Lamarche B. Review of the effect of dairy products on non-lipid risk factors for cardiovascular disease. J Am Coll Nutr. 2008;27:S741-6.
3. FitzGerald RJ, Murray BA, Walsh DJ. Hypotensive peptides from milk proteins. J Nutr. 2004;134:S980-8.
4. Pal S, Ellis V. The chronic effects of whey proteins on blood pressure, vascular function, and inflammatory markers in overweight individuals. Obesity (Silver Spring). 2010;18:1354-9.
5. Hirota T, Ohki K, Kawagishi R, Kajimoto Y, Mizuno S, Nakamura Y, Kitakaze M. Casein hydrolysate containing the antihypertensive tripeptides Val-Pro-Pro and Ile-Pro-Pro improves vascular endothelial function independent of blood pressure-lowering effects: contribution of the inhibitory action of angiotensin-converting enzyme. Hypertens Res. 2007;30:489-96.
6. Ballard KD, Bruno RS, Seip RL, Quann EE, Volk BM, Freidenreich DJ, Kawiecki DM, Kupchak BR, Chung MY, Kraemer WJ, et al. Acute ingestion of a novel whey-derived peptide improves vascular endothelial responses in healthy individuals: a randomized, placebo controlled trial. Nutr J. 2009;8:34.
7. Ballard KD, Kupchak BR, Volk BM, Mah E, Shkreta A, Liptak C, Ptolemy AS, Kellogg MS, Bruno RS, Seip RL, et al. Acute effects of ingestion of a novel whey-derived extract on vascular endothelial function in overweight, middle-aged men and women. Br J Nutr. 2013;109: 882-93.
8. Yeboah J, Folsom AR, Burke GL, Johnson C, Polak JF, PostW, Lima JA, Crouse JR, Herrington DM. Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis. Circulation. 2009;120:502-9.
9. Saito T. Antihypertensive peptides derived from bovine casein and whey proteins. Adv Exp Med Biol. 2008;606:295-317.
10. Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999-2006. Diabetes Care. 2011;34:216-9.
11. Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, Rinfret S, Schiffrin EL, Eisenberg MJ. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol. 2010;56:1113-32.
12. Fumeron F, Lamri A, Abi Khalil C, Jaziri R, Porchay-Balderelli I, Lantieri O, Vol S, Balkau B, Marre M. Dairy consumption and the incidence of hyperglycemia and the metabolic syndrome: results from a French prospective study, Data from the Epidemiological Study on the Insulin Resistance Syndrome (DESIR). Diabetes Care. 2011;34:813-7.
13. Alipour A, Elte JW, van Zaanen HC, Rietveld AP, Cabezas MC. Postprandial inflammation and endothelial dysfuction. Biochem Soc Trans. 2007;35:466-9.
14. DECODE Study Group, The European Diabetes Epidemiology Group. Glucose tolerance and cardiovascular mortality: comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med. 2001;161: 397-405.
15. Mah E, Noh SK, Ballard KD, Matos ME, Volek JS, Bruno RS. Postprandial hyperglycemia impairs vascular endothelial function in healthy men by inducing lipid peroxidation and increasing asymmetric dimethylarginine:arginine. J Nutr. 2011;141:1961-8.
16. Mah E, Bruno RS. Postprandial hyperglycemia on vascular endothelial function: mechanisms and consequences. Nutr Res. 2012;32:727-40.
17. Brand-Miller JC, Stockmann K, Atkinson F, Petocz P, Denyer G. Glycemic index, postprandial glycemia, and the shape of the curve in healthy subjects: analysis of a database of more than 1,000 foods. Am J Clin Nutr. 2009;89:97-105.
18. Ghiadoni L, Penno G, Giannarelli C, Plantinga Y, Bernardini M, Pucci L, Miccoli R, Taddei S, Salvetti A, Del Prato S. Metabolic syndrome and vascular alterations in normotensive subjects at risk of diabetes mellitus. Hypertension. 2008;51:440-5.
19. Hansel B, Giral P, Nobecourt E, Chantepie S, Bruckert E, Chapman MJ, Kontush A. Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. J Clin Endocrinol Metab. 2004;89: 4963-71.
20. Van Guilder GP, Hoetzer GL, Greiner JJ, Stauffer BL, Desouza CA. Influence of metabolic syndrome on biomarkers of oxidative stress and inflammation in obese adults. Obesity (Silver Spring). 2006;14:2127-31.
21. Jonk AM, Houben AJ, Schaper NC, de Leeuw PW, Serne EH, Smulders YM, Stehouwer CD. Obesity is associated with impaired endothelial function in the postprandial state. Microvasc Res. 2011;82:423-9.
22. Bode-Böger SM, Scalera F, Ignarro LJ. The L-arginine paradox: Importance of the L-arginine/asymmetrical dimethylarginine ratio. Pharmacol Ther. 2007;114:295-306.
23. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640-5.
24. USDA, Agricultural Research Service. USDA National Nutrient Database for Standard Reference, Release 25. Nutrient Data Laboratory Home Page; 2012 [cited 2013 June 20]. Available from: http://www.ars. usda.gov/ba/bhnrc/ndl.
25. USDA and US Department of Health and Human Services. Dietary Guidelines for Americans, 2010. In: USDA and US Department of Health and Human Services, editor. 7th ed. Washington: US Government Printing Office; 2010.
26. Hilary Green J, Richards JK, Bunning RL. Blood pressure responses to high-calcium skim milk and potassium-enriched high-calcium skim milk. J Hypertens. 2000;18:1331-9.
27. Hashimoto M, Akishita M, Eto M, Ishikawa M, Kozaki K, Toba K, Sagara Y, Taketani Y, Orimo H, Ouchi Y. Modulation of endotheliumdependent flow-mediated dilatation of the brachial artery by sex and menstrual cycle. Circulation. 1995;92:3431-5.
