Relevance of uric acid and asymmetric dimethylarginine for modeling cardiovascular risk prediction in chronic kidney disease patients

International Urology and Nephrology

Volumn 48, Issue 7, 2016, Pages 1129-1136

  Kanbay, Mehmet ^a   Afsar, Baris ^b   Siriopol, Dimitrie ^c,d   Unal, Hilmi Umut ^e   Karaman, Murat ^e   Saglam, Mutlu ^e   Eyileten, Tayfun ^e   Gezer, Mustafa ^e   Verim, Samet ^e   Oguz, Yusuf ^e   Vural, Abdulgaffar ^e   Ortiz, Alberto ^f   Johnson, Richard J ^g   Covic, Adrian ^c,d   Yilmaz, Mahmut Ilker ^e  

^a KOÇ UNIVERSITY   (Turkey)

^b Konya Numune State Hospital   (Turkey)

^c C I PARHON NATIONAL INSTITUTE OF ENDOCRINOLOGY   (Romania)

^d GRIGORE T POPA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^e GULHANE SCHOOL OF MEDICINE   (Turkey)

^f Section of Nephrology   (Spain)

^g UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Asymmetric dimethylarginine; Cardiovascular disease; Chronic kidney disease; Uric acid

Indexed keywords

C REACTIVE PROTEIN; N(G),N(G) DIMETHYLARGININE; URIC ACID; ARGININE; BIOLOGICAL MARKER; N,N-DIMETHYLARGININE;

ADULT; AMINO ACID BLOOD LEVEL; ARTICLE; CARDIOVASCULAR RISK; CEREBROVASCULAR ACCIDENT; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DEATH; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE SEVERITY; ECHOGRAPHY; ENDOTHELIAL DYSFUNCTION; FEMALE; FOLLOW UP; GLOMERULUS FILTRATION RATE; HEART INFARCTION; HIGH RISK PATIENT; HUMAN; MAJOR CLINICAL STUDY; MALE; MORTALITY; PROGNOSTIC ASSESSMENT; PROTEIN BLOOD LEVEL; PROTEINURIA; RISK ASSESSMENT; URIC ACID BLOOD LEVEL; VASCULAR ENDOTHELIUM; VASODILATATION; AGED; ANALOGS AND DERIVATIVES; BLOOD; CARDIOVASCULAR DISEASES; CAUSE OF DEATH; COHORT ANALYSIS; COMPLICATION; KAPLAN MEIER METHOD; KIDNEY FAILURE, CHRONIC; KIDNEY FUNCTION TEST; MIDDLE AGED; PREDICTIVE VALUE; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; PROSPECTIVE STUDY; SEVERITY OF ILLNESS INDEX; SURVIVAL ANALYSIS; UNIVERSITY HOSPITAL;

ACADEMIC MEDICAL CENTERS; AGED; ARGININE; BIOMARKERS; CARDIOVASCULAR DISEASES; CAUSE OF DEATH; COHORT STUDIES; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; KIDNEY FAILURE, CHRONIC; KIDNEY FUNCTION TESTS; MALE; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; RISK ASSESSMENT; SEVERITY OF ILLNESS INDEX; SURVIVAL ANALYSIS; URIC ACID;

EID: 84961788979     PISSN: 03011623     EISSN: 15732584     Source Type: Journal    
DOI: 10.1007/s11255-016-1271-6     Document Type: Article

References (41)

