Sodium Intake, Circulating Microvesicles and Cardiovascular Outcomes in Type 2 Diabetes

Author(s): Dorothy Liu, Sara Baqar, Lisa L. Lincz, Elif I. Ekinci*.

Journal Name: Current Diabetes Reviews

Volume 15 , Issue 6 , 2019

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Abstract:

There is ongoing debate surrounding the complex relationship between dietary sodium intake and cardiovascular morbidity and mortality. The existing literature consists largely of observational studies that have demonstrated positive, negative, U-/J-shaped or unclear associations between sodium intake and cardiovascular outcomes. Our group and others have previously demonstrated an inverse relationship between dietary sodium intake and cardiovascular outcomes in people with type 2 diabetes. Increased activity of the renin-angiotensin-aldosterone system and sympathetic nervous system is postulated to contribute to these paradoxical findings through endothelial dysfunction, a precursor to the development of cardiovascular disease. Microvesicles are submicron (0.1 – 1.0μm) vesicles that form during cellular activation, injury or death with endothelial microvesicles being recognized markers of endothelial dysfunction. They are pathologically elevated in a variety of vascular-related conditions including type 2 diabetes. Lower habitual sodium intake in type 2 diabetes has been associated with higher pro-coagulant platelet microvesicles levels but not with endothelial microvesicles. Research utilizing endothelial microvesicles to evaluate the mechanistic relationship between dietary sodium intake and adverse cardiovascular outcomes in type 2 diabetes remains scarce.

Keywords: Cardiovascular disease, endothelial dysfunction, endothelial microvesicles, sodium intake, twenty four hour urinary sodium excretion, type 2 diabetes.

[1]
He FJ, MacGregor GA. A comprehensive review on salt and health and current experience of worldwide salt reduction programmes. J Hum Hypertens 2009; 23(6): 363-84.
[2]
Clifton PM, Keogh JB. Salt restriction in diabetes. Curr Diab Rep 2015; 15(9): 58.
[3]
Powles J, Fahimi S, Micha R, et al. Global, regional and national sodium intakes in 1990 and 2010: a systematic analysis of 24 h urinary sodium excretion and dietary surveys worldwide. BMJ Open 2013; 3(12)e003733
[4]
Committee on the Consequences of Sodium Reduction in P, Food, Nutrition B, Board on Population H, Public Health P, Institute of M. In:Strom BL, Yaktine AL, Oria M, Eds. Sodium Intake in Populations: Assessment of Evidence. Washington (DC): National Academies Press (US) Copyright 2013 by the National Academy of Sciences. All rights reserved. 2013.
[5]
He J, Ogden LG, Vupputuri S, Bazzano LA, Loria C, Whelton PK. Dietary sodium intake and subsequent risk of cardiovascular disease in overweight adults. JAMA 1999; 282(21): 2027-34.
[6]
Tuomilehto J, Jousilahti P, Rastenyte D, et al. Urinary sodium excretion and cardiovascular mortality in Finland: a prospective study. Lancet 2001; 357(9259): 848-51.
[7]
He FJ, MacGregor GA. Effect of modest salt reduction on blood pressure: a meta-analysis of randomized trials. Implications for public health. J Hum Hypertens 2002; 16(11): 761-70.
[8]
Umesawa M, Iso H, Date C, et al. Relations between dietary sodium and potassium intakes and mortality from cardiovascular disease: the Japan Collaborative Cohort Study for Evaluation of Cancer Risks. Am J Clin Nutr 2008; 88(1): 195-202.
[9]
Horikawa C, Yoshimura Y, Kamada C, et al. Dietary sodium intake and incidence of diabetes complications in Japanese patients with type 2 diabetes: analysis of the Japan Diabetes Complications Study (JDCS). J Clin Endocrinol Metab 2014; 99(10): 3635-43.
[10]
Kalogeropoulos AP, Georgiopoulou VV, Murphy RA, et al. Dietary sodium content, mortality, and risk for cardiovascular events in older adults: the Health, Aging, and Body Composition (Health ABC) Study. JAMA Intern Med 2015; 175(3): 410-9.
[11]
Cook NR, Appel LJ, Whelton PK. Sodium intake and all-cause mortality over 20 years in the trials of hypertension prevention. J Am Coll Cardiol 2016; 68(15): 1609-17.
