Effect of dose and duration of reduction in dietary sodium on blood pressure levels: systematic review and meta-analysis of randomised trials

Liping Huang, Kathy Trieu, Sohei Yoshimura, Bruce Neal, Mark Woodward, Norm R C Campbell, Qiang Li, Daniel T Lackland, Alexander A Leung, Cheryl A M Anderson, Graham A MacGregor, Feng J He, Liping Huang, Kathy Trieu, Sohei Yoshimura, Bruce Neal, Mark Woodward, Norm R C Campbell, Qiang Li, Daniel T Lackland, Alexander A Leung, Cheryl A M Anderson, Graham A MacGregor, Feng J He

Abstract

Objective: To examine the dose-response relation between reduction in dietary sodium and blood pressure change and to explore the impact of intervention duration.

Design: Systematic review and meta-analysis following PRISMA guidelines.

Data sources: Ovid MEDLINE(R), EMBASE, and Cochrane Central Register of Controlled Trials (Wiley) and reference lists of relevant articles up to 21 January 2019.

Inclusion criteria: Randomised trials comparing different levels of sodium intake undertaken among adult populations with estimates of intake made using 24 hour urinary sodium excretion.

Data extraction and analysis: Two of three reviewers screened the records independently for eligibility. One reviewer extracted all data and the other two reviewed the data for accuracy. Reviewers performed random effects meta-analyses, subgroup analyses, and meta-regression.

Results: 133 studies with 12 197 participants were included. The mean reductions (reduced sodium v usual sodium) of 24 hour urinary sodium, systolic blood pressure (SBP), and diastolic blood pressure (DBP) were 130 mmol (95% confidence interval 115 to 145, P<0.001), 4.26 mm Hg (3.62 to 4.89, P<0.001), and 2.07 mm Hg (1.67 to 2.48, P<0.001), respectively. Each 50 mmol reduction in 24 hour sodium excretion was associated with a 1.10 mm Hg (0.66 to 1.54; P<0.001) reduction in SBP and a 0.33 mm Hg (0.04 to 0.63; P=0.03) reduction in DBP. Reductions in blood pressure were observed in diverse population subsets examined, including hypertensive and non-hypertensive individuals. For the same reduction in 24 hour urinary sodium there was greater SBP reduction in older people, non-white populations, and those with higher baseline SBP levels. In trials of less than 15 days' duration, each 50 mmol reduction in 24 hour urinary sodium excretion was associated with a 1.05 mm Hg (0.40 to 1.70; P=0.002) SBP fall, less than half the effect observed in studies of longer duration (2.13 mm Hg; 0.85 to 3.40; P=0.002). Otherwise, there was no association between trial duration and SBP reduction.

Conclusions: The magnitude of blood pressure lowering achieved with sodium reduction showed a dose-response relation and was greater for older populations, non-white populations, and those with higher blood pressure. Short term studies underestimate the effect of sodium reduction on blood pressure.

Systematic review registration: PROSPERO CRD42019140812.

Conflict of interest statement

Competing interests: All authors have completed the ICMJE uniform disclosure form at www.icmje.org/coi_disclosure.pdf and declare: no support from any organisation for the submitted work. Outside this work, BN has received salt substitute for trials from Salt Manufacturing Company in China and Nutek; MW is supported by the National Health and Medical Research Foundation of Australia grants (1080206 and 1149987) and receives personal fees from Amgen, personal fees from Kirin; NRCC is an unpaid member of World Action on Salt and Health and an unpaid consultant on dietary sodium and hypertension control to numerous governmental and non-governmental organisations; AAL is funded by the Hypertension Canada New Investigator Award; FJH is a member of Consensus Action on Salt and Health (CASH) and World Action on Salt and Health (WASH). Both CASH and WASH are non-profit charitable organisations and FJH does not receive any financial support from CASH or WASH; GAM is the Chairman of Blood Pressure UK (BPUK), Chairman of Consensus Action on Salt and Health (CASH) and Chairman of World Action on Salt and Health (WASH). BPUK, CASH and WASH are non-profit charitable organisations and GAM does not receive any financial support from any of these organisations.

Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions.

Figures

Fig 1
Fig 1
Flowchart for inclusion criteria
Fig 2
Fig 2
Association of magnitude of sodium reduction (mmol) with size of blood pressure reduction (mm Hg)
Fig 3
Fig 3
Effects of age, sex, ethnicity, baseline sodium intake, baseline blood pressure, and blood pressure status on the size of blood pressure reduction (mm Hg) achieved with a 50 mmol reduction in sodium excretion
Fig 4
Fig 4
Association of duration of sodium reduction intervention with size of blood pressure reduction (mm Hg)
https://www.ncbi.nlm.nih.gov/pmc/articles/instance/7190039/bin/hual051597.va.jpg