1. Kanbay M, Segal M, Afsar B, Kang DH, Rodriguez-Iturbe B, Johnson RJ (2013) The role of uric acid in the pathogenesis of human cardiovascular disease. Heart 99:759–766
2. Oda M, Satta Y, Takenaka O, Takahata N (2002) Loss of urate oxidase activity in hominoids and its evolutionary implications. Mol Biol Evol 19:640–653
3. Ames BN, Cathcart R, Schwiers E, Hochstein P (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci USA 78:6858–6862
4. Kanbay M, Afsar B, Covic A (2011) Uric acid as a cardiometabolic risk factor: to be or not to be. Contrib Nephrol 171:62–67
5. Kanbay M, Ikizek M, Solak Y, Selcoki Y, Uysal S, Armutcu F, Eryonucu B, Covic A, Johnson RJ (2011) Uric Acid and pentraxin-3 levels are independently associated with coronary artery disease risk in patients with stage 2 and 3 kidney disease. Am J Nephrol 33:325–331
6. Schwartz IF, Grupper A, Chernichovski T, Grupper A, Hillel O, Engel A, Schwartz D (2011) Hyperuricemia attenuates aortic nitric oxide generation, through inhibition of arginine transport, in rats. J Vasc Res 48:252–260
7. Zharikov S, Krotova K, Hu H, Baylis C, Johnson RJ, Block ER, Patel J (2008) Uric acid decreases NO production and increases arginase activity in cultured pulmonary artery endothelial cells. Am J Physiol Cell Physiol 295:C1183–C1190
8. Sautin YY, Nakagawa T, Zharikov S, Johnson RJ (2007) Adverse effects of the classic antioxidant uric acid in adipocytes: NADPH oxidase-mediated oxidative/nitrosative stress. Am J Physiol Cell Physiol 293:C584–C596
9. Gersch C, Palii SP, Kim KM, Angerhofer A, Johnson RJ, Henderson GN (2008) Inactivation of nitric oxide by uric acid. Nucleosides Nucleotides Nucleic Acids 27:967–978
10. Nakagawa T, Hu H, Zharikov S, Tuttle KR, Short RA, Glushakova O, Ouyang X, Feig DI, Block ER, Herrera-Acosta J, Patel JM, Johnson RJ (2006) A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol Renal Physiol 290:F625–F631
11. Kanbay M, Huddam B, Azak A, Solak Y, Kadioglu GK, Kirbas I, Duranay M, Covic A, Johnson RJ (2011) A randomized study of allopurinol on endothelial function and estimated glomular filtration rate in asymptomatic hyperuricemic subjects with normal renal function. Clin J Am Soc Nephrol 6:1887–1894
12. Ando R, Ueda S, Yamagishi S, Miyazaki H, Kaida Y, Kaifu K, Yokoro M, Nakayama Y, Obara N, Fukami K, Takeuchi M, Okuda S (2013) Involvement of advanced glycation end product-induced asymmetric dimethylarginine generation in endothelial dysfunction. Diabetes Vascu Disease Res 10:436–441
13. Tenderenda-Banasiuk E, Wasilewska A, Taranta-Janusz K, Korzeniecka-Kozerska A (2013) Asymmetric and symmetric dimethylarginine in adolescents with hyperuricemia. Dis Markers 35:407–412
14. Boger RH, Maas R, Schulze F, Schwedhelm E (2005) Elevated levels of asymmetric dimethylarginine (ADMA) as a marker of cardiovascular disease and mortality. Clin Chem Lab Med/FESCC 43:1124–1129
15. Sen N, Ozlu MF, Akgul EO, Kanat S, Cayci T, Turak O, Yaman H, Sokmen E, Ozcan F, Maden O, Demir AD, Covic A, Kanbay M (2011) Elevated plasma asymmetric dimethylarginine level in acute myocardial infarction patients as a predictor of poor prognosis and angiographic impaired reperfusion. Atherosclerosis 219:304–310
16. Kuwahata S, Hamasaki S, Ishida S, Kataoka T, Yoshikawa A, Orihara K, Ogawa M, Oketani N, Saihara K, Okui H, Shinsato T, Kubozono T, Ichiki H, Fujita S, Takumi T, Yoshino S, Nakazaki M, Miyata M, Tei C (2010) Effect of uric acid on coronary microvascular endothelial function in women: association with eGFR and ADMA. J Atheroscler Thromb 17:259–269
17. Testa A, Mallamaci F, Leonardis D, Spoto B, Pisano A, Sanguedolce MC, Tripepi G, Zoccali C, Investigators MS (2015) Synergism between asymmetric dimethylarginine (ADMA) and a genetic marker of uric acid in CKD progression. Nutr Metab Cardiovasc Dis 25:167–172
18. Kanbay M, Yilmaz MI, Sonmez A, Solak Y, Saglam M, Cakir E, Unal HU, Arslan E, Verim S, Madero M, Caglar K, Oguz Y, McFann K, Johnson RJ (2012) Serum uric acid independently predicts cardiovascular events in advanced nephropathy. Am J Nephrol 36:324–331
19. Schwedhelm E, Wallaschofski H, Atzler D, Dorr M, Nauck M, Volker U, Kroemer HK, Volzke H, Boger RH, Friedrich N (2014) Incidence of all-cause and cardiovascular mortality predicted by symmetric dimethylarginine in the population-based study of health in pomerania. PLoS ONE 9:e96875
20. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis (2002) 39:S1–S266
21. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 130(6):461–470