[12]
Alderman MH, Cohen H, Madhavan S. Dietary sodium intake and mortality: the National Health and Nutrition Examination Survey (NHANES I). Lancet 1998; 351(9105): 781-5.
[13]
Cohen HW, Hailpern SM, Fang J, Alderman MH. Sodium intake and mortality in the NHANES II follow-up study. Am J Med 2006; 119(3): 275.e7-275.e14.
[14]
Cohen HW, Hailpern SM, Alderman MH. Sodium intake and mortality follow-up in the Third National Health and Nutrition Examination Survey (NHANES III). J Gen Intern Med 2008; 23(9): 1297-302.
[15]
Stolarz-Skrzypek K, Kuznetsova T, Thijs L, et al. Fatal and nonfatal outcomes, incidence of hypertension, and blood pressure changes in relation to urinary sodium excretion. JAMA 2011; 305(17): 1777-85.
[16]
Ekinci EI, Clarke S, Thomas MC, et al. Dietary salt intake and mortality in patients with type 2 diabetes. Diabetes Care 2011; 34(3): 703-9.
[17]
Ekinci EI, Moran JL, Thomas MC, et al. Relationship between urinary sodium excretion over time and mortality in type 2 diabetes. Diabetes Care 2014; 37(4): e62-3.
[18]
O’Donnell MJ, Yusuf S, Mente A, et al. Urinary sodium and potassium excretion and risk of cardiovascular events. JAMA 2011; 306(20): 2229-38.
[19]
O’Donnell M, Mente A, Rangarajan S, et al. Urinary sodium and potassium excretion, mortality, and cardiovascular events. N Engl J Med 2014; 371(7): 612-23.
[20]
Graudal N, Jürgens G, Baslund B, Alderman MH. Compared with usual sodium intake, low- and excessive-sodium diets are associated with increased mortality: a meta-analysis. Am J Hypertens 2014; 27(9): 1129-37.
[21]
Mente A, O’Donnell M, Rangarajan S, et al. Associations of urinary sodium excretion with cardiovascular events in individuals with and without hypertension: a pooled analysis of data from four studies. The Lancet 2016.
[22]
Thomas MC, Moran J, Forsblom C, et al. The association between dietary sodium intake, ESRD, and all-cause mortality in patients with type 1 diabetes. Diabetes Care 2011; 34(4): 861-6.
[23]
Adler AJ, Taylor F, Martin N, Gottlieb S, Taylor RS, Ebrahim S. Reduced dietary salt for the prevention of cardiovascular disease. Cochrane Database Syst Rev 2014; 12CD009217
[24]
Graudal NA, Hubeck-Graudal T, Jürgens G. Effects of low-sodium diet vs. high-sodium diet on blood pressure, renin, aldosterone, catecholamines, cholesterol, and triglyceride (Cochrane Review). Am J Hypertens 2012; 25(1): 1-15.
[25]
Burger D, Schock S, Thompson CS, Montezano AC, Hakim AM, Touyz RM. Microparticles: biomarkers and beyond. Clin Sci (Colch) 2013; 124(7): 423-41.
[26]
Ekinci EI, Cheong KY, Dobson M, et al. High sodium and low potassium intake in patients with Type 2 diabetes. Diabet Med 2010; 27(12): 1401-8.
[27]
Holbrook JT, Patterson KY, Bodner JE, et al. Sodium and potassium intake and balance in adults consuming self-selected diets. Am J Clin Nutr 1984; 40(4): 786-93.
[28]
Mente A, O’Donnell MJ, Dagenais G, et al. Validation and comparison of three formulae to estimate sodium and potassium excretion from a single morning fasting urine compared to 24-h measures in 11 countries. J Hypertens 2014; 32(5): 1005-15.
[29]
Tanaka T, Okamura T, Miura K, et al. A simple method to estimate populational 24-h urinary sodium and potassium excretion using a casual urine specimen. J Hum Hypertens 2002; 16(2): 97-103.
[30]
Brown IJ, Dyer AR, Chan Q, Cogswell ME, Ueshima H, Stamler J, et al. Estimating 24-hour urinary sodium excretion from casual urinary sodium concentrations in Western populations: the INTERSALT study. Am J Epidemiol 2013; 177(11): 1180-92.
