Controlled Feeding of an 8-d, High-Dairy Cheese Diet Prevents Sodium-Induced Endothelial Dysfunction in the Cutaneous Microcirculation of Healthy, Older Adults through Reductions in Superoxide

Journal of Nutrition

Volumn 150, Issue 1, 2020, Pages 55-63

  Alba, Billie K ^a   Stanhewicz, Anna E ^a   Dey, Priyankar ^b   Bruno, Richard S ^b   Kenney, W Larry ^a   Alexander, Lacy M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

cheese; dairy; endothelial function; nitric oxide; older adults; oxidative stress; sodium; superoxide; vasodilation

Indexed keywords

ACETYLCHOLINE; APOCYNIN; ASCORBIC ACID; HEMOGLOBIN; MALONALDEHYDE; N(G) NITROARGININE; NITRIC OXIDE SYNTHASE; RENALASE; SODIUM; SUPEROXIDE; TEMPOL;

ADULT; ARTICLE; BLOOD PRESSURE REGULATION; CHEESE; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIASTOLIC BLOOD PRESSURE; DIET RESTRICTION; DIET SUPPLEMENTATION; DIET THERAPY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM DEPENDENT DILATION; FEMALE; HEMODYNAMIC PARAMETERS; HIGH SODIUM INTAKE; HUMAN; MALE; MEAN ARTERIAL PRESSURE; MICROCIRCULATION; MICRODIALYSIS; MIDDLE AGED; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; SKIN CONDUCTANCE; SODIUM RESTRICTION; SYSTOLIC BLOOD PRESSURE; VASODILATATION; ADMINISTRATION AND DOSAGE; ADVERSE EVENT; AGED; BLOOD PRESSURE; DIET; DRUG EFFECT; METABOLISM; SODIUM INTAKE; URINE; VASCULAR ENDOTHELIUM;

ACETYLCHOLINE; AGED; BLOOD PRESSURE; CHEESE; CROSS-OVER STUDIES; DIET; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MICROCIRCULATION; SODIUM; SODIUM, DIETARY; SUPEROXIDES;

EID: 85077669904     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/nxz205     Document Type: Article

References (57)