22. Solak Y, Yilmaz MI, Saglam M, Demirbas S, Verim S, Unal HU, Gaipov A, Oguz Y, Kayrak M, Caglar K, Vural A, Turk S, Covic A, Kanbay M (2013). Mean corpuscular volume is associated with endothelial dysfunction and predicts composite cardiovascular events in patients with chronic kidney disease. Nephrology (Carlton)
23. Yilmaz MI, Saglam M, Caglar K, Cakir E, Sonmez A, Ozgurtas T, Aydin A, Eyileten T, Ozcan O, Acikel C, Tasar M, Genctoy G, Erbil K, Vural A, Zoccali C (2006) The determinants of endothelial dysfunction in CKD: oxidative stress and asymmetric dimethylarginine. Am J Kidney Dis 47:42–50
24. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115
25. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R (2002) International brachial artery reactivity task F. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39:257–265
26. Pencina MJ, D’Agostino RB (2004) Overall C as a measure of discrimination in survival analysis: model specific population value and confidence interval estimation. Stat Med 23:2109–2123
27. Pencina MJ, D’Agostino RB Sr, Steyerberg EW (2011) Extensions of net reclassification improvement calculations to measure usefulness of new biomarkers. Stat Med 30:11–21
28. Fujimi-Hayashida A, Ueda S, Yamagishi S, Kaida Y, Ando R, Nakayama Y, Fukami K, Okuda S (2011) Association of asymmetric dimethylarginine with severity of kidney injury and decline in kidney function in IgA nephropathy. Am J Nephrol 33:1–6
29. von Haehling S, Bode-Boger SM, Martens-Lobenhoffer J, Rauchhaus M, Schefold JC, Genth-Zotz S, Karhausen T, Cicoira M, Anker SD, Doehner W (2010) Elevated levels of asymmetric dimethylarginine in chronic heart failure: a pathophysiologic link between oxygen radical load and impaired vasodilator capacity and the therapeutic effect of allopurinol. Clin Pharmacol Ther 88:506–512
30. Culleton BF, Larson MG, Kannel WB, Levy D (1999) Serum uric acid and risk for cardiovascular disease and death: the Framingham Heart Study. Ann Intern Med 131:7–13
31. Kanbay A, Inonu H, Solak Y, Erden A, Uslu E, Yuksel SA, Ozturk MA, McFann K, Johnson RJ, Kanbay M (2014) Uric acid as a potential mediator of cardiovascular morbidity in obstructive sleep apnea syndrome. Eur J Int Med 25:471–476
32. Turak O, Afsar B, Ozcan F, Canpolat U, Grbovic E, Mendi MA, Oksuz F, Siriopol D, Covic A, Caliskan M, McFann K, Johnson RJ, Kanbay M (2014) Relationship between elevated morning blood pressure surge, uric acid, and cardiovascular outcomes in hypertensive patients. J Clin Hypertens 16:530–535
33. Sanchez-Lozada LG, Lanaspa MA, Cristobal-Garcia M, Garcia-Arroyo F, Soto V, Cruz-Robles D, Nakagawa T, Yu MA, Kang DH, Johnson RJ (2012) Uric acid-induced endothelial dysfunction is associated with mitochondrial alterations and decreased intracellular ATP concentrations. Nephron Exp Nephrol 121:e71–e78
34. Sanchez-Lozada LG, Tapia E, Lopez-Molina R, Nepomuceno T, Soto V, Avila-Casado C, Nakagawa T, Johnson RJ, Herrera-Acosta J, Franco M (2007) Effects of acute and chronic l-arginine treatment in experimental hyperuricemia. Am J Physiol Renal Physiol 292:F1238–F1244
35. Khosla UM, Zharikov S, Finch JL, Nakagawa T, Roncal C, Mu W, Krotova K, Block ER, Prabhakar S, Johnson RJ (2005) Hyperuricemia induces endothelial dysfunction. Kidney Int 67:1739–1742
36. Schwartz IF, Grupper A, Chernichovski T, Hillel O, Engel A, Schwartz D (2011) Hyperuricemia attenuates aortic nitric oxide generation, through inhibition of arginine transport, in rats. J Vasc Res 48:252–260
37. Kang DH, Park SK, Lee IK, Johnson RJ (2005) Uric acid-induced C-reactive protein expression: implication on cell proliferation and nitric oxide production of human vascular cells. J Am Soc Nephrol 16:3553–3562
38. Cook S, Hugli O, Egli M, Vollenweider P, Burcelin R, Nicod P, Thorens B, Scherrer U (2003) Clustering of cardiovascular risk factors mimicking the human metabolic syndrome X in eNOS null mice. Swiss Med Wkly 133:360–363
39. Duplain H, Burcelin R, Sartori C, Cook S, Egli M, Lepori M, Vollenweider P, Pedrazzini T, Nicod P, Thorens B, Scherrer U (2001) Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104:342–345
40. Goicoechea M, de Vinuesa SG, Verdalles U, Ruiz-Caro C, Ampuero J, Rincon A, Arroyo D, Luno J (2010) Effect of allopurinol in chronic kidney disease progression and cardiovascular risk. Clin J Am Soc Nephrol 5:1388–1393
41. Goicoechea M, Garcia de Vinuesa S, Verdalles U, Verde E, Macias N, Santos A, Perez de Jose A, Cedeno S, Linares T, Luno J (2015) Allopurinol and progression of CKD and cardiovascular events: long-term follow-up of a randomized clinical trial. Am J Kidney Dis 65:543–549