[31]
Kawasaki T, Itoh K, Uezono K, Sasaki H. A simple method for estimating 24 h urinary sodium and potassium excretion from second morning voiding urine specimen in adults. Clin Exp Pharmacol Physiol 1993; 20(1): 7-14.
[32]
Peng Y, Li W, Wang Y, et al. Validation and assessment of three methods to estimate 24-h urinary sodium excretion from spot urine samples in chinese adults. PLoS One 2016; 11(2)e0149655
[33]
McLean RM, Farmer VL, Nettleton A, Cameron CM, Cook NR, Campbell NRC. Assessment of dietary sodium intake using a food frequency questionnaire and 24-hour urinary sodium excretion: a systematic literature review. J Clin Hypertens (Greenwich) 2017; 19(12): 1214-30.
[34]
Alderman MH, Madhavan S, Cohen H, Sealey JE, Laragh JH. Low urinary sodium is associated with greater risk of myocardial infarction among treated hypertensive men. Hypertension 1995; 25(6): 1144-52.
[35]
Katz J. Sodium and cardiovascular disease. Lancet 2016; 388(10056): 2112-3.
[36]
Group HPTR. The Hypertension Prevention Trial: three-year effects of dietary changes on blood pressure. Hypertension Prevention Trial Research Group. Arch Intern Med 1990; 150(1): 153-62.
[37]
Whelton PK, Appel L, Charleston J, et al. The effects of nonpharmacologic interventions on blood pressure of persons with high normal levels. Results of the Trials of Hypertension Prevention, Phase I. JAMA 1992; 267(9): 1213-20.
[38]
Group ToHPCR. Effects of weight loss and sodium reduction intervention on blood pressure and hypertension incidence in overweight people with high-normal blood pressure. The Trials of Hypertension Prevention, phase II. Arch Intern Med 1997; 157(6): 657.
[39]
Morgan T, Adam W, Gillies A, Wilson M, Morgan G, Carney S. Hypertension treated by salt restriction. Lancet 1978; 1(8058): 227-30.
[40]
Whelton PK, Appel LJ, Espeland MA, et al. Sodium reduction and weight loss in the treatment of hypertension in older persons: a randomized controlled trial of nonpharmacologic interventions in the elderly (TONE). TONE Collaborative Research Group. JAMA 1998; 279(11): 839-46.
[41]
Chang HY, Hu YW, Yue CS, et al. Effect of potassium-enriched salt on cardiovascular mortality and medical expenses of elderly men. Am J Clin Nutr 2006; 83(6): 1289-96.
[42]
Group TCSSSC. Salt substitution: a low-cost strategy for blood pressure control among rural Chinese. A randomized, controlled trial. J Hypertens 2007; 25(10): 2011-8.
[43]
Kwok TC, Lam LC, Sea MM, Goggins W, Woo J. A randomized controlled trial of dietetic interventions to prevent cognitive decline in old age hostel residents. Eur J Clin Nutr 2012; 66(10): 1135-40.
[44]
Bibbins-Domingo K. The institute of medicine report sodium intake in populations: assessment of evidence: summary of primary findings and implications for clinicians. JAMA Intern Med 2014; 174(1): 136-7.
[45]
Mitka M. IOM report: Evidence fails to support guidelines for dietary salt reduction. JAMA 2013; 309(24): 2535-6.
[46]
Evert AB, Boucher JL, Cypress M, et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care 2014; 37(Suppl. 1): S120-43.
[47]
Kong YW, Baqar S, Jerums G, Ekinci EI. Sodium and its role in cardiovascular disease - the debate continues. Front Endocrinol 2016; 7: 164.
[48]
Graudal NA, Hubeck-Graudal T, Jurgens G. Effects of low sodium diet versus high sodium diet on blood pressure, renin, aldosterone, catecholamines, cholesterol, and triglyceride. Cochrane Database Syst Rev 2017; 4CD004022
[49]
Britten MB, Zeiher AM, Schächinger V. Clinical importance of coronary endothelial vasodilator dysfunction and therapeutic options. J Intern Med 1999; 245(4): 315-27.
[50]
Tikellis C, Pickering RJ, Tsorotes D, et al. Activation of the Renin-Angiotensin system mediates the effects of dietary salt intake on atherogenesis in the apolipoprotein E knockout mouse. Hypertension 2012; 60(1): 98-105.
