Skip to main content
×
×
Home

Dairy cheese consumption ameliorates single-meal sodium-induced cutaneous microvascular dysfunction by reducing ascorbate-sensitive oxidants in healthy older adults

  • Anna E. Stanhewicz (a1), Billie K. Alba (a2), W. Larry Kenney (a1) (a2) and Lacy M. Alexander (a1) (a2)
Abstract

Chronic dairy product intake is associated with improved cardiovascular outcomes, whereas high dietary Na impairs endothelial function through increased oxidative stress and reduced nitric oxide (NO) bioavailability. The purpose of this study was to compare the effect of acute cheese consumption with consumption of Na from non-dairy sources on microvascular function. We hypothesised that dairy cheese ingestion would augment NO-dependent vasodilation compared with Na from non-dairy sources. On five visits, fourteen subjects (61 (sem 2) years, eight male/six female) consumed either 85 g dairy cheese (560 mg Na), 85 g soya cheese (560 mg Na), 65 g pretzels (560 mg Na), 170 g dairy cheese (1120 mg Na) or 130 g pretzels (1120 mg Na). Two intradermal microdialysis fibres were inserted in the ventral forearm for delivery of lactated Ringer’s solution or 10 mm-ascorbate (antioxidant) during local skin heating (approximately 50 min). Erythrocyte flux was measured continuously by laser-Doppler flowmetry (LDF), and cutaneous vascular conductance (CVC=LDF/mean arterial pressure) was normalised as %CVCmax (28 mm-sodium nitroprusside). Following a plateau in CVC, 15 mm-N G -nitro-l-arginine-methyl-ester was perfused to quantify NO-dependent vasodilation (approximately 45 min). NO-dependent vasodilation was greater following consumption of dairy products (560 mg Na 57 (sem 3) %) (1120 mg Na 55 (sem 5) %) compared with soya (560 mg Na 42 (sem 3) %; P=0·002) or pretzels (560 mg Na 43 (sem 4) %; P=0·004) (1120 mg Na 46 (sem 3) %; P=0·04). Ascorbate augmented NO-dependent vasodilation following intake of soya (control: 42 (sem 3) v. ascorbate: 54 (sem 3) %; P=0·01) or pretzels (560 mg Na; control: 43 (sem 4) v. ascorbate: 56 (sem 3) %; P=0·006) (1120 mg Na; control: 46 (sem 5) v. ascorbate: 56 (sem 3) %; P=0·02), but not dairy products. Na ingestion via dairy products was associated with greater NO-dependent vasodilation compared with non-dairy products, a difference that was ameliorated with ascorbate perfusion. The antioxidant properties of dairy proteins may protect against Na-induced reductions in NO-dependent dilation.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Dairy cheese consumption ameliorates single-meal sodium-induced cutaneous microvascular dysfunction by reducing ascorbate-sensitive oxidants in healthy older adults
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Dairy cheese consumption ameliorates single-meal sodium-induced cutaneous microvascular dysfunction by reducing ascorbate-sensitive oxidants in healthy older adults
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Dairy cheese consumption ameliorates single-meal sodium-induced cutaneous microvascular dysfunction by reducing ascorbate-sensitive oxidants in healthy older adults
      Available formats
      ×
Copyright
Corresponding author
* Corresponding author: A. E. Stanhewicz, fax +814 865 4602, email axs1056@psu.edu
References
Hide All
1. Mozaffarian, D, Benjamin, EJ, Go, AS, et al. (2015) Heart disease and stroke statistics – 2015 update: a report from the American Heart Association. Circulation 131, e29e322.
2. Crichton, GE & Alkerwi, A (2014) Dairy food intake is positively associated with cardiovascular health: findings from observation of cardiovascular risk factors in Luxembourg study. Nutr Res 34, 10361044.
3. Markey, O, Vasilopoulou, D, Givens, DI, et al. (2014) Dairy and cardiovascular health: friend or foe? Nutr Bull 39, 161171.
4. Wang, L, Manson, JE, Buring, JE, et al. (2008) Dietary intake of dairy products, calcium, and vitamin D and the risk of hypertension in middle-aged and older women. Hypertension 51, 10731079.
5. Ballard, KD & Bruno, RS (2015) Protective role of dairy and its constituents on vascular function independent of blood pressure-lowering activities. Nutr Rev 73, 3650.
6. Xu, JY, Qin, LQ, Wang, PY, et al. (2008) Effect of milk tripeptides on blood pressure: a meta-analysis of randomized controlled trials. Nutrition 24, 933940.
7. Murakami, M, Tonouchi, H, Takahashi, R, et al. (2004) Structural analysis of a new anti-hypertensive peptide (beta-lactosin B) isolated from a commercial whey product. J Dairy Sci 87, 19671974.
8. van der Zander, K, Jakel, M, Bianco, V, et al. (2008) Fermented lactotripeptides-containing milk lowers daytime blood pressure in high normal-to-mild hypertensive subjects. J Hum Hypertens 22, 804806.