28. Harris JA, Benedict FG. A biometric study of human basal metabolism. Proc Natl Acad Sci USA. 1918;4:370-3.
29. Parker BA, Trehearn TL, Meendering JR. Pick your Poiseuille: normalizing the shear stimulus in studies of flow-mediated dilation. J Appl Physiol. 2009;107:1357-9.
30. Pyke KE, Tschakovsky ME. Peak vs. total reactive hyperemia: which determines the magnitude of flow-mediated dilation? J Appl Physiol. 2007;102:1510-9.
31. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499-502.
32. Duncan MH, Singh BM, Wise PH, Carter G, Alaghband-Zadeh J. A simple measure of insulin resistance. Lancet. 1995;346:120-1.
33. Bruno RS, Dugan CE, Smyth JA, DiNatale DA, Koo SI. Green tea extract protects leptin-deficient, spontaneously obese mice from hepatic steatosis and injury. J Nutr. 2008;138:323-31.
34. Leonard SW, Bruno RS, Paterson E, Schock BC, Atkinson J, Bray TM, Cross CE, Traber MG. 5-Nitro-gamma-tocopherol increases in human plasma exposed to cigarette smoke in vitro and in vivo. Free Radic Biol Med. 2003;35:1560-7.
35. Masterjohn C, Mah E, Guo Y, Koo SI, Bruno RS. gamma-Tocopherol abolishes postprandial increases in plasma methylglyoxal following an oral dose of glucose in healthy, college-agedmen. J Nutr Biochem. 2012;23:292-8.
36. Bland JM, Altman DG. Calculating correlation coefficients with repeated observations: Part 1: correlation within subjects. BMJ. 1995;310:446.
37. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: executive summary. Expert Panel on the Identification, Evaluation, and Treatment of Overweight in Adults. Am J Clin Nutr. 1998;68:899-917.
38. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, et al. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation. 2012;125:e2-220.
39. DemircanN,GurelA,Armutcu F, UnalacakM,Aktunc E, Atmaca H. The evaluation of serum cystatin C, malondialdehyde, and total antioxidant status in patients with metabolic syndrome. Med Sci Monit. 2008;14: CR97-101.
40. Versari D, Daghini E, Virdis A, Ghiadoni L, Taddei S. Endothelial dysfunction as a target for prevention of cardiovascular disease. Diabetes Care. 2009;32 Suppl 2:S314-21.
41. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999;340:115-26.
42. Vergnani L, Hatrik S, Ricci F, Passaro A, Manzoli N, Zuliani G, Brovkovych V, Fellin R, Malinski T. Effect of native and oxidized lowdensity lipoprotein on endothelial nitric oxide and superoxide production: key role of L-arginine availability. Circulation. 2000;101:1261-6.
43. Williams SB, Goldfine AB, Timimi FK, Ting HH, Roddy MA, Simonson DC, Creager MA. Acute hyperglycemia attenuates endothelium-dependent vasodilation in humans in vivo. Circulation. 1998;97:1695-701.
44. Gunnerud UJ, Ostman EM, Bjorck IM. Effects of whey proteins on glycaemia and insulinaemia to an oral glucose load in healthy adults; a dose-response study. Eur J Clin Nutr. 2013;67:749-53.
45. BlomWA, Lluch A, Stafleu A, Vinoy S, Holst JJ, Schaafsma G, Hendriks HF. Effect of a high-protein breakfast on the postprandial ghrelin response. Am J Clin Nutr. 2006;83:211-20.
46. Christen S, Jiang Q, Shigenaga MK, Ames BN. Analysis of plasma tocopherols alpha, gamma, and 5-nitro-gamma in rats with inflammation by HPLC coulometric detection. J Lipid Res. 2002;43:1978-85.
47. Pal S, Ellis V. Acute effects of whey protein isolate on blood pressure, vascular function and inflammatory markers in overweight postmenopausal women. Br J Nutr. 2011;105:1512-9.
48. RomeroMJ, Platt DH, TawfikHE, LabaziM, El-Remessy AB, Bartoli M, Caldwell RB, Caldwell RW. Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ Res. 2008; 102:95-102.
49. Cooke JP. Does ADMA cause endothelial dysfunction? Arterioscler Thromb Vasc Biol. 2000;20:2032-7.
50. Jabecka A, Ast J, Bogdaski P, Drozdowski M, Pawlak-Lemaska K, Cielewicz AR, Pupek-Musialik D. Oral L-arginine supplementation in patients with mild arterial hypertension and its effect on plasma level of asymmetric dimethylarginine, L-citruline, L-arginine and antioxidant status. Eur Rev Med Pharmacol Sci. 2012;16:1665-74.
51. Jia SJ, Jiang DJ, Hu CP, Zhang XH, Deng HW, Li YJ. Lysophosphatidylcholine- induced elevation of asymmetric dimethylarginine level by the NADPH oxidase pathway in endothelial cells. Vascul Pharmacol. 2006;44:143-8.
52. Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME, Green DJ. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol. 2011;300:H2-12.
53. Stancliffe RA, Thorpe T, Zemel MB. Dairy attentuates oxidative and inflammatory stress in metabolic syndrome. Am J Clin Nutr. 2011;94: 422-30.
54. Pal S, Radavelli-Bagatini S. The effects of whey protein on cardiometabolic risk factors. Obes Rev. 2013;14:324-43.
55. Sipola M, Finckenberg P, Vapaatalo H, Pihlanto-Leppala A, Korhonen H, Korpela R, Nurminen ML. Alpha-lactorphin and beta-lactorphin improve arterial function in spontaneously hypertensive rats. Life Sci. 2002;71:1245-53.