Abstract
Purpose
Dietary sodium and potassium intake are associated with stroke, but the potential mechanisms are unclear. We aimed to study the association between sodium and potassium intake and subclinical cerebrovascular health in hypertensive older males using multimodal magnetic resonance imaging.
Methods
A total of 189 hypertensive male subjects without previous cardiovascular or cerebrovascular disease were included. Daily urinary sodium and potassium excretion were estimated from a fasting spot urine sample using a formula approach. A dedicated cerebrovascular health imaging protocol including vessel wall imaging, angiography, arterial spin labeling imaging and T2-weighted fluid-attenuated inversion recovery imaging was performed to study intracranial atherosclerosis, vascular rarefaction (defined as fewer discernible vessels on angiography), brain perfusion and small vessel disease, respectively.
Results
The mean age was 64.9 (± 7.2) years. The average daily urinary and potassium excretion was 4.7 (± 1.4) g/L and 2.1 (± 0.5) g/L, respectively. Increased urinary sodium excretion was associated with decreased cerebral blood flow and elevated urinary potassium excretion was associated with reduced prevalence of intracranial plaque. The associations remained significant after adjusting for covariates, even including blood pressure control. Quadratic regression analysis indicated a marginally significant U-shaped association between urinary sodium intake and white matter hyperintensity, which lost significance in fully adjusted models. No significant association of urinary sodium and potassium excretion with other cerebrovascular health measures was noted.
Conclusion
We concluded that in hypertensive older males without overt cardiovascular disease, increased sodium intake and reduced potassium intake are associated with impaired subclinical cerebrovascular health.
Similar content being viewed by others
Data availability
All the relevant data have been presented in this paper. Further request should be addressed to Dr. Junwei Yang.
Code availability
Not applicable.
References
Strazzullo P, D’Elia L, Kandala NB, Cappuccio FP (2009) Salt intake, stroke, and cardiovascular disease: meta-analysis of prospective studies. BMJ 339:b4567. https://doi.org/10.1136/bmj.b4567
D’Elia L, Barba G, Cappuccio FP, Strazzullo P (2011) Potassium intake, stroke, and cardiovascular disease a meta-analysis of prospective studies. J Am Coll Cardiol 57(10):1210–1219. https://doi.org/10.1016/j.jacc.2010.09.070
Mente A, O’Donnell M, Rangarajan S, Dagenais G, Lear S, McQueen M, Diaz R, Avezum A, Lopez-Jaramillo P, Lanas F, Li W, Lu Y, Yi S, Rensheng L, Iqbal R, Mony P, Yusuf R, Yusoff K, Szuba A, Oguz A, Rosengren A, Bahonar A, Yusufali A, Schutte AE, Chifamba J, Mann JF, Anand SS, Teo K, Yusuf S, Pure E, Investigators OT (2016) Associations of urinary sodium excretion with cardiovascular events in individuals with and without hypertension: a pooled analysis of data from four studies. Lancet 388(10043):465–475. https://doi.org/10.1016/S0140-6736(16)30467-6
Mente A, O’Donnell MJ, Rangarajan S, McQueen MJ, Poirier P, Wielgosz A, Morrison H, Li W, Wang X, Di C, Mony P, Devanath A, Rosengren A, Oguz A, Zatonska K, Yusufali AH, Lopez-Jaramillo P, Avezum A, Ismail N, Lanas F, Puoane T, Diaz R, Kelishadi R, Iqbal R, Yusuf R, Chifamba J, Khatib R, Teo K, Yusuf S, Investigators P (2014) Association of urinary sodium and potassium excretion with blood pressure. N Engl J Med 371(7):601–611. https://doi.org/10.1056/NEJMoa1311989