9. Xia, Z, Liu, M, Wu, Y, et al. (2006) N-acetylcysteine attenuates TNF-alpha-induced human vascular endothelial cell apoptosis and restores eNOS expression. Eur J Pharmacol 550, 134142.
10. Szabo, C, Hardebo, JE & Salford, LG (1992) Role of endothelium in the responses of human intracranial arteries to a slight reduction of extracellular magnesium. Exp Physiol 77, 209211.
11. Turpeinen, AM, Jarvenpaa, S, Kautiainen, H, et al. (2013) Antihypertensive effects of bioactive tripeptides-a random effects meta-analysis. Ann Med 45, 5156.
12. Jain, SK, Velusamy, T, Croad, JL, et al. (2009) L-cysteine supplementation lowers blood glucose, glycated hemoglobin, CRP, MCP-1, and oxidative stress and inhibits NF-kappaB activation in the livers of Zucker diabetic rats. Free Radic Biol Med 46, 16331638.
13. Tsai, GY, Cui, JZ, Syed, H, et al. (2009) Effect of N-acetylcysteine on the early expression of inflammatory markers in the retina and plasma of diabetic rats. Clin Experiment Ophthalmol 37, 223231.
14. De Mattia, G, Bravi, MC, Laurenti, O, et al. (1998) Reduction of oxidative stress by oral N-acetyl-L-cysteine treatment decreases plasma soluble vascular cell adhesion molecule-1 concentrations in non-obese, non-dyslipidaemic, normotensive, patients with non-insulin-dependent diabetes. Diabetologia 41, 13921396.
15. Elliott, P, Stamler, J, Nichols, R, et al. (1996) Intersalt revisited: further analyses of 24 hour sodium excretion and blood pressure within and across populations. Intersalt Cooperative Research Group. BMJ 312, 12491253.
16. O’Donnell, M, Mente, A & Yusuf, S (2015) Sodium intake and cardiovascular health. Circ Res 116, 10461057.
17. Liu, Y, Rusch, NJ & Lombard, JH (1999) Loss of endothelium and receptor-mediated dilation in pial arterioles of rats fed a short-term high salt diet. Hypertension 33, 686688.
18. Lenda, DM & Boegehold, MA (2002) Effect of a high salt diet on microvascular antioxidant enzymes. J Vasc Res 39, 4150.
19. Nurkiewicz, TR, Wu, G, Li, P, et al. (2010) Decreased arteriolar tetrahydrobiopterin is linked to superoxide generation from nitric oxide synthase in mice fed high salt. Microcirculation 17, 147157.
20. Zhu, J, Mori, T, Huang, T, et al. (2004) Effect of high-salt diet on NO release and superoxide production in rat aorta. Am J Physiol Heart Circ Physiol 286, H575H583.
21. Zhu, J, Huang, T & Lombard, JH (2007) Effect of high-salt diet on vascular relaxation and oxidative stress in mesenteric resistance arteries. J Vasc Res 44, 382390.
22. Jablonski, KL, Racine, ML, Geolfos, CJ, et al. (2013) Dietary sodium restriction reverses vascular endothelial dysfunction in middle-aged/older adults with moderately elevated systolic blood pressure. J Am Coll Cardiol 61, 335343.
23. Jablonski, KL, Gates, PE, Pierce, GL, et al. (2009) Low dietary sodium intake is associated with enhanced vascular endothelial function in middle-aged and older adults with elevated systolic blood pressure. Ther Adv Cardiovasc Dis 3, 347356.
24. Tzemos, N, Lim, PO, Wong, S, et al. (2008) Adverse cardiovascular effects of acute salt loading in young normotensive individuals. Hypertension 51, 15251530.
25. DuPont, JJ, Greaney, JL, Wenner, MM, et al. (2013) High dietary sodium intake impairs endothelium-dependent dilation in healthy salt-resistant humans. J Hypertens 31, 530536.
26. Eisenach, JH, Gullixson, LR, Kost, SL, et al. (2012) Sex differences in salt sensitivity to nitric oxide dependent vasodilation in healthy young adults. J Appl Physiol (1985) 112, 10491053.
27. Dickinson, KM, Clifton, PM & Keogh, JB (2011) Endothelial function is impaired after a high-salt meal in healthy subjects. Am J Clin Nutr 93, 500505.
28. Holowatz, LA, Thompson-Torgerson, CS & Kenney, WL (2008) The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 105, 370372.
29. IJzerman, RG, de Jongh, RT, Beijk, MA, et al. (2003) Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur J Clin Invest 33, 536542.
30. Abularrage, CJ, Sidawy, AN, Aidinian, G, et al. (2005) Evaluation of the microcirculation in vascular disease. J Vasc Surg 42, 574581.
31. Greaney, JL, DuPont, JJ, Lennon-Edwards, SL, et al. (2012) Dietary sodium loading impairs microvascular function independent of blood pressure in humans: role of oxidative stress. J Physiol 590, 55195528.
32. DuPont, JJ, Farquhar, WB & Edwards, DG (2011) Intradermal microdialysis of hypertonic saline attenuates cutaneous vasodilatation in response to local heating. Exp Physiol 96, 674680.