1. Qin LQ, Xu JY, Han SF, Zhang ZL, Zhao YY, Szeto IM. Dairy consumption and risk of cardiovascular disease: an updated metaanalysis of prospective cohort studies.Asia Pac J Clin Nutr 2015;24:90-100.
2. Soedamah-Muthu SS, Ding EL, Al-Delaimy WK,Hu FB, EngberinkMF, Willett WC, Geleijnse JM. Milk and dairy consumption and incidence of cardiovascular diseases and all-cause mortality: dose-response metaanalysis of prospective cohort studies. Am J Clin Nutr 2011;93:158-71.
3. US Department of Health and Human Services and USDA. 2015-2020 dietary guidelines for Americans. 8th Edition [Internet]. December 2015. Available from: http://health.gov/dietaryguidelines/2015/guidelin es/.
4. Tuomilehto J, Jousilahti P, Rastenyte D, Moltchanov V, Tanskanen A, Pietinen P, Nissinen A. Urinary sodium excretion and cardiovascular mortality in Finland: a prospective study. Lancet 2001;357: 848-51.
5. Meneton P, Jeunemaitre X, de Wardener HE, MacGregor GA. Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol Rev 2005;85:679-715.
6. DuPont JJ, Greaney JL, Wenner MM, Lennon-Edwards SL, Sanders PW, Farquhar WB, Edwards DG. High dietary sodium intake impairs endothelium-dependent dilation in healthy salt-resistant humans. J Hypertens 2013;31:530-6.
7. Greaney JL,DuPont JJ, Lennon-Edwards SL, Sanders PW, Edwards DG, Farquhar WB. Dietary sodium loading impairs microvascular function independent of blood pressure in humans: role of oxidative stress. Journal of Physiology-London 2012;590:5519-28.
8. Bruning RS, Santhanam L, Stanhewicz AE, Smith CJ, Berkowitz DE, Kenney WL, Holowatz LA. Endothelial nitric oxide synthase mediates cutaneous vasodilation during local heating and is attenuated inmiddleaged human skin. J Appl Physiol 2012;112:2019-26.
9. Edwards DG, Farquhar WB. Vascular effects of dietary salt. Curr Opin Nephrol Hypertens 2015;24:8-13.
10. Boegehold MA. The effect of high salt intake on endothelial function: reduced vascular nitric oxide in the absence of hypertension. J Vasc Res 2013;50:458-67.
11. Lenda DM, Sauls BA, Boegehold MA. Reactive oxygen species may contribute to reduced endothelium-dependent dilation in rats fed high salt. Am J Physiol Heart Circ Physiol 2000;279:H7-H14.
12. Zhu J, Huang T, Lombard JH. Effect of high-salt diet on vascular relaxation and oxidative stress in mesenteric resistance arteries. J Vasc Res 2007;44:382-90.
13. Nurkiewicz TR, Wu GY, Li P, Boegehold MA. Decreased arteriolar tetrahydrobiopterin is linked to superoxide generation from nitric oxide synthase in mice fed high salt. Microcirculation 2010;17: 147-57.
14. Nurkiewicz TR, Boegehold MA. High salt intake reduces endotheliumdependent dilation of mouse arterioles via superoxide anion generated from nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 2007;292:R1550-6.
15. Durand MJ, Lombard JH. Low-dose angiotensin II infusion restores vascular function in cerebral arteries of high salt-fed rats by increasing copper/zinc superoxide dimutase expression.Am JHypertens 2013;26:739-47.
16. Lenda DM, Boegehold MA. Effect of a high salt diet on microvascular antioxidant enzymes. J Vasc Res 2002;39:41-50.
17. Jablonski KL, Racine ML, Geolfos CJ, Gates PE, Chonchol M, McQueen MB, Seals DR. Dietary sodium restriction reverses vascular endothelial dysfunction in middle-aged/older adults with moderately elevated systolic blood pressure. J Am Coll Cardiol 2013;61:335-43.
18. Livingstone KM, Lovegrove JA, Cockcroft JR, Elwood PC, Pickering JE, Givens DI. Does dairy food intake predict arterial stiffness and blood pressure in men? Evidence from the Caerphilly Prospective Study. Hypertension 2013;61:42-7.
19. Crichton GE, Elias MF, Dore GA, Abhayaratna WP, Robbins MA. Relations between dairy food intake and arterial stiffness pulse wave velocity and pulse pressure. Hypertension 2012;59:1044-51.
20. Hernandez-Ledesma B, Miralles B, Amigo L, Ramos M, Recio I. Identification of antioxidant and ACE-inhibitory peptides in fermented milk. J Sci Food Agric 2005;85:1041-8.
21. Nongonierma AB, FitzGerald RJ. Dipeptidyl peptidase IV inhibitory and antioxidative properties of milk protein-derived dipeptides and hydrolysates. Peptides 2013;39:157-63.
22. Zemel MB, Sun XC. Dietary calcium and dairy products modulate oxidative and inflammatory stress in mice and humans. J Nutr 2008;138:1047-52.
23. Diaz M, Decker EA. Antioxidant mechanisms of caseinophosphopeptides and casein hydrolysates and their application in ground beef. J Agric Food Chem 2004;52:8208-13.
24. O'Keeffe MB, FitzGerald RJ. Antioxidant effects of enzymatic hydrolysates of whey protein concentrate on cultured human endothelial cells. Int Dairy J 2014;36:128-35.
25. Phelan M, Aherne-Bruce SA,O'Sullivan D, FitzGerald RJ,O'Brien NM. Potential bioactive effects of casein hydrolysates on human cultured cells. Int Dairy J 2009;19:279-85.
26. Stanhewicz AE, Alba BK, Kenney WL, Alexander LM. Dairy cheese consumption ameliorates single-meal sodium-induced cutaneous microvascular dysfunction by reducing ascorbate-sensitive oxidants in healthy older adults. Br J Nutr 2016;116:658-65.
27. Khan F, Patterson D, Belch JJF, Hirata K, Lang CC. Relationship between peripheral and coronary function using laser Doppler imaging and transthoracic echocardiography. Clin Sci 2008;115:295-300.
28. Holowatz LA, Thompson-Torgerson CS, Kenney WL. The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 2008;105:370-2.
29. WeinbergerMH, Miller JZ, Luft FC, Grim CE, Fineberg NS. Definitions and characteristics of sodium sensitivity and blood pressure resistance. Hypertension 1986;8:II127-34.