References

    1. GBD 2017 Causes of Death Collaborators Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018;392:1736-88. 10.1016/S0140-6736(18)32203-7
    1. Denton D, Weisinger R, Mundy NI, et al. The effect of increased salt intake on blood pressure of chimpanzees. Nat Med 1995;1:1009-16. 10.1038/nm1095-1009
    1. Intersalt Cooperative Research Group Intersalt: an international study of electrolyte excretion and blood pressure. Results for 24 hour urinary sodium and potassium excretion. BMJ 1988;297:319-28. 10.1136/bmj.297.6644.319
    1. Walkowska A, Kuczeriszka M, Sadowski J, et al. High salt intake increases blood pressure in normal rats: putative role of 20-HETE and no evidence on changes in renal vascular reactivity. Kidney Blood Press Res 2015;40:323-34. 10.1159/000368508
    1. Michell AR. Physiological aspects of the requirement for sodium in mammals. Nutr Res Rev 1989;2:149-60. 10.1079/NRR19890012
    1. Powles J, Fahimi S, Micha R, et al. Global Burden of Diseases Nutrition and Chronic Diseases Expert Group (NutriCoDE) 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:e003733. 10.1136/bmjopen-2013-003733
    1. World Health Organization Guideline: Sodium intake for adults and children. World Health Organization, 2012.
    1. Scientific Advisory Committee on Nutrition Salt and health. The Stationery Office, 2003.
    1. US Department of Health and Human Services and US Department of Agriculture. 2015-2020 Dietary guidelines for Americans. 8th Ed. .
    1. World Health Organization Global action plan for the prevention and control of noncommunicable diseases 2013-2020: World Health Organization. WHO, 2013.
    1. Graudal N, Hubeck-Graudal T, Jürgens G, Taylor RS. Dose-response relation between dietary sodium and blood pressure: a meta-regression analysis of 133 randomized controlled trials. Am J Clin Nutr 2019;109:1273-8. 10.1093/ajcn/nqy384
    1. 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;4:CD004022. 10.1002/14651858.CD004022.pub4
    1. 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;27:1129-37. 10.1093/ajh/hpu028
    1. Zhu Y, Zhang J, Li Z, et al. Association of sodium intake and major cardiovascular outcomes: a dose-response meta-analysis of prospective cohort studies. BMC Cardiovasc Disord 2018;18:192. 10.1186/s12872-018-0927-9
    1. Cappuccio FP, Beer M, Strazzullo P, European Salt Action Network Population dietary salt reduction and the risk of cardiovascular disease. A scientific statement from the European Salt Action Network. Nutr Metab Cardiovasc Dis 2018;29:107-14. 10.1016/j.numecd.2018.11.010
    1. He FJ, Campbell NRC, Ma Y, MacGregor GA, Cogswell ME, Cook NR. Errors in estimating usual sodium intake by the Kawasaki formula alter its relationship with mortality: implications for public health. Int J Epidemiol 2018;47:1784-95. 10.1093/ije/dyy114
    1. Wang M, Moran AE, Liu J, et al. A meta-analysis of effect of dietary salt restriction on blood pressure in Chinese adults. Glob Heart 2015;10:291-299.e6. 10.1016/j.gheart.2014.10.009
    1. Newberry SJ, Chung M, Anderson CAM, et al. Sodium and potassium intake: effects on chronic disease outcomes and risks. Rockville (MD) Agency for Healthcare Research and Quality (US) 2018
    1. Midgley JP, Matthew AG, Greenwood CM, Logan AG. Effect of reduced dietary sodium on blood pressure: a meta-analysis of randomized controlled trials. JAMA 1996;275:1590-7. 10.1001/jama.1996.03530440070039
    1. Huang L, Crino M, Wu JH, et al. Mean population salt intake estimated from 24-h urine samples and spot urine samples: a systematic review and meta-analysis. Int J Epidemiol 2016;45:239-50. 10.1093/ije/dyv313
    1. He FJ, Li J, Macgregor GA. Effect of longer term modest salt reduction on blood pressure: Cochrane systematic review and meta-analysis of randomised trials. BMJ 2013;346:f1325. 10.1136/bmj.f1325
    1. Graudal N, Hubeck-Graudal T, Jürgens G, McCarron DA. The significance of duration and amount of sodium reduction intervention in normotensive and hypertensive individuals: a meta-analysis. Adv Nutr 2015;6:169-77. 10.3945/an.114.007708
    1. TRUE Consortium (inTernational consoRtium for qUality resEarch on dietary sodium/salt) Recommended standards for assessing blood pressure in human research where blood pressure or hypertension is a major focus. J Clin Hypertens (Greenwich) 2017;19:108-13. 10.1111/jch.12948
    1. Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions 2008.
    1. McCarron DA, Kazaks AG, Geerling JC, Stern JS, Graudal NA. Normal range of human dietary sodium intake: a perspective based on 24-hour urinary sodium excretion worldwide. Am J Hypertens 2013;26:1218-23. 10.1093/ajh/hpt139
    1. He FJ, MacGregor GA. Role of salt intake in prevention of cardiovascular disease: controversies and challenges. Nat Rev Cardiol 2018;15:371-7. 10.1038/s41569-018-0004-1
    1. Parijs J, Joossens JV, Van der Linden L, Verstreken G, Amery AK. Moderate sodium restriction and diuretics in the treatment of hypertension. Am Heart J 1973;85:22-34. 10.1016/0002-8703(73)90522-X
    1. Mark AL, Lawton WJ, Abboud FM, Fitz AE, Connor WE, Heistad DD. Effects of high and low sodium intake on arterial pressure and forearm vasular resistance in borderline hypertension. A preliminary report. Circ Res 1975;36(Suppl 1):194-8. 10.1161/01.RES.36.6.194
    1. Morgan TO, Myers JB. Hypertension treated by sodium restriction. Med J Aust 1981;2:396-7. 10.5694/j.1326-5377.1981.tb101026.x
    1. Skrabal F, Auböck J, Hörtnagl H. Low sodium/high potassium diet for prevention of hypertension: probable mechanisms of action. Lancet 1981;2:895-900. 10.1016/S0140-6736(81)91392-1
    1. MacGregor GA, Markandu ND, Best FE, et al. Double-blind randomised crossover trial of moderate sodium restriction in essential hypertension. Lancet 1982;1:351-5. 10.1016/S0140-6736(82)91389-7
    1. Puska P, Iacono JM, Nissinen A, et al. Controlled, randomised trial of the effect of dietary fat on blood pressure. Lancet 1983;1:1-5. 10.1016/S0140-6736(83)91556-8
    1. Silman AJ, Locke C, Mitchell P, Humpherson P. Evaluation of the effectiveness of a low sodium diet in the treatment of mild to moderate hypertension. Lancet 1983;1:1179-82. 10.1016/S0140-6736(83)92463-7
    1. Watt GCM, Edwards C, Hart JT, Hart M, Walton P, Foy CJ. Dietary sodium restriction for mild hypertension in general practice. Br Med J (Clin Res Ed) 1983;286:432-6. 10.1136/bmj.286.6363.432
    1. Erwteman TM, Nagelkerke N, Lubsen J, Koster M, Dunning AJ. Beta blockade, diuretics, and salt restriction for the management of mild hypertension: a randomised double blind trial. Br Med J (Clin Res Ed) 1984;289:406-9. 10.1136/bmj.289.6442.406
    1. Gillies AH, Carney SL, Smith AJ, Waga SM. Adjunctive effect of salt restriction on antihypertensive efficacy. Clin Exp Pharmacol Physiol 1984;11:395-8. 10.1111/j.1440-1681.1984.tb00286.x
    1. Koolen MI, van Brummelen P. Sodium sensitivity in essential hypertension: role of the renin-angiotensin-aldosterone system and predictive value of an intravenous frusemide test. J Hypertens 1984;2:55-9. 10.1097/00004872-198402000-00010
    1. Koolen MI, van Brummelen P. Adrenergic activity and peripheral hemodynamics in relation to sodium sensitivity in patients with essential hypertension. Hypertension 1984;6:820-5. 10.1161/01.HYP.6.6.820
    1. Maxwell MH, Kushiro T, Dornfeld LP, Tuck ML, Waks AU. BP changes in obese hypertensive subjects during rapid weight loss. Comparison of restricted v unchanged salt intake. Arch Intern Med 1984;144:1581-4. 10.1001/archinte.1984.00350200073012
    1. Myers JB, Morgan TO. Effect of alteration in sodium chloride intake on blood pressure of normotensive subjects. J Cardiovasc Pharmacol 1984;6(Suppl 1):S204-9. 10.1097/00005344-198400061-00032
    1. Richards AM, Nicholls MG, Espiner EA, et al. Blood-pressure response to moderate sodium restriction and to potassium supplementation in mild essential hypertension. Lancet 1984;1:757-61. 10.1016/S0140-6736(84)91276-5
    1. Skrabal F, Herholz H, Neumayr M, et al. Salt sensitivity in humans is linked to enhanced sympathetic responsiveness and to enhanced proximal tubular reabsorption. Hypertension 1984;6:152-8. 10.1161/01.HYP.6.2.152
    1. Resnick LM, Nicholson JP, Laragh JH. Alterations in calcium metabolism mediate dietary salt sensitivity in essential hypertension. Trans Assoc Am Physicians 1985;98:313-21.
    1. Skrabal F, Hamberger L, Cerny E. Salt sensitivity in normotensives with and salt resistance in normotensives without heredity of hypertension. Scand J Clin Lab Invest Suppl 1985;176(suppl. 176):47-57.
    1. Ashry A, Heagerty AM, Alton SM, Bing RF, Swales JD, Thurston H. Effects of manipulation of sodium balance on erythrocyte sodium transport. J Hum Hypertens 1987;1:105-11.
    1. Grobbee DE, Hofman A, Roelandt JT, Boomsma F, Schalekamp MA, Valkenburg HA. Sodium restriction and potassium supplementation in young people with mildly elevated blood pressure. J Hypertens 1987;5:115-9. 10.1097/00004872-198702000-00016
    1. MacGregor GA, Markandu ND, Singer DRJ, Cappuccio FP, Shore AC, Sagnella GA. Moderate sodium restriction with angiotensin converting enzyme inhibitor in essential hypertension: a double blind study. Br Med J (Clin Res Ed) 1987;294:531-4. 10.1136/bmj.294.6571.531
    1. Morgan T, Anderson A. Sodium restriction can delay the return of hypertension in patients previously well-controlled on drug therapy. Can J Physiol Pharmacol 1987;65:1752-5. 10.1139/y87-274
    1. Lawton WJ, Sinkey CA, Fitz AE, Mark AL. Dietary salt produces abnormal renal vasoconstrictor responses to upright posture in borderline hypertensive subjects. Hypertension 1988;11:529-36. 10.1161/01.HYP.11.6.529
    1. Morgan T, Anderson A. Interaction in hypertensive man between sodium intake, converting enzyme inhibitor (enalapril), plasma renin and blood pressure control. J Hum Hypertens 1988;1:311-5.
    1. Morgan T, Anderson A. Interaction of slow-channel calcium blocking drugs with sodium restriction, diuretics and angiotensin converting enzyme inhibitors. J Hypertens Suppl 1988;6(4):S652-4. 10.1097/00004872-198812040-00205
    1. Nowson CA, Morgan TO. Change in blood pressure in relation to change in nutrients effected by manipulation of dietary sodium and potassium. Clin Exp Pharmacol Physiol 1988;15:225-42. 10.1111/j.1440-1681.1988.tb01065.x
    1. Staessen J, Bulpitt CJ, Fagard R, Joossens JV, Lijnen P, Amery A. Salt intake and blood pressure in the general population: a controlled intervention trial in two towns. J Hypertens 1988;6:965-73. 10.1097/00004872-198812000-00003
    1. Chalmers JP, Doyle AE, Hopper JL, et al. Australian National Health and Medical Research Council Dietary Salt Study Management Committee Fall in blood pressure with modest reduction in dietary salt intake in mild hypertension. Lancet 1989;1:399-402.
    1. Chalmers JP, Doyle AE, Hopper JL, et al. Effects of replacing sodium intake in subjects on a low sodium diet: a crossover study. Australian National Health & Medical Research Council Dietary Salt Study Management Committee. Clin Exp Hypertens A 1989;11:1011-24. 10.3109/10641968909035388
    1. Dodson PM, Beevers M, Hallworth R, Webberley MJ, Fletcher RF, Taylor KG. Sodium restriction and blood pressure in hypertensive type II diabetics: randomised blind controlled and crossover studies of moderate sodium restriction and sodium supplementation. BMJ 1989;298:227-30. 10.1136/bmj.298.6668.227
    1. Hargreaves M, Morgan TO, Snow R, Guerin M. Exercise tolerance in the heat on low and normal salt intakes. Clin Sci (Lond) 1989;76:553-7. 10.1042/cs0760553
    1. MacGregor GA, Markandu ND, Sagnella GA, Singer DR, Cappuccio FP. Double-blind study of three sodium intakes and long-term effects of sodium restriction in essential hypertension. Lancet 1989;2:1244-7. 10.1016/S0140-6736(89)91852-7
    1. Bruun NE, Skøtt P, Damkjaer Nielsen M, et al. Normal renal tubular response to changes of sodium intake in hypertensive man. J Hypertens 1990;8:219-27.
    1. Parker M, Puddey IB, Beilin LJ, Vandongen R. Two-way factorial study of alcohol and salt restriction in treated hypertensive men. Hypertension 1990;16:398-406. 10.1161/01.HYP.16.4.398
    1. Del Río A, Rodríguez-Villamil JL, López-Campos JM, Carrera F. [Effect of moderate salt restriction on the antihypertensive action of nifedipine: a double blind study]. Rev Clin Esp 1990;186:5-10.
    1. Sharma AM, Arntz HR, Kribben A, Schattenfroh S, Distler A. Dietary sodium restriction: adverse effect on plasma lipids. Klin Wochenschr 1990;68:664-8. 10.1007/BF01667013
    1. Sharma AM, Kribben A, Schattenfroh S, Cetto C, Distler A. Salt sensitivity in humans is associated with abnormal acid-base regulation. Hypertension 1990;16:407-13. 10.1161/01.HYP.16.4.407
    1. Carney SL, Gillies AH, Smith AJ, Smitham S. Increased dietary sodium chloride in patients treated with antihypertensive drugs. Clin Exp Hypertens A 1991;13:401-7. 10.3109/10641969109045059
    1. Creager MA, Roddy MA, Holland KM, Hirsch AT, Dzau VJ. Sodium depresses arterial baroreceptor reflex function in normotensive humans. Hypertension 1991;17:989-96. 10.1161/01.HYP.17.6.989
    1. Sharma AM, Ruland K, Spies KP, Distler A. Salt sensitivity in young normotensive subjects is associated with a hyperinsulinemic response to oral glucose. J Hypertens 1991;9:329-35. 10.1097/00004872-199104000-00004
    1. Singer DRJ, Markandu ND, Sugden AL, Miller MA, MacGregor GA. Sodium restriction in hypertensive patients treated with a converting enzyme inhibitor and a thiazide. Hypertension 1991;17:798-803. 10.1161/01.HYP.17.6.798
    1. Alli C, Avanzini F, Bettelli G, et al. Feasibility of a long-term low-sodium diet in mild hypertension. J Hum Hypertens 1992;6:281-6.
    1. Arroll B. The Auckland blood pressure control study: a randomised controlled trial of physical activity and salt restriction in persons. Med Health Sci 1992;PhD.
    1. Benetos A, Xiao YY, Cuche JL, Hannaert P, Safar M. Arterial effects of salt restriction in hypertensive patients. A 9-week, randomized, double-blind, crossover study. J Hypertens 1992;10:355-60. 10.1097/00004872-199204000-00006
    1. Cobiac L, Nestel PJ, Wing LMH, Howe PR. A low-sodium diet supplemented with fish oil lowers blood pressure in the elderly. J Hypertens 1992;10:87-92. 10.1097/00004872-199201000-00014
    1. Cutler JA, Whelton PK, Appel L, 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;267:1213-20. 10.1001/jama.1992.03480090061028
    1. Gow IF, Dockrell M, Edwards CR, et al. The sensitivity of human blood platelets to the aggregating agent ADP during different dietary sodium intakes in healthy men. Eur J Clin Pharmacol 1992;43:635-8. 10.1007/BF02284963
    1. Huggins RL, Di Nicolantonio R, Morgan TO. Preferred salt levels and salt taste acuity in human subjects after ingestion of untasted salt. Appetite 1992;18:111-9. 10.1016/0195-6663(92)90188-C
    1. Fotherby MD, Potter JF. Effects of moderate sodium restriction on clinic and twenty-four-hour ambulatory blood pressure in elderly hypertensive subjects. J Hypertens 1993;11:657-63. 10.1097/00004872-199306000-00010
    1. Nestel PJ, Clifton PM, Noakes M, McArthur R, Howe PR. Enhanced blood pressure response to dietary salt in elderly women, especially those with small waist: hip ratio. J Hypertens 1993;11:1387-94. 10.1097/00004872-199312000-00011
    1. Redón-Más J, Abellán-Alemán J, Aranda-Lara P, et al. The VERSAL Study Group Antihypertensive activity of verapamil: impact of dietary sodium. J Hypertens 1993;11:665-71. 10.1097/00004872-199306000-00011
    1. Del Río A, Rodríguez-Villamil JL. Metabolic effects of strict salt restriction in essential hypertensive patients. J Intern Med 1993;233:409-14. 10.1111/j.1365-2796.1993.tb00692.x
    1. Ruilope LM, Lahera V. Influence of salt intake on the antihypertensive effect of carvedilol. J Hypertens Suppl 1993;11(4):S17-9. 10.1097/00004872-199306003-00005
    1. Ruppert M, Overlack A, Kolloch R, Kraft K, Göbel B, Stumpe KO. Neurohormonal and metabolic effects of severe and moderate salt restriction in non-obese normotensive adults. J Hypertens 1993;11:743-9. 10.1097/00004872-199307000-00010
    1. Sharma AM, Schorr U, Oelkers W, Distler A. Effects of sodium salts on plasma renin activity and norepinephrine response to orthostasis in salt-sensitive normotensive subjects. Am J Hypertens 1993;6:780-5. 10.1093/ajh/6.9.780
    1. Sharma AM, Schorr U, Distler A. Insulin resistance in young salt-sensitive normotensive subjects. Hypertension 1993;21:273-9. 10.1161/01.HYP.21.3.273
    1. Sharma AM, Schorr U, Thiede HM, Distler A. Effect of dietary salt restriction on urinary serotonin and 5-hydroxyindoleacetic acid excretion in man. J Hypertens 1993;11:1381-6. 10.1097/00004872-199312000-00010
    1. Zoccali C, Mallamaci F, Leonardis D, Romeo M. Randomly allocated crossover study of various levels of sodium intake in patients with mild hypertension. J Hypertens Suppl 1993;11(5):S326-7. 10.1097/00004872-199312050-00142
    1. Howe PRC, Lungershausen YK, Cobiac L, Dandy G, Nestel PJ. Effect of sodium restriction and fish oil supplementation on BP and thrombotic risk factors in patients treated with ACE inhibitors. J Hum Hypertens 1994;8:43-9.
    1. Iwaoka T, Umeda T, Inoue J, et al. Dietary NaCl restriction deteriorates oral glucose tolerance in hypertensive patients with impairment of glucose tolerance. Am J Hypertens 1994;7:460-3. 10.1093/ajh/7.5.460
    1. MacFadyen RJ, Lees KR, Reid JL. Responses to low dose intravenous perindoprilat infusion in salt deplete/salt replete normotensive volunteers. Br J Clin Pharmacol 1994;38:329-34. 10.1111/j.1365-2125.1994.tb04362.x
    1. Zoccali C, Mallamaci F, Parlongo S. The influence of salt intake on plasma calcitonin gene-related peptide in subjects with mild essential hypertension. J Hypertens 1994;12:1249-53. 10.1097/00004872-199411000-00007
    1. Doig JK, MacFadyen RJ, Sweet CS, Reid JL. Haemodynamic and renal responses to oral losartan potassium during salt depletion or salt repletion in normal human volunteers. J Cardiovasc Pharmacol 1995;25:511-7. 10.1097/00005344-199504000-00001
    1. Draaijer P, de Leeuw P, Maessen J, van Hooff J, Leunissen K. Salt-sensitivity testing in patients with borderline hypertension: reproducibility and potential mechanisms. J Hum Hypertens 1995;9:263-9.
    1. Stein CM, Nelson R, Brown M, He H, Wood M, Wood AJ. Dietary sodium intake modulates systemic but not forearm norepinephrine release. Clin Pharmacol Ther 1995;58:425-33. 10.1016/0009-9236(95)90056-X
    1. Weir MR, Dengel DR, Behrens MT, Goldberg AP. Salt-induced increases in systolic blood pressure affect renal hemodynamics and proteinuria. Hypertension 1995;25:1339-44. 10.1161/01.HYP.25.6.1339
    1. Bellini C, Ferri C, Carlomagno A, et al. Impaired inactive to active kallikrein conversion in human salt-sensitive hypertension. J Am Soc Nephrol 1996;7:2565-77.
    1. Ferri C, Bellini C, Carlomagno A, Desideri G, Santucci A. Active kallikrein response to changes in sodium-chloride intake in essential hypertensive patients. J Am Soc Nephrol 1996;7:443-53.
    1. Grey A, Braatvedt G, Holdaway I. Moderate dietary salt restriction does not alter insulin resistance or serum lipids in normal men. Am J Hypertens 1996;9:317-22. 10.1016/0895-7061(95)00390-8
    1. Inoue J, Cappuccio FP, Sagnella GA, et al. Glucose load and renal sodium handling in mild essential hypertension on different sodium intakes. J Hum Hypertens 1996;10:523-9.
    1. Ishimitsu T, Nishikimi T, Matsuoka H, et al. Behaviour of adrenomedullin during acute and chronic salt loading in normotensive and hypertensive subjects. Clin Sci (Lond) 1996;91:293-8. 10.1042/cs0910293
    1. Schorr U, Distler A, Sharma AM. Effect of sodium chloride- and sodium bicarbonate-rich mineral water on blood pressure and metabolic parameters in elderly normotensive individuals: a randomized double-blind crossover trial. J Hypertens 1996;14:131-5.
    1. Zoccali C, Mallamaci F, Cuzzola F, Leonardis D. Reproducibility of the response to short-term low salt intake in essential hypertension. J Hypertens 1996;14:1455-9. 10.1097/00004872-199612000-00011
    1. Cappuccio FP, Markandu ND, Carney C, Sagnella GA, MacGregor GA. Double-blind randomised trial of modest salt restriction in older people. Lancet 1997;350:850-4. 10.1016/S0140-6736(97)02264-2
    1. The Trials of Hypertension Prevention Collaborative Research Group 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;157:657-67. 10.1001/archinte.1997.00440270105009