Faraci FM, Heistad DD (1990) Regulation of large cerebral arteries and cerebral microvascular pressure. Circ Res 66(1):8–17. https://doi.org/10.1161/01.res.66.1.8
Heistad DD, Marcus ML, Abboud FM (1978) Role of large arteries in regulation of cerebral blood flow in dogs. J Clin Investig 62(4):761–768. https://doi.org/10.1172/JCI109187
Wardlaw JM, Allerhand M, Doubal FN, Valdes Hernandez M, Morris Z, Gow AJ, Bastin M, Starr JM, Dennis MS, Deary IJ (2014) Vascular risk factors, large-artery atheroma, and brain white matter hyperintensities. Neurology 82(15):1331–1338. https://doi.org/10.1212/WNL.0000000000000312
Liu W, Huang X, Liu X, Ortega D, Chen L, Chen Z, Sun J, Wang L, Hatsukami TS, Yuan C, Li H (2021) Uncontrolled hypertension associates with subclinical cerebrovascular health globally: a multimodal imaging study. Eur Radiol 31(4):2233–2241
Chen L, Sun J, Hippe DS, Balu N, Yuan Q, Yuan I, Zhao X, Li R, He L, Hatsukami TS, Hwang JN, Yuan C (2019) Quantitative assessment of the intracranial vasculature in an older adult population using iCafe. Neurobiol Aging 79:59–65. https://doi.org/10.1016/j.neurobiolaging.2019.02.027
Bullitt E, Lin NU, Smith JK, Zeng D, Winer EP, Carey LA, Lin W, Ewend MG (2007) Blood vessel morphologic changes depicted with MR angiography during treatment of brain metastases: a feasibility study. Radiology 245(3):824–830. https://doi.org/10.1148/radiol.2453061889
Liu W, Huang X, Liu X, Ortega D, Chen L, Chen Z, Sun J, Wang L, Hatsukami TS, Yuan C, Li H, Yang J (2020) Uncontrolled hypertension associates with subclinical cerebrovascular health globally: a multimodal imaging study. Eur Radiol. https://doi.org/10.1007/s00330-020-07218-5
Chen L, Mossa-Basha M, Balu N, Canton G, Sun J, Pimentel K, Hatsukami TS, Hwang JN, Yuan C (2018) Development of a quantitative intracranial vascular features extraction tool on 3D MRA using semiautomated open-curve active contour vessel tracing. Magn Reson Med 79(6):3229–3238. https://doi.org/10.1002/mrm.26961
Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, van Osch MJ, Wang DJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73(1):102–116. https://doi.org/10.1002/mrm.25197
Roura E, Oliver A, Cabezas M, Valverde S, Pareto D, Vilanova JC, Ramio-Torrenta L, Rovira A, Llado X (2015) A toolbox for multiple sclerosis lesion segmentation. Neuroradiology 57(10):1031–1043. https://doi.org/10.1007/s00234-015-1552-2
Kawasaki T, Itoh K, Uezono K, Sasaki H (1993) A simple method for estimating 24 h urinary sodium and potassium excretion from second morning voiding urine specimen in adults. Clin Exp Pharmacol Physiol 20(1):7–14. https://doi.org/10.1111/j.1440-1681.1993.tb01496.x
Mente A, O’Donnell MJ, Dagenais G, Wielgosz A, Lear SA, McQueen MJ, Jiang Y, Xingyu W, Jian B, Calik KB, Akalin AA, Mony P, Devanath A, Yusufali AH, Lopez-Jaramillo P, Avezum A Jr, Yusoff K, Rosengren A, Kruger L, Orlandini A, Rangarajan S, Teo K, Yusuf S (2014) 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 32(5):1005–1014. https://doi.org/10.1097/HJH.0000000000000122
Kawamura M, Kusano Y, Takahashi T, Owada M, Sugawara T (2006) Effectiveness of a spot urine method in evaluating daily salt intake in hypertensive patients taking oral antihypertensive drugs. Hypertens Res 29(6):397–402. https://doi.org/10.1291/hypres.29.397
Jager KJ, Zoccali C, Macleod A, Dekker FW (2008) Confounding: what it is and how to deal with it. Kidney Int 73(3):256–260. https://doi.org/10.1038/sj.ki.5002650
Graudal N, Jurgens G, Baslund B, Alderman MH (2014) Compared with usual sodium intake, low- and excessive-sodium diets are associated with increased mortality: a meta-analysis. Am J Hypertens 27(9):1129–1137. https://doi.org/10.1093/ajh/hpu028
O’Donnell M, Mente A, Rangarajan S, McQueen MJ, Wang X, Liu L, Yan H, Lee SF, Mony P, Devanath A, Rosengren A, Lopez-Jaramillo P, Diaz R, Avezum A, Lanas F, Yusoff K, Iqbal R, Ilow R, Mohammadifard N, Gulec S, Yusufali AH, Kruger L, Yusuf R, Chifamba J, Kabali C, Dagenais G, Lear SA, Teo K, Yusuf S, Investigators P (2014) Urinary sodium and potassium excretion, mortality, and cardiovascular events. N Engl J Med 371(7):612–623. https://doi.org/10.1056/NEJMoa1311889
O’Donnell MJ, Yusuf S, Mente A, Gao P, Mann JF, Teo K, McQueen M, Sleight P, Sharma AM, Dans A, Probstfield J, Schmieder RE (2011) Urinary sodium and potassium excretion and risk of cardiovascular events. JAMA 306(20):2229–2238. https://doi.org/10.1001/jama.2011.1729
Willie CK, Tzeng YC, Fisher JA, Ainslie PN (2014) Integrative regulation of human brain blood flow. J Physiol 592(5):841–859. https://doi.org/10.1113/jphysiol.2013.268953
Dai W, Lopez OL, Carmichael OT, Becker JT, Kuller LH, Gach HM (2008) Abnormal regional cerebral blood flow in cognitively normal elderly subjects with hypertension. Stroke 39(2):349–354. https://doi.org/10.1161/STROKEAHA.107.495457
Beason-Held LL, Moghekar A, Zonderman AB, Kraut MA, Resnick SM (2007) Longitudinal changes in cerebral blood flow in the older hypertensive brain. Stroke 38(6):1766–1773. https://doi.org/10.1161/STROKEAHA.106.477109
Tryambake D, He J, Firbank MJ, O’Brien JT, Blamire AM, Ford GA (2013) Intensive blood pressure lowering increases cerebral blood flow in older subjects with hypertension. Hypertension 61(6):1309–1315. https://doi.org/10.1161/HYPERTENSIONAHA.112.200972
Allen LA, Schmidt JR, Thompson CT, Carlson BE, Beard DA, Lombard JH (2019) High salt diet impairs cerebral blood flow regulation via salt-induced angiotensin II suppression. Microcirculation 26(3):e12518. https://doi.org/10.1111/micc.12518
Faraco G, Brea D, Garcia-Bonilla L, Wang G, Racchumi G, Chang H, Buendia I, Santisteban MM, Segarra SG, Koizumi K, Sugiyama Y, Murphy M, Voss H, Anrather J, Iadecola C (2018) Dietary salt promotes neurovascular and cognitive dysfunction through a gut-initiated TH17 response. Nat Neurosci 21(2):240–249. https://doi.org/10.1038/s41593-017-0059-z
Khaw KT, Barrett-Connor E (1987) Dietary potassium and stroke-associated mortality. A 12-year prospective population study. N Engl J Med 316(5):235–240. https://doi.org/10.1056/NEJM198701293160502
Bazzano LA, He J, Ogden LG, Loria C, Vupputuri S, Myers L, Whelton PK (2001) Dietary potassium intake and risk of stroke in US men and women: national health and nutrition examination survey I epidemiologic follow-up study. Stroke 32(7):1473–1480. https://doi.org/10.1161/01.str.32.7.1473
Green DM, Ropper AH, Kronmal RA, Psaty BM, Burke GL (2002) Serum potassium level and dietary potassium intake as risk factors for stroke. Neurology 59(3):314–320. https://doi.org/10.1212/wnl.59.3.314
Seth A, Mossavar-Rahmani Y, Kamensky V, Silver B, Lakshminarayan K, Prentice R, Van Horn L, Wassertheil-Smoller S (2014) Potassium intake and risk of stroke in women with hypertension and nonhypertension in the women’s health initiative. Stroke 45(10):2874–2880. https://doi.org/10.1161/STROKEAHA.114.006046