30. Schulman IH, Aranda P, Raij L, Veronesi M, Aranda FJ, Martin R. Surgical menopause increases salt sensitivity of blood pressure. Hypertension 2006;47:1168-74.
31. Cubeddu LX, Alfieri AB, Hoffmann IS, Jimenez E, Roa CM, Cubeddu R, Palermo C, Baldonedo RM. Nitric oxide and salt sensitivity. Am J Hypertens 2000;13:973-9.
32. Alba BK, Stanhewicz AE, Kenney WL, Alexander LM. Acute dairy milk ingestion does not improve nitric oxide-dependent vasodilation in the cutaneous microcirculation. Br J Nutr 2016;116:204-10.
33. Greaney JL, Saunders EFH, Santhanam L, Alexander LM. Oxidative stress contributes to microvascular endothelial dysfunction in men and women with major depressive disorder. Circ Res 2019;124: 564-74.
34. Corretti MC, Anderson TJ, Benjamin EJ,Celermajer D,Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, et al. Guidelines for the ultrasound assessment of endothelialdependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002;39:257-65.
35. 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.
36. Holowatz LA, Thompson CS,Minson CT, Kenney WL.Mechanisms of acetylcholine-mediated vasodilatation in young and aged human skin. Journal of Physiology-London 2005;563:965-73.
37. Anderson TJ, Uehata A, GerhardMD, Meredith IT,Knab S,Delagrange D, Lieberman EH, Ganz P, Creager MA, Yeung AC, et al. Close relation of endothelial function in the human coronary and peripheral circulations. J Am Coll Cardiol 1995;26:1235-41.
38. Dickinson KM, Keogh JB, Clifton PM. Effects of a low-salt diet on flowmediated dilatation in humans. Am J Clin Nutr 2009;89:485-90.
39. Dickinson KM, Clifton PM, Keogh JB. Endothelial function is impaired after a high-salt meal in healthy subjects. Am J Clin Nutr 2011;93: 500-5.
40. Lenda DM, BoegeholdMA. Effect of a high-salt diet on oxidant enzyme activity in skeletal muscle microcirculation. Am J Physiol Heart Circ Physiol 2002;282:H395-402.
41. Zhu JX, Mori T, Huang T, Lombard JH. Effect of high-salt diet on NO release and superoxide production in rat aorta. American Journal of Physiology-Heart and Circulatory Physiology 2004;286: H575-H83.
42. Bondarenko A, Panasiuk O, Stepanenko L, Goswami N, Sagach V. Reduced hyperpolarization of endothelial cells following high dietary Na+: effects of enalapril and tempol. Clin Exp Pharmacol Physiol 2012;39:608-13.
43. Stanhewicz AE, Bruning RS, Smith CJ, Kenney WL, Holowatz LA. Local tetrahydrobiopterin administration augments reflex cutaneous vasodilation through nitric oxide-dependent mechanisms in aged human skin. J Appl Physiol 2012;112:791-7.
44. Power-Grant O, McCormack WG, De Cap MR, Amigo-Benavent M, Fitzgerald RJ, Jakeman P. Evaluation of the antioxidant capacity of a milk protein matrix in vitro and in vivo in women aged 50-70 years. Int J Food Sci Nutr 2016;67:325-34.
45. Stancliffe RA, Thorpe T, Zemel MB. Dairy attentuates oxidative and inflammatory stress in metabolic syndrome. Am J Clin Nutr 2011;94:422-30.
46. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M, Kelm M. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci USA 2001;98:12814-9.
47. Otto MCD, Mozaffarian D, Kromhout D, Bertoni AG, Sibley CT, Jacobs DR, Nettleton JA. Dietary intake of saturated fat by food source and incident cardiovascular disease: The Multi-Ethnic Study of Atherosclerosis. Am J Clin Nutr 2012;96:397-404.
48. Campese VM. Salt sensitivity in hypertension. Renal and cardiovascular implications. Hypertension 1994;23:531-50.
49. Lennon-Edwards S, Ramick MG, Matthews EL, Brian MS, Farquhar WB, Edwards DG. Salt loading has a more deleterious effect on flow-mediated dilation in salt-resistant men than women. Nutr Metab Cardiovasc Dis 2014;24:990-5.
50. Eisenach JH, Gullixson LR, Kost SL, Joyner MJ, Turner ST, Nicholson WT. Sex differences in salt sensitivity to nitric oxide dependent vasodilation in healthy young adults. J Appl Physiol (1985) 2012;112:1049-53.
51. Blanch N, Clifton PM, Petersen KS, Keogh JB. Effect of sodium and potassium supplementation on vascular and endothelial function: a randomized controlled trial. Am J Clin Nutr 2015;101:939-46.
52. Cook NR, Obarzanek E, Cutler JA, Buring JE, Rexrode KM, Kumanyika SK, Appel LJ, Whelton PK; Trials of Hypertension Prevention Collaborative Research Group. Joint effects of sodium and potassium intake on subsequent cardiovascular disease: The trials of hypertension prevention follow-up study. Arch Intern Med 2009;169:32-40.
53. Simons JM, Hart BA, Ip Vai Ching TR, Van Dijk H, Labadie RP. Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free Radic Biol Med 1990;8:251-8.
54. Stefanska J, Pawliczak R. Apocynin: Molecular aptitudes. Mediators Inflamm. [Internet]. 2008;2008. Article ID 106507. Available from: https://www.hindawi.com/journals/mi/2008/106507/.
55. Freed JK, Beyer AM, LoGiudice JA, Hockenberry JC, Gutterman DD. Ceramide changes themediator of flow-induced vasodilation from nitric oxide to hydrogen peroxide in the human microcirculation. Circ Res 2014;115:525-32.
56. Freed JK, Gutterman DD. Communication is key: mechanisms of intercellular signaling in vasodilation. J Cardiovasc Pharmacol 2017;69:264-72.
57. Van Horn L, Carson JA, Appel LJ, Burke LE, Economos C, Karmally W, Lancaster K, Lichtenstein AH, Johnson RK, Thomas RJet al. Recommended dietary pattern to achieve adherence to the American Heart Association/American College of Cardiology (AHA/ACC) guidelines: a scientific statement from the American Heart Association. Circulation 2016;134:E505-29.