    1. McCarron DA, Weder AB, Egan BM, et al. Blood pressure and metabolic responses to moderate sodium restriction in isradipine-treated hypertensive patients. Am J Hypertens 1997;10:68-76. 10.1016/S0895-7061(96)00295-6
    1. Meland E, Laerum E, Aakvaag A, Ulvik RJ, Høstmark AT. Salt restriction: effects on lipids and insulin production in hypertensive patients. Scand J Clin Lab Invest 1997;57:501-5. 10.3109/00365519709084600
    1. Schorr U, Turan S, Distler A, Sharma AM. Relationship between ambulatory and resting blood pressure responses to dietary salt restriction in normotensive men. J Hypertens 1997;15:845-9. 10.1097/00004872-199715080-00007
    1. Yamamoto H. Randomized controlled trial of salt-restriction program for primary prevention of hypertension in the community. J Osaka City Med Center. 1997;46:255-67.
    1. Foo M, Denver AE, Coppack SW, Yudkin JS. Effect of salt-loading on blood pressure, insulin sensitivity and limb blood flow in normal subjects. Clin Sci (Lond) 1998;95:157-64. 10.1042/cs0950157
    1. Gomi T, Shibuya Y, Sakurai J, Hirawa N, Hasegawa K, Ikeda T. Strict dietary sodium reduction worsens insulin sensitivity by increasing sympathetic nervous activity in patients with primary hypertension. Am J Hypertens 1998;11:1048-55. 10.1016/S0895-7061(98)00126-5
    1. Herlitz H, Dahlöf B, Jonsson O, Friberg P. Relationship between salt and blood pressure in hypertensive patients on chronic ACE-inhibition. Blood Press 1998;7:47-52. 10.1080/080370598437565
    1. Wing LM, Arnolda LF, Harvey PJ, et al. Low-dose diuretic and/or dietary sodium restriction when blood pressure is resistant to ACE inhibitor. Blood Press 1998;7:299-307. 10.1080/080370598437169
    1. Davrath LR, Gotshall RW, Tucker A, et al. Moderate sodium restriction does not alter lower body negative pressure tolerance. Aviat Space Environ Med 1999;70:577-82.
    1. Schorr U, Blaschke K, Beige J, Distler A, Sharma AM. Angiotensinogen M235T variant and salt sensitivity in young normotensive Caucasians. J Hypertens 1999;17:475-9. 10.1097/00004872-199917040-00004
    1. Uzu T, Fujii T, Nishimura M, et al. Determinants of circadian blood pressure rhythm in essential hypertension. Am J Hypertens 1999;12:35-9. 10.1016/S0895-7061(98)00182-4
    1. Boero R, Pignataro A, Bancale E, et al. [Metabolic effects of changes in dietary sodium intake in patients with essential hypertension] [Italian]. Minerva Urol Nefrol 2000;52:13-6.
    1. Ames RP. The effect of sodium supplementation on glucose tolerance and insulin concentrations in patients with hypertension and diabetes mellitus. Am J Hypertens 2001;14:653-9. 10.1016/S0895-7061(01)01310-3
    1. Appel LJ, Espeland MA, Easter L, Wilson AC, Folmar S, Lacy CR. Effects of reduced sodium intake on hypertension control in older individuals: results from the Trial of Nonpharmacologic Interventions in the Elderly (TONE). Arch Intern Med 2001;161:685-93. 10.1001/archinte.161.5.685
    1. Johnson AG, Nguyen TV, Davis D. Blood pressure is linked to salt intake and modulated by the angiotensinogen gene in normotensive and hypertensive elderly subjects. J Hypertens 2001;19:1053-60. 10.1097/00004872-200106000-00009
    1. Akita S, Sacks FM, Svetkey LP, Conlin PR, Kimura G, DASH-Sodium Trial Collaborative Research Group Effects of the Dietary Approaches to Stop Hypertension (DASH) diet on the pressure-natriuresis relationship. Hypertension 2003;42:8-13. 10.1161/01.HYP.0000074668.08704.6E
    1. Dishy V, Sofowora GG, Imamura H, et al. Nitric oxide production decreases after salt loading but is not related to blood pressure changes or nitric oxide-mediated vascular responses. J Hypertens 2003;21:153-7. 10.1097/00004872-200301000-00025
    1. Nowson CA, Morgan TO, Gibbons C. Decreasing dietary sodium while following a self-selected potassium-rich diet reduces blood pressure. J Nutr 2003;133:4118-23. 10.1093/jn/133.12.4118
    1. Pechère-Bertschi A, Maillard M, Stalder H, et al. Renal hemodynamic and tubular responses to salt in women using oral contraceptives. Kidney Int 2003;64:1374-80. 10.1046/j.1523-1755.2003.00239.x
    1. Perry CG, Palmer T, Cleland SJ, et al. Decreased insulin sensitivity during dietary sodium restriction is not mediated by effects of angiotensin II on insulin action. Clin Sci (Lond) 2003;105:187-94. 10.1042/CS20020320
    1. Beeks E, van der Klauw MM, Kroon AA, Spiering W, Fuss-Lejeune MJ, de Leeuw PW. Alpha-adducin Gly460Trp polymorphism and renal hemodynamics in essential hypertension. Hypertension 2004;44:419-23. 10.1161/01.HYP.0000141410.72537.fd
    1. van Berge-Landry H, James GD. Serum electrolyte, serum protein, serum fat and renal responses to a dietary sodium challenge: allostasis and allostatic load. Ann Hum Biol 2004;31:477-87. 10.1080/03014460412331281746
    1. Gates PE, Tanaka H, Hiatt WR, Seals DR. Dietary sodium restriction rapidly improves large elastic artery compliance in older adults with systolic hypertension. Hypertension 2004;44:35-41. 10.1161/01.HYP.0000132767.74476.64
    1. Forrester T, Adeyemo A, Soarres-Wynter S, et al. A randomized trial on sodium reduction in two developing countries. J Hum Hypertens 2005;19:55-60. 10.1038/sj.jhh.1001782