33. Bruning, RS, Santhanam, L, Stanhewicz, AE, et al. (2012) Endothelial nitric oxide synthase mediates cutaneous vasodilation during local heating and is attenuated in middle-aged human skin. J Appl Physiol 112, 20192026.
34. Holowatz, LA & Kenney, WL (2007) Local ascorbate administration augments NO- and non-NO-dependent reflex cutaneous vasodilation in hypertensive humans. Am J Physiol Heart Circ Physiol 293, H1090H1096.
35. Holowatz, LA, Thompson, CS & Kenney, WL (2006) Acute ascorbate supplementation alone or combined with arginase inhibition augments reflex cutaneous vasodilation in aged human skin. Am J Physiol Heart Circ Physiol 291, H2965H2970.
36. Boutrou, R, Gaudichon, C, Dupont, D, et al. (2013) Sequential release of milk protein-derived bioactive peptides in the jejunum in healthy humans. Am J Clin Nutr 97, 13141323.
37. Minson, CT, Berry, LT & Joyner, MJ (2001) Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol (1985) 91, 16191626.
38. Alexander, LM, Kutz, JL & Kenney, WL (2013) Tetrahydrobiopterin increases NO-dependent vasodilation in hypercholesterolemic human skin through eNOS-coupling mechanisms. Am J Physiol Regul Integr Comp Physiol 304, R164R169.
39. Stanhewicz, AE, Greaney, JL, Larry Kenney, W, et al. (2014) Sex- and limb-specific differences in the nitric oxide-dependent cutaneous vasodilation in response to local heating. Am J Physiol Regul Integr Comp Physiol 307, R914R919.
40. Johnson, JM, O’Leary, DS, Taylor, WF, et al. (1986) Effect of local warming on forearm reactive hyperaemia. Clin Physiol 6, 337346.
41. Bruning, RS, Santhanam, L, Stanhewicz, AE, et al. (2012) Endothelial nitric oxide synthase mediates cutaneous vasodilation during local heating and is attenuated in middle-aged human skin. J Appl Physiol (1985) 112, 20192026.
42. Kellogg, DL Jr, Zhao, JL & Wu, Y (2009) Roles of nitric oxide synthase isoforms in cutaneous vasodilation induced by local warming of the skin and whole body heat stress in humans. J Appl Physiol (1985) 107, 14381444.
43. Minson, CT (2010) Thermal provocation to evaluate microvascular reactivity in human skin. J Appl Physiol 109, 12391246.
44. Aburto, NJ, Ziolkovska, A, Hooper, L, et al. (2013) Effect of lower sodium intake on health: systematic review and meta-analyses. BMJ 346, f1326.
45. Moore, LL, Bradlee, ML, Singer, MR, et al. (2012) Dietary Approaches to Stop Hypertension (DASH) eating pattern and risk of elevated blood pressure in adolescent girls. Br J Nutr 108, 16781685.
46. Livingstone, KM, Lovegrove, JA, Cockcroft, JR, et al. (2013) Does dairy food intake predict arterial stiffness and blood pressure in men?: evidence from the Caerphilly Prospective Study. Hypertension 61, 4247.
47. Yoshizawa, M, Maeda, S, Miyaki, A, et al. (2009) Additive beneficial effects of lactotripeptides and aerobic exercise on arterial compliance in postmenopausal women. Am J Physiol Heart Circ Physiol 297, H1899H1903.
48. Crichton, GE, Elias, MF, Dore, GA, et al. (2012) Relations between dairy food intake and arterial stiffness: pulse wave velocity and pulse pressure. Hypertension 59, 10441051.
49. Holowatz, LA, Thompson-Torgerson, C & Kenney, WL (2010) Aging and the control of human skin blood flow. Front Biosci (Landmark Ed) 15, 718739.
50. Minson, CT, Holowatz, LA, Wong, BJ, et al. (2002) Decreased itric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol (1985) 93, 16441649.
51. Botham, KM & Wheeler-Jones, CP (2013) Postprandial lipoproteins and the molecular regulation of vascular homeostasis. Prog Lipid Res 52, 446464.
52. Mah, E, Noh, SK, Ballard, KD, et al. (2011) Postprandial hyperglycemia impairs vascular endothelial function in healthy men by inducing lipid peroxidation and increasing asymmetric dimethylarginine:arginine. J Nutr 141, 19611968.
53. Reid, IR, Bolland, MG, Sambrook, PN, et al. (2011) Calcium supplementation: balancing the cardiovascular risks. Maturitas 69, 289295.
54. Reid, IR, Bolland, MJ & Grey, A (2010) Does calcium supplementation increase cardiovascular risk? Clin Endocrinol (Oxf) 73, 689695.
55. Zhang, QX, Jin, MM, Zhang, L, et al. (2015) Hydrophobicity of whey protein hydrolysates enhances the protective effect against oxidative damage on PC 12 cells. J Dairy Res 82, 17.
56. Ballard, KD, Mah, E, Guo, Y, et al. (2013) Low-fat milk ingestion prevents postprandial hyperglycemia-mediated impairments in vascular endothelial function in obese individuals with metabolic syndrome. J Nutr 143, 16021610.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed