Sex-related differences for uric acid in the prediction of cardiovascular events in essential hypertension. A population prospective study

  • Mazzali M, Hughes J, Kim YG, Jefferson JA, Kang DH, Gordon KL, et al. Elevated uric acid increases blood pressure in the rat by a novel crystal-independent mechanism. Hypertension. 2001;38:1101–6. https://doi.org/10.1161/hy1101.092839.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Feig DI, Johnson RJ. Hyperuricemia in childhood primary hypertension. Hypertension. 2003;42:247–52. https://doi.org/10.1161/01.HYP.0000085858.66548.59.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Johnson RJ, Feig DI, Herrera-Acosta J, Kang DH. Resurrection of uric acid as a causal risk factor in essential hypertension. Hypertension. 2005;45:18–20. https://doi.org/10.1161/01.HYP.0000150785.39055.e8.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Grayson PC, Kim SY, LaValley M, Choi HK. Hyperuricemia and incident hypertension: a systematic review and meta-analysis. Arthritis Care Res (Hoboken). 2011;63:102–10. https://doi.org/10.1002/acr.20344.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Feig DI, Madero M, Jalal DI, Sanchez-Lozada LG, Johnson RJ. Uric acid and the origins of hypertension. J Pediatr. 2013;162:896–902. https://doi.org/10.1016/j.jpeds.2012.12.078.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Borghi C, Agnoletti D, Cicero AFG, Lurbe E, Virdis A. Uric acid and hypertension: a review of evidence and future perspectives for the management of cardiovascular risk. Hypertension. 2022;79:1927–36. https://doi.org/10.1161/HYPERTENSIONAHA.122.17956.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kang DH, Nakagawa T, Feng L, Watanabe S, Han L, Mazzali M, et al. A role for uric acid in the progression of renal disease. J Am Soc Nephrol. 2002;13:2888–97. https://doi.org/10.1097/01.asn.0000034910.58454.fd.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Montalcini T, Gorgone G, Gazzaruso C, Sesti G, Perticone F, Pujia A. Relation between serum uric acid and carotid intima-media thickness in healthy postmenopausal women. Intern Emerg Med. 2007;2:19–23. https://doi.org/10.1007/s11739-007-0004-3.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zoccali C, Maio R, Mallamaci F, Sesti G, Perticone F. Uric acid and endothelial dysfunction in essential hypertension. J Am Soc Nephrol. 2006;17:1466–71. https://doi.org/10.1681/ASN.2005090949.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Corry DB, Eslami P, Yamamoto K, Nyby MD, Makino H, Tuck ML. Uric acid stimulates vascular smooth muscle cell proliferation and oxidative stress via the vascular renin-angiotensin system. J Hypertens. 2008;26:269–75. https://doi.org/10.1097/HJH.0b013e3282f240bf.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yu MA, Sanchez-Lozada LG, Johnson RJ, Kang DH. Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid-induced endothelial dysfunction. J Hypertens. 2010;28:1234–42.

    Article 
    PubMed 

    Google Scholar 

  • Cassano V, Crescibene D, Hribal ML, Pelaia C, Armentaro G, Magurno M, et al. Uric acid and vascular damage in essential hypertension: role of insulin resistance. Nutrients. 2020;12:2509. https://doi.org/10.3390/nu12092509.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI, Kang DH, et al. Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr. 2007;86:899–906. https://doi.org/10.1093/ajcn/86.4.899.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • DeBosch BJ, Kluth O, Fujiwara H, Schurmann A, Moley K. Early-onset metabolic syndrome in mice lacking the intestinal uric acid transporter SLC2A9. Nat Commun. 2014;5:4642. https://doi.org/10.1038/ncomms5642.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kodama S, Saito K, Yachi Y, Asumi M, Sugawara A, Totsuka K, et al. Association between serum uric acid and development of type 2 diabetes. Diabetes Care. 2009;32:1737–42. https://doi.org/10.2337/dc09-0288.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Johnson RJ, Nakagawa T, Sanchez-Lozada LG, Shafiu M, Sundaram S, Le M, et al. Sugar, uric acid, and the etiology of diabetes and obesity. Diabetes. 2013;62:3307–15. https://doi.org/10.2337/db12-1814.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lv Q, Meng XF, He FF, Chen S, Su H, Xiong J, et al. High serum uric acid and increased risk of type 2 diabetes: a systemic review and meta-analysis of prospective cohort studies. PLoS ONE. 2013;8:e56864. https://doi.org/10.1371/journal.pone.0056864.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Perticone F, Sciacqua A, Perticone M, Arturi F, Scarpino PE, Quero M, et al. Serum uric acid and 1-h postload glucose in essential hypertension. Diabetes Care. 2012;35:153–7. https://doi.org/10.2337/dc11-1727.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Perticone F, Maio R, Tassone JE, Perticone M, Pascale A, Sciacqua A, et al. Interaction between uric acid and endothelial dysfunction predict new onset of diabetes in hypertensive patients. Int J Cardiol. 2013;167:232–6. https://doi.org/10.1016/j.ijcard.2011.12.065.

    Article 
    PubMed 

    Google Scholar 

  • Fiorentino TV, Sesti F, Succurro E, Pedace E, Andreozzi F, Sciacqua A, et al. Higher serum levels of uric acid are associated with a reduced insulin clearance in non-diabetic individuals. Acta Diabetol. 2018;55:835–42. https://doi.org/10.1007/s00592-018-1153-8.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tassone EJ, Cimellaro A, Perticone M, Hribal ML, Sciacqua A, Andreozzi F, et al. Uric acid impairs insulin signaling promoting Enpp1 binding to insulin receptor in human umbilical vein endothelial cells. Front Endocrinol (Lausanne). 2018;9:98. https://doi.org/10.3389/fendo.2018.00098.

    Article 
    PubMed 

    Google Scholar 

  • Culleton BF, Larson MG, Kannel WB, Levy D. Serum uric acid and risk for cardiovascular disease and death: the Framingham Heart Study. Ann Intern Med. 1999;131:7–13. https://doi.org/10.7326/0003-4819-131-1-199907060-00003.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Verdecchia P, Schillaci G, Reboldi G, Santeusanio F, Porcellati C, Brunetti P. Relation between serum uric acid and risk of cardiovascular disease in essential hypertension: the PIUMA study. Hypertension. 2000;36:1072–8. https://doi.org/10.1161/01.hyp.36.6.1072.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Bos MJ, Koudstaal PJ, Hofman A, Witteman JC, Breteler MM. Uric acid is a risk factor for myocardial infarction and stroke: the Rotterdam study. Stroke. 2006;37:1503–7. https://doi.org/10.1161/01.STR.0000221716.55088.d4.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sciacqua A, Perticone M, Tassone EJ, Cimellaro A, Miceli S, Maio R, et al. Uric acid is an independent predictor of cardiovascular events in post-menopausal women. Int J Cardiol. 2015;197:271–5. https://doi.org/10.1016/j.ijcard.2015.06.069.

    Article 
    PubMed 

    Google Scholar 

  • Perticone M, Tripepi G, Maio R, Cimellaro A, Addesi D, Baggetta R, et al. Risk reclassification ability of uric acid for cardiovascular outcomes in essential hypertension. Int J Cardiol. 2017;243:473–8. https://doi.org/10.1016/j.ijcard.2017.05.051.

    Article 
    PubMed 

    Google Scholar 

  • Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, ESC Scientific Document Group, et al. 2018 ESC/ESH guidelines for the management of arterial hypertension. Eur Heart J. 2018;39:3021–104. https://doi.org/10.1093/eurheartj/ehy339.

    Article 
    PubMed 

    Google Scholar 

  • Shah AD, Langenberg C, Rapsomaniki E, Denaxas S, Pujades-Rodriguez M, Gale CP, et al. Type 2 diabetes and incidence of cardiovascular diseases: a cohort study in 19 million people. Lancet Diabetes Endocrinol. 2015;3:105–13. https://doi.org/10.1016/S2213-8587(14)70219-0.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Peters SA, Huxley RR, Woodward M. Diabetes as a risk factor for stroke in women compared with men: a systematic review and meta-analysis of 64 cohorts, including 775,385 individuals and 12,539 strokes. Lancet. 2014;383:1973–80. https://doi.org/10.1016/S0140-6736(14)60040-4.

    Article 
    PubMed 

    Google Scholar 

  • Succurro E, Fiorentino TV, Miceli S, Perticone M, Sciacqua A, Andreozzi F, et al. Relative risk of cardiovascular disease is higher in women with type 2 diabetes, but not in those with prediabetes, as compared with men. Diabetes Care. 2020;43:3070–8. https://doi.org/10.2337/dc20-1401.

    Article 
    PubMed 

    Google Scholar 

  • Chalmers J, MacMahon S, Mancia G, Whitworth J, Beilin L, Hansson L, et al. World Health Organization-International Society of Hypertension guidelines for the management of hypertension. Guidelines subcommittee of the World Healt Organization. Clin Exp Hypertens. 1999;21:1009–60. https://doi.org/10.3109/10641969909061028.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentration in man. Diabetologia. 1985;28:412–9. https://doi.org/10.1007/BF00280883.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Thygesen K, Alpert JS, White HD. Joint ESC/ACCF/AHA/WHF task force for the redefinition of myocardial infarction. Universal definition of myocardial infarction. Circulation. 2007;116:2634–53. https://doi.org/10.1016/j.jacc.2007.09.011.

    Article 
    PubMed 

    Google Scholar 

  • Adams HP Jr, del Zoppo G, Alberts MJ, Bhatt DL, Brass L, Furlan A, et al. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: The American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Circulation. 2007;115:e478-534. https://doi.org/10.1161/CIRCULATIONAHA.107.181486.

    Article 
    PubMed 

    Google Scholar 

  • Sautin YY, Nakagawa T, Zharikov S, Johnson RJ. Adverse effects of the classic antioxidant uric acid in adipocytes: NADPH-oxidase-mediated oxditavive/nitrosative stress. Am J Physiol Cell Physiol. 2007;293:C584–96. https://doi.org/10.1152/ajpcell.00600.2006.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Corry DB, Eslami P, Yamamoto K, Nyby MD, Makino H, Tuck ML. Uric acid stimulates vascular smooth muscle cell proliferation and oxidative stress via the vascular renin-angiotensin system. J Hypertens. 2008;26:269–75. https://doi.org/10.1097/HJH.0b013e3282f240bf.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Yu MA, Sanchez-Lozada LG, Johnson RJ, Kang DH. Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid induced endothelial dysfunction. J Hypertens. 2010;28:1234–42.

    Article 
    PubMed 

    Google Scholar 

  • Maloberti A, Maggioni S, Occhi L, Triglione N, Panzeri F, Nava S, et al. Sex-related relationships between uric acid and target organ damage in hypertension. J Clin Hypertens (Greenwich). 2018;20:193–200. https://doi.org/10.1111/jch.13136.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Redon P, Maloberti A, Facchetti R, Redon J, Lurbe E, Bombelli M, et al. Gender-related differences in serum uric acid in treated hypertensive patients from central and east European countries: findings from the Blood Pressure control rate and Cardiovascular Risl profile study. J Hypertens. 2019;37:380–8. https://doi.org/10.1097/HJH.0000000000001908.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ferrannini G, De Bacquer D, Vynckier P, De Backer G, Gyberg V, Kotseva K, et al. Gender differences in screening for glucose perturbations, cardiovascular risk factor management and prognosis in patients with dysglycaemia and coronary artery disease: results from the ESC-EORP EUROASPIRE surveys. Cardiovasc Diabetol. 2021;20:38. https://doi.org/10.1186/s12933-021-01233-6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ramezankhani A, Azizi F, Hadaegh F. Gender differences in changes in metabolic syndrome status and its components and risk of cardiovascular disease: a longitudinal cohort study. Cardiovasc Diabetol. 2022;21:227. https://doi.org/10.1186/s12933-022-01665-8.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Reckelhoff J. Mechanisms of sex and gender differences in hypertension. J Hum Hypertension. 2023;37:596–601. https://doi.org/10.1038/s41371-023-00810-4.

    Article 

    Google Scholar 

  • Funck KL, Bjerg L, Isaksen AA, Sandbaeek A, Grove EL. Gender disparities in time-to-initiation of cardioprotective glucose-lowering drugs in patients with type 2 diabetes and cardiovascular disease: a Danish nationwide cohort study. Cardiovasc Diabetol. 2022;21:279. https://doi.org/10.1186/s12933-022-01713-3.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gerdts E, Sudano I, Brouwers S, Borghi C, Bruno RM, Ceconi C, et al. Sex differences in arterial hypertension. A scientific statement from the ESC Council on Hypertension, the European Association of Preventive Cardiology, Association of Cardiovascular Nursing and Allied Professions, the ESC Council for Cardiology Practice, and the ESC Working Group on Cardiovascular Pharmacotherapy. Eur Heart J. 2022;43:4777–88. https://doi.org/10.1093/eurheartj/ehac470.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risk of death, cardiovascular events, and hospitalisation. N Engl J Med. 2004;351:1296–305. https://doi.org/10.1056/NEJMoa041031.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Parikh NI, Hwang SJ, Larson MG, Meigs JB, Levy D, Fox CS. Cardiovascular disease risk factors in chronic kidney disease. Arch Intern Med. 2006;166:1884–91. https://doi.org/10.1001/archinte.166.17.1884.

    Article 
    PubMed 

    Google Scholar 

  • Mazzali M, Kanellis J, Han L, Feng L, Xia YY, Chen Q, et al. Hyperuricemia induces a primary renal arteriolopathy in rats by a blood pressure-independent mechanism. Am J Physiol Renal Physiol. 2002;282:F991–7. https://doi.org/10.1152/ajprenal.00283.2001.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Puig JG, Mateos F, Buno A, Ortega R, Rodriguez F, Dal Re R. Effect of eprosartan and losartan on uric acid metabolism in patients with essential hypertension. J Hypertens. 1999;17:1033–9. https://doi.org/10.1097/00004872-199917070-00021.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dahlof B, Devereux RB, Kjeldsen SE, Julius S, Beevers G, de Faire U, et al. Cardiovascular morbidity and mortality in the Losartan Intervention for Endpoint reduction in hypertension study (LIFE): a randomized trial against atenolol. Lancet. 2002;359:995–1003. https://doi.org/10.1016/S0140-6736(02)08089-3.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Athyros VG, Elisaf M, Papageorgiou AA, Symeonidis AN, Pehlivanidis AN, Bouloukos VI, et al. Effect of statins versus untreated dyslipidemia on serum uric acid levels in patients with coronary heart disease: a subgroup analysis of the GREek Atorvastatin and Coronary-heart-disease Evaluation (GREACE) Study. Am J Kidney Dis. 2004;43(4):589–99. https://doi.org/10.1053/j.ajkd.2003.12.023.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Weimert NA, Tanke WF, Sims JJ. Allopurinol as a cardioprotective during coronary artery bypass graft surgery. Ann Pharmacother. 2003;37:1708–11. https://doi.org/10.1345/aph.1D023.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Virdis A, Masi S, Casiglia E, Tikhonoff V, Cicero AFG, Ungar A, et al. Identification of the uric acid threshold predicting an increased total and cardiovascular mortality over 20 years. Hypertension. 2020;75:302–8. https://doi.org/10.1161/HYPERTENSIONAHA.119.13643.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dutta A, Henley W, Pilling LC, Wallace RB, Melzer D. Uric acid measurement improves prediction of cardiovascular mortality in later life. J Am Geriatr Soc. 2013;61:319–26. https://doi.org/10.1111/jgs.12149.

    Article 
    PubMed 

    Google Scholar 

  • Tscharre M, Herman R, Rohla M, Hauser C, Farhan S, Freynhofer MK, et al. Uric acid is associated with long-term adverse cardiovascular outcomes in patients with acute coronary syndrome undergoing percutaneous coronary intervention. Atherosclerosis. 2018;270:173–9. https://doi.org/10.1016/j.atherosclerosis.2018.02.003.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Reboldi G, Verdecchia P, Saladini F, Pane M, Beilin LJ, Eguchi K, et al. Added predictive value of high uric acid for cardiovascular events in the ambulatory blood pressure international study. J Clin Hypertens (Greenwich). 2019;21:966–74. https://doi.org/10.1111/jch.13584.

    Article 
    PubMed 

    Google Scholar 

  • Leave a Reply

    Your email address will not be published. Required fields are marked *