    1. Swift PA, Markandu ND, Sagnella GA, He FJ, MacGregor GA. Modest salt reduction reduces blood pressure and urine protein excretion in black hypertensives: a randomized control trial. Hypertension 2005;46:308-12. 10.1161/01.HYP.0000172662.12480.7f
    1. Cappuccio FP, Kerry SM, Micah FB, Plange-Rhule J, Eastwood JB. A community programme to reduce salt intake and blood pressure in Ghana [ISRCTN88789643]. BMC Public Health 2006;6:13. 10.1186/1471-2458-6-13
    1. Ho JT, Keogh JB, Bornstein SR, et al. Moderate weight loss reduces renin and aldosterone but does not influence basal or stimulated pituitary-adrenal axis function. Horm Metab Res 2007;39:694-9. 10.1055/s-2007-985354
    1. Melander O, von Wowern F, Frandsen E, et al. Moderate salt restriction effectively lowers blood pressure and degree of salt sensitivity is related to baseline concentration of renin and N-terminal atrial natriuretic peptide in plasma. J Hypertens 2007;25:619-27. 10.1097/HJH.0b013e328013cd50
    1. Townsend RR, Kapoor S, McFadden CB. Salt intake and insulin sensitivity in healthy human volunteers. Clin Sci (Lond) 2007;113:141-8. 10.1042/CS20060361
    1. Jessani S, Hatcher J, Chaturvedi N, Jafar TH. Effect of low vs. high dietary sodium on blood pressure levels in a normotensive Indo-Asian population. Am J Hypertens 2008;21:1238-44. 10.1038/ajh.2008.256
    1. Tzemos N, Lim PO, Wong S, Struthers AD, MacDonald TM. Adverse cardiovascular effects of acute salt loading in young normotensive individuals. Hypertension 2008;51:1525-30. 10.1161/HYPERTENSIONAHA.108.109868
    1. Visser FW, Boonstra AH, Titia Lely A, Boomsma F, Navis G. Renal response to angiotensin II is blunted in sodium-sensitive normotensive men. Am J Hypertens 2008;21:323-8. 10.1038/ajh.2007.63
    1. Dickinson KM, Keogh JB, Clifton PM. Effects of a low-salt diet on flow-mediated dilatation in humans. Am J Clin Nutr 2009;89:485-90. 10.3945/ajcn.2008.26856
    1. He FJ, Marciniak M, Visagie E, et al. Effect of modest salt reduction on blood pressure, urinary albumin, and pulse wave velocity in white, black, and Asian mild hypertensives. Hypertension 2009;54:482-8. 10.1161/HYPERTENSIONAHA.109.133223
    1. Meland E, Aamland A. Salt restriction among hypertensive patients: modest blood pressure effect and no adverse effects. Scand J Prim Health Care 2009;27:97-103. 10.1080/02813430802661795
    1. Paulsen L, Holst LM, Bech JN, Starklint J, Pedersen EB. Glomerular filtration rate and blood pressure are unchanged by increased sodium intake in atorvastatin-treated healthy men. Scand J Clin Lab Invest 2009;69:323-9. 10.1080/00365510802571007
    1. Pimenta E, Gaddam KK, Oparil S, et al. Effects of dietary sodium reduction on blood pressure in subjects with resistant hypertension: results from a randomized trial. Hypertension 2009;54:475-81. 10.1161/HYPERTENSIONAHA.109.131235
    1. Weir MR, Yadao AM, Purkayastha D, Charney AN. Effects of high- and low-sodium diets on ambulatory blood pressure in patients with hypertension receiving aliskiren. J Cardiovasc Pharmacol Ther 2010;15:356-63. 10.1177/1074248410377173
    1. Zanchi A, Maillard M, Jornayvaz FR, et al. Effects of the peroxisome proliferator-activated receptor (PPAR)-gamma agonist pioglitazone on renal and hormonal responses to salt in diabetic and hypertensive individuals. Diabetologia 2010;53:1568-75. 10.1007/s00125-010-1756-2
    1. Starmans-Kool MJ, Stanton AV, Xu YY, McG Thom SA, Parker KH, Hughes AD. High dietary salt intake increases carotid blood pressure and wave reflection in normotensive healthy young men. J Appl Physiol (1985) 2011;110:468-71. 10.1152/japplphysiol.00917.2010
    1. Carey RM, Schoeffel CD, Gildea JJ, et al. Salt sensitivity of blood pressure is associated with polymorphisms in the sodium-bicarbonate cotransporter. Hypertension 2012;60:1359-66. 10.1161/HYPERTENSIONAHA.112.196071
    1. Graffe CC, Bech JN, Pedersen EB. Effect of high and low sodium intake on urinary aquaporin-2 excretion in healthy humans. Am J Physiol Renal Physiol 2012;302:F264-75. 10.1152/ajprenal.00442.2010
    1. Bonfils PK, Taskiran M, Damgaard M, et al. The influence of high versus low sodium intake on blood pressure and haemodynamics in patients with morbid obesity. J Hypertens 2013;31:2220-9, discussion 2229. 10.1097/HJH.0b013e328363c769
    1. Mallamaci F, Leonardis D, Pizzini P, Cutrupi S, Tripepi G, Zoccali C. Procalcitonin and the inflammatory response to salt in essential hypertension: a randomized cross-over clinical trial. J Hypertens 2013;31:1424-30, discussion 1430. 10.1097/HJH.0b013e328360ddd5
    1. Allen AR, Gullixson LR, Wolhart SC, Kost SL, Schroeder DR, Eisenach JH. Dietary sodium influences the effect of mental stress on heart rate variability: a randomized trial in healthy adults. J Hypertens 2014;32:374-82. 10.1097/HJH.0000000000000045
    1. Cavka A, Cosic A, Jukic I, et al. The role of cyclo-oxygenase-1 in high-salt diet-induced microvascular dysfunction in humans. J Physiol 2015;593:5313-24. 10.1113/JP271631
    1. Gijsbers L, Dower JI, Schalkwijk CG, et al. Effects of sodium and potassium supplementation on endothelial function: a fully controlled dietary intervention study. Br J Nutr 2015;114:1419-26. 10.1017/S0007114515002986