Mente A, O’Donnell M, Rangarajan S, McQueen M, Dagenais G, Wielgosz A, Lear S, Ah STL, Wei L, Diaz R, Avezum A, Lopez-Jaramillo P, Lanas F, Mony P, Szuba A, Iqbal R, Yusuf R, Mohammadifard N, Khatib R, Yusoff K, Ismail N, Gulec S, Rosengren A, Yusufali A, Kruger L, Tsolekile LP, Chifamba J, Dans A, Alhabib KF, Yeates K, Teo K, Yusuf S (2018) Urinary sodium excretion, blood pressure, cardiovascular disease, and mortality: a community-level prospective epidemiological cohort study. Lancet 392(10146):496–506. https://doi.org/10.1016/S0140-6736(18)31376-X
Alexander MD, Yuan C, Rutman A, Tirschwell DL, Palagallo G, Gandhi D, Sekhar LN, Mossa-Basha M (2016) High-resolution intracranial vessel wall imaging: imaging beyond the lumen. J Neurol Neurosurg Psychiatry 87(6):589–597. https://doi.org/10.1136/jnnp-2015-312020
Wang Y, Liu X, Wu X, Degnan AJ, Malhotra A, Zhu C (2019) Culprit intracranial plaque without substantial stenosis in acute ischemic stroke on vessel wall MRI: a systematic review. Atherosclerosis 287:112–121. https://doi.org/10.1016/j.atherosclerosis.2019.06.907
Hu D, Huang J, Wang Y, Zhang D, Qu Y (2014) Fruits and vegetables consumption and risk of stroke: a meta-analysis of prospective cohort studies. Stroke 45(6):1613–1619. https://doi.org/10.1161/STROKEAHA.114.004836
Kido M, Ando K, Onozato ML, Tojo A, Yoshikawa M, Ogita T, Fujita T (2008) Protective effect of dietary potassium against vascular injury in salt-sensitive hypertension. Hypertension 51(2):225–231. https://doi.org/10.1161/HYPERTENSIONAHA.107.098251
Ishimitsu T, Tobian L, Sugimoto K, Everson T (1996) High potassium diets reduce vascular and plasma lipid peroxides in stroke-prone spontaneously hypertensive rats. Clin Exp Hypertens 18(5):659–673. https://doi.org/10.3109/10641969609081773
Sun Y, Byon CH, Yang Y, Bradley WE, Dell’Italia LJ, Sanders PW, Agarwal A, Wu H, Chen Y (2017) Dietary potassium regulates vascular calcification and arterial stiffness. JCI Insight. https://doi.org/10.1172/jci.insight.94920
Makin SDJ, Mubki GF, Doubal FN, Shuler K, Staals J, Dennis MS, Wardlaw JM (2017) Small vessel disease and dietary salt intake: cross-sectional study and systematic review. J Stroke Cerebrovasc Dis 26(12):3020–3028. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.08.004
Heye AK, Thrippleton MJ, Chappell FM, Hernandez Mdel C, Armitage PA, Makin SD, Maniega SM, Sakka E, Flatman PW, Dennis MS, Wardlaw JM (2016) Blood pressure and sodium: association with MRI markers in cerebral small vessel disease. J Cereb Blood Flow Metab 36(1):264–274. https://doi.org/10.1038/jcbfm.2015.64
Funding
The study is supported by a grant from Jiangsu Science and Technology Department (BE2017762) to Dr. Junwei Yang.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
None.
Ethics approval
The study was approved by the Institutional Ethics Committee of The Second Affiliated Hospital of Nanjing Medical University and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Consent to participate
All participants provided written informed consent.
Rights and permissions
About this article
Cite this article
Liu, W., Huang, X., Liu, X. et al. Urinary sodium and potassium excretion and cerebrovascular health: a multimodal imaging study. Eur J Nutr 60, 4555–4563 (2021). https://doi.org/10.1007/s00394-021-02612-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-021-02612-1