[51]
Tikellis C, Pickering RJ, Tsorotes D, et al. Association of dietary sodium intake with atherogenesis in experimental diabetes and with cardiovascular disease in patients with Type 1 diabetes. Clinical science (London, England : 1979) 2013; 124(10): 617-26.
[52]
Brunner HR, Laragh JH, Baer L, et al. Essential hypertension: renin and aldosterone, heart attack and stroke. N Engl J Med 1972; 286(9): 441-9.
[53]
Sealey JE, Alderman MH, Furberg CD, Laragh JH. Renin-angiotensin system blockers may create more risk than reward for sodium-depleted cardiovascular patients with high plasma renin levels. Am J Hypertens 2013; 26(6): 727-38.
[54]
Verma S, Gupta M, Holmes DT, et al. Plasma renin activity predicts cardiovascular mortality in the Heart Outcomes Prevention Evaluation (HOPE) study. Eur Heart J 2011; 32(17): 2135-42.
[55]
Libianto R, Jerums G, Lam Q, et al. Relationship between urinary sodium excretion and serum aldosterone in patients with diabetes in the presence and absence of modifiers of the renin-angiotensin-aldosterone system. Clinical Sci (London, England : 1979) 2014; 126(2): 147-54..
[56]
Chen A, Jerums G, Baqar S, et al. Short-term dietary salt supplementation blunts telmisartan induced increases in plasma renin activity in hypertensive patients with type 2 diabetes mellitus. Clin Sci (Colch) 2015; 129(5): 415-22.
[57]
Puddu P, Puddu GM, Cravero E, Muscari S, Muscari A. The involvement of circulating microparticles in inflammation, coagulation and cardiovascular diseases. Can J Cardiol 2010; 26(4): 140-5.
[58]
Curtis AM, Edelberg J, Jonas R, et al. Endothelial microparticles: sophisticated vesicles modulating vascular function. Vasc Med 2013; 18(4): 204-14.
[59]
Tramontano AF, Lyubarova R, Tsiakos J, Palaia T, Deleon JR, Ragolia L. Circulating endothelial microparticles in diabetes mellitus. Mediators Inflamm 2010; 2010250476
[60]
Lawson C, Vicencio JM, Yellon DM, Davidson SM. Microvesicles and exosomes: new players in metabolic and cardiovascular disease. J Endocrinol 2016; 228(2): R57-71.
[61]
Chen Y, Li G, Liu M-L. Microvesicles as emerging biomarkers and therapeutic targets in cardiometabolic diseases. Genomics Proteomics Bioinformatics 2018; 16(1): 50-62.
[62]
Chandler WL. Measurement of microvesicle levels in human blood using flow cytometry. Cytometry Part B: Clinical Cytometry 2016.
[63]
França C, Izar MCdO, Amaral JBd, Tegani DM, Fonseca FAH. Microparticles as potential biomarkers of cardiovascular disease. Arquivos brasileiros de cardiologia 2015; 104(2): 169-74.
[64]
Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 2011; 31(1): 27-33.
[65]
Koga H, Sugiyama S, Kugiyama K, et al. Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 2005; 45(10): 1622-30.
[66]
Feng B, Chen Y, Luo Y, Chen M, Li X, Ni Y. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus. Atherosclerosis 2010; 208(1): 264-9.
[67]
Jung KH, Chu K, Lee ST, et al. Risk of macrovascular complications in type 2 diabetes mellitus: endothelial microparticle profiles. Cerebrovasc Dis 2011; 31(5): 485-93.
[68]
Chen Y, Feng B, Li X, Ni Y, Luo Y. Plasma endothelial microparticles and their correlation with the presence of hypertension and arterial stiffness in patients with type 2 diabetes. J Clin Hypertens (Greenwich) 2012; 14(7): 455-60.
[69]
Li S, Wei J, Zhang C, et al. Cell-derived microparticles in patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Cellular Physiol Biochem: Int J Experiment Cellular Physiol Biochem Pharmacol 2016; 39(6): 2439-50.
[70]
Preston RA, Jy W, Jimenez JJ, et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41(2): 211-7.
[71]
Wang JM, Su C, Wang Y, et al. Elevated circulating endothelial microparticles and brachial-ankle pulse wave velocity in well-controlled hypertensive patients. J Hum Hypertens 2009; 23(5): 307-15.