    1. He FJ, Wu Y, Feng XX, et al. School based education programme to reduce salt intake in children and their families (School-EduSalt): cluster randomised controlled trial. BMJ 2015;350:h770. 10.1136/bmj.h770
    1. Matthews EL, Brian MS, Ramick MG, Lennon-Edwards S, Edwards DG, Farquhar WB. High dietary sodium reduces brachial artery flow-mediated dilation in humans with salt-sensitive and salt-resistant blood pressure. J Appl Physiol (1985) 2015;118:1510-5. 10.1152/japplphysiol.00023.2015
    1. Pinjuh Markota N, Rumboldt M, Rumboldt Z. Emphasized warning reduces salt intake: a randomized controlled trial. J Am Soc Hypertens 2015;9:214-20. 10.1016/j.jash.2014.12.022
    1. Riphagen IJ, Gijsbers L, van Gastel MD, et al. Effects of potassium supplementation on markers of osmoregulation and volume regulation: results of a fully controlled dietary intervention study. J Hypertens 2016;34:215-20. 10.1097/HJH.0000000000000786
    1. Suckling RJ, He FJ, Markandu ND, MacGregor GA. Modest salt reduction lowers blood pressure and albumin excretion in impaired glucose tolerance and type 2 diabetes mellitus: A randomized double-blind trial. Hypertension 2016;67:1189-95. 10.1161/HYPERTENSIONAHA.115.06637
    1. Brian MS, Dalpiaz A, Matthews EL, Lennon-Edwards S, Edwards DG, Farquhar WB. Dietary sodium and nocturnal blood pressure dipping in normotensive men and women. J Hum Hypertens 2017;31:145-50. 10.1038/jhh.2016.53
    1. Gefke M, Christensen NJ, Bech P, et al. Hemodynamic responses to mental stress during salt loading. Clin Physiol Funct Imaging 2017;37:688-94. 10.1111/cpf.12360
    1. Babcock MC, Brian MS, Watso JC, et al. Alterations in dietary sodium intake affect cardiovagal baroreflex sensitivity. Am J Physiol Regul Integr Comp Physiol 2018;315:R688-95. 10.1152/ajpregu.00002.2018
    1. Parvanova A, Trillini M, Podestà MA, et al. PROCEED Study Organization and the Scientific Writing Academy (SWA) 2016 Moderate salt restriction with or without paricalcitol in type 2 diabetes and losartan-resistant macroalbuminuria (PROCEED): a randomised, double-blind, placebo-controlled, crossover trial. Lancet Diabetes Endocrinol 2018;6:27-40. 10.1016/S2213-8587(17)30359-5
    1. Rorije NMG, Olde Engberink RHG, Chahid Y, et al. Microvascular permeability after an acute and chronic salt load in healthy subjects: a randomized open-label crossover intervention study. Anesthesiology 2018;128:352-60. 10.1097/ALN.0000000000001989
    1. Wang Y, Chu C, Wang KK, et al. Effect of salt intake on plasma and urinary uric acid levels in Chinese adults: an interventional trial. Sci Rep 2018;8:1434. 10.1038/s41598-018-20048-2
    1. Cutler JA, Follmann D, Allender PS. Randomized trials of sodium reduction: an overview. Am J Clin Nutr 1997;65(Suppl):643S-51S. 10.1093/ajcn/65.2.643S
    1. Ebrahim S, Smith GD. Lowering blood pressure: a systematic review of sustained effects of non-pharmacological interventions. J Public Health Med 1998;20:441-8. 10.1093/oxfordjournals.pubmed.a024800
    1. Graudal NA, Galløe AM, Garred P. Effects of sodium restriction on blood pressure, renin, aldosterone, catecholamines, cholesterols, and triglyceride: a meta-analysis. JAMA 1998;279:1383-91. 10.1001/jama.279.17.1383
    1. Jürgens G, Graudal NA. Effects of low sodium diet versus high sodium diet on blood pressure, renin, aldosterone, catecholamines, cholesterols, and triglyceride. Cochrane Database Syst Rev 2004;(1):CD004022. 10.1002/14651858.CD004022.pub2
    1. Mozaffarian D, Fahimi S, Singh GM, et al. Global Burden of Diseases Nutrition and Chronic Diseases Expert Group Global sodium consumption and death from cardiovascular causes. N Engl J Med 2014;371:624-34. 10.1056/NEJMoa1304127
    1. Rhee OJ, Rhee MY, Oh SW, et al. Effect of sodium intake on renin level: Analysis of general population and meta-analysis of randomized controlled trials. Int J Cardiol 2016;215:120-6. 10.1016/j.ijcard.2016.04.109
    1. He FJ, Markandu ND, Sagnella GA, MacGregor GA. Importance of the renin system in determining blood pressure fall with salt restriction in black and white hypertensives. Hypertension 1998;32:820-4. 10.1161/01.HYP.32.5.820
    1. Peters RM, Flack JM. Salt sensitivity and hypertension in African Americans: implications for cardiovascular nurses. Prog Cardiovasc Nurs 2000;15:138-44. 10.1111/j.0889-7204.2000.080404.x
    1. Mente A, O’Donnell M, Rangarajan S, et al. Urinary sodium excretion, blood pressure, cardiovascular disease, and mortality: a community-level prospective epidemiological cohort study. Lancet 2018;392:496-506. 10.1016/S0140-6736(18)31376-X
    1. Cogswell ME, Mugavero K, Bowman BA, Frieden TR. Dietary sodium and cardiovascular disease risk–measurement matters. N Engl J Med 2016;375:580-6. 10.1056/NEJMsb1607161
    1. Juraschek SP, Woodward M, Sacks FM, Carey VJ, Miller ER, 3rd, Appel LJ. Time course of change in blood pressure from sodium reduction and the DASH diet. Hypertension 2017;70:923-9. 10.1161/HYPERTENSIONAHA.117.10017

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