[72]
Huang PH, Huang SS, Chen YH, et al. Increased circulating CD31+/annexin V+ apoptotic microparticles and decreased circulating endothelial progenitor cell levels in hypertensive patients with microalbuminuria. J Hypertens 2010; 28(8): 1655-65.
[73]
Bernal-Mizrachi L, Jy W, Fierro C, et al. Endothelial microparticles correlate with high-risk angiographic lesions in acute coronary syndromes. Int J Cardiol 2004; 97(3): 439-46.
[74]
Nozaki T, Sugiyama S, Koga H, et al. Significance of a multiple biomarkers strategy including endothelial dysfunction to improve risk stratification for cardiovascular events in patients at high risk for coronary heart disease. J Am Coll Cardiol 2009; 54(7): 601-8.
[75]
Sinning JM, Losch J, Walenta K, Böhm M, Nickenig G, Werner N. Circulating CD31+/Annexin V+ microparticles correlate with cardiovascular outcomes. Eur Heart J 2011; 32(16): 2034-41.
[76]
Bernal-Mizrachi L, Jy W, Jimenez JJ, et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J 2003; 145(6): 962-70.
[77]
Boulanger CM, Scoazec A, Ebrahimian T, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 2001; 104(22): 2649-52.
[78]
Cherian P, Hankey GJ, Eikelboom JW, et al. Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes. Stroke 2003; 34(9): 2132-7.
[79]
Williams JB, Jauch EC, Lindsell CJ, Campos B. Endothelial microparticle levels are similar in acute ischemic stroke and stroke mimics due to activation and not apoptosis/necrosis. Academic Emergency Med: Official J Society Academic Emergency Med 2007; 14(8): 685-90.
[80]
Simak J, Gelderman MP, Yu H, Wright V, Baird AE. Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. JTH 2006; 4(6): 1296-302.
[81]
Wang Y, Chen LM, Liu ML. Microvesicles and diabetic complications--novel mediators, potential biomarkers and therapeutic targets. Chung Kuo Yao Li Hsueh Pao 2014; 35(4): 433-43.
[82]
Bernard S, Loffroy R, Sérusclat A, et al. Increased levels of endothelial microparticles CD144 (VE-Cadherin) positives in type 2 diabetic patients with coronary noncalcified plaques evaluated by multidetector computed tomography (MDCT). Atherosclerosis 2009; 203(2): 429-35.
[83]
Shantsila E. Endothelial microparticles: a universal marker of vascular health [quest]. J Hum Hypertens 2008; 23(5): 359-61.
[84]
Kuvin JT, Karas RH. Clinical utility of endothelial function testing. Circulation 2003; 107(25): 3243-7.
[85]
Flammer AJ, Anderson T, Celermajer DS, et al. The assessment of endothelial function. Circulation 2012; 126(6): 753-67.
[86]
Cordazzo C, Neri T, Petrini S, et al. Angiotensin II induces the generation of procoagulant microparticles by human mononuclear cells via an angiotensin type 2 receptor-mediated pathway. Thromb Res 2013; 131(4): e168-74.
[87]
Martinez Silvestre M. The effects of eprosartan on cytoplasmic free calcium mobilisation, platelet activation and microparticle formation in hypertension. could they be relevant to stroke prevention? JRAAS 2005; 6(1_suppl): S1-3.
[88]
Moriya H, Kobayashi S, Ohtake T, et al. Aliskiren, a direct renin inhibitor, improves vascular endothelial function in patients on hemodialysis independent of antihypertensive effect approximately a pilot study approximately. Kidney Blood Press Res 2013; 37(2-3): 190-8.
[89]
Nomura S, Shouzu A, Omoto S, Nishikawa M, Fukuhara S, Iwasaka T. Effect of valsartan on monocyte/endothelial cell activation markers and adiponectin in hypertensive patients with type 2 diabetes mellitus. Thromb Res 2006; 117(4): 385-92.
[90]
Baqar S, Liu D, Lincz LF, Kong YW, Jerums G, Ekinci EI. The relationship between habitual dietary sodium intake and RAAS blockade on circulating microparticle levels in type two diabetes. Clin Sci (Colch) 2018; 132(20): 2207-20.


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VOLUME: 15
ISSUE: 6
Year: 2019
Page: [435 - 445]
Pages: 11
DOI: 10.2174/1573399815666190212120822
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