Biomarkers of Atrial Fibrillation in Metabolic Syndrome

Author(s): Christos Georgakopoulos, Charalambos Vlachopoulos*, Dimitrios Tousoulis.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 5 , 2019

Submit Manuscript
Submit Proposal

Abstract:

Whether the increased atrial fibrillation (AF) risk in metabolic syndrome (MetS) patients is due to the syndrome as a whole or simply the sum of the risks of its individual component parts is still obscure. These two clinical entities share many pathophysiological links and thus distinction between a casual observation and a significant association is difficult. Biomarkers associated with pathogenesis of AF in the context of MetS have the ability to refine future risk prediction. In the present review we identify circulating substances that could be regarded as potential biomarkers for prediction of incident AF, or of cardiovascular events in the setting of AF in patients with MetS. Cardiac myocyte injury and stress markers (troponin and natriuretic peptides), markers of renal function (glomeral filtration rate, cystatin-C), and inflammation markers/mediators (interleukin- 6, CRP) are promising biomarkers of patients with AF and MetS.

Keywords: Biomarkers, Atrial fibrillation, Metabolic Syndrome, Troponin, BNP, GFR, Cystatin-C, Kidney disease, CRP, IL-6, Inflammation.

[1]
Ford, E.S.; Giles, W.H.; Dietz, W.H. Prevalence of the metabolic syndrome among US adults: Findings from the third national health and nutrition examination survey. JAMA, 2002, 287(3), 356-359.
[2]
Hijazi, Z.; Oldgren, J.; Siegbahn, A.; Granger, C.B.; Wallentin, L. Biomarkers in atrial fibrillation: A clinical review. Eur. Heart J., 2013, 34(20), 1475-1480.
[3]
Vlachopoulos, C.; Xaplanteris, P.; Aboyans, V.; Brodmann, M.; Cífková, R.; Cosentino, F.; De Carlo, M.; Gallino, A.; Landmesser, U.; Laurent, S.; Lekakis, J.; Mikhailidis, D.P.; Naka, K.K.; Protogerou, A.D.; Rizzoni, D.; Schmidt-Trucksäss, A.; Van Bortel, L.; Weber, T.; Yamashina, A.; Zimlichman, R.; Boutouyrie, P.; Cockcroft, J.; O’Rourke, M.; Park, J.B.; Schillaci, G.; Sillesen, H.; Townsend, R.R. The role of vascular biomarkers for primary and secondary prevention. A position paper from the European society of cardiology working group on peripheral circulation: Endorsed by the Association for Research into Arterial Structure and Physiology (ARTERY) Society. Atherosclerosis, 2015, 241(2), 507-532.
[4]
Antman, E.M.; Tanasijevic, M.J.; Thompson, B.; Schactman, M.; McCabe, C.H.; Cannon, C.P.; Fischer, G.A.; Fung, A.Y.; Thompson, C.; Wybenga, D.; Braunwald, E. Cardiac-specific troponin I levels to predict the risk of mortality in patients with acute coronary syndromes. N. Engl. J. Med., 1996, 335(18), 1342-1349.
[5]
Katus, H.A.; Remppis, A.; Neumann, F.J.; Scheffold, T.; Diederich, K.W.; Vinar, G.; Noe, A.; Matern, G.; Kuebler, W. Diagnostic efficiency of troponin T measurements in acute myocardial infarction. Circulation, 1991, 83(3), 902-912.
[6]
James, S.K.; Armstrong, P.; Barnathan, E.; Califf, R.; Lindahl, B.; Siegbahn, A.; Simoons, M.L.; Topol, E.J.; Venge, P.; Wallentin, L. Troponin and C-reactive protein have different relations to subsequent mortality and myocardial infarction after acute coronary syndrome: a GUSTO-IV substudy. J. Am. Coll. Cardiol., 2003, 41(6), 916-924.
[7]
Lindahl, B.; Toss, H.; Siegbahn, A.; Venge, P.; Wallentin, L. Markers of myocardial damage and inflammation in relation to long-term mortality in unstable coronary artery disease. FRISC Study Group. Fragmin during instability in coronary artery disease. N. Engl. J. Med., 2000, 343(16), 1139-1147.
[8]
Horwich, T.B.; Patel, J.; MacLellan, W.R.; Fonarow, G.C. Cardiac troponin I is associated with impaired hemodynamics, progressive left ventricular dysfunction, and increased mortality rates in advanced heart failure. Circulation, 2003, 108(7), 833-838.
[9]
Omland, T.; de Lemos, J.A.; Sabatine, M.S.; Christophi, C.A.; Rice, M.M.; Jablonski, K.A.; Tjora, S.; Domanski, M.J.; Gersh, B.J.; Rouleau, J.L.; Pfeffer, M.A.; Braunwald, E. A sensitive cardiac troponin T assay in stable coronary artery disease. N. Engl. J. Med., 2009, 361(26), 2538-2547.
[10]
Zethelius, B.; Johnston, N.; Venge, P. Troponin I as a predictor of coronary heart disease and mortality in 70-year-old men: a community-based cohort study. Circulation, 2006, 113(8), 1071-1078.
[11]
Pervanidou, P.; Akalestos, A.; Bastaki, D.; Apostolakou, F.; Papassotiriou, I.; Chrousos, G. Increased circulating high-sensitivity troponin T concentrations in children and adolescents with obesity and the metabolic syndrome: A marker for early cardiac damage? Metabolism, 2013, 62(4), 527-531.
[12]
Siervo, M.; Ruggiero, D.; Sorice, R.; Nutile, T.; Aversano, M.; Stephan, B.C.; Ciullo, M. Angiogenesis and biomarkers of cardiovascular risk in adults with metabolic syndrome. J. Intern. Med., 2010, 268(4), 338-347.
[13]
Wallace, T.W.; Abdullah, S.M.; Drazner, M.H.; Das, S.R.; Khera, A.; McGuire, D.K.; Wians, F.; Sabatine, M.S.; Morrow, D.A.; de Lemos, J.A. Prevalence and determinants of troponin T elevation in the general population. Circulation, 2006, 113(16), 1958-1965.
[14]
Nattel, S. Defining “culprit mechanisms” in arrhythmogenic cardiac remodeling. Circ. Res., 2004, 94(11), 1403-1405.
[15]
Spach, M.S.; Boineau, J.P. Microfibrosis produces electrical load variations due to loss of side-to-side cell connections. Pacing Clin. Electrophysiol., 1997, 20(2 Pt 2), 397-413.
[16]
Burstein, B.; Nattel, S. Atrial fibrosis: mechanisms and clinical relevance in atrial fibrillation. J. Am. Coll. Cardiol., 2008, 51(8), 802-809.
[17]
Everett, T.H., IV; Olgin, J.E. Atrial fibrosis and the mechanisms of atrial fibrillation. Heart Rhythm, 2007, 4(3)(Suppl.), S24-S27.
[18]
Kostin, S.; Klein, G.; Szalay, Z.; Hein, S.; Bauer, E.P.; Schaper, J. Structural correlate of atrial fibrillation in human patients. Cardiovasc. Res., 2002, 54(2), 361-379.
[19]
Anné, W.; Willems, R.; Roskams, T.; Sergeant, P.; Herijgers, P.; Holemans, P.; Ector, H.; Heidbüchel, H. Matrix metalloproteinases and atrial remodeling in patients with mitral valve disease and atrial fibrillation. Cardiovasc. Res., 2005, 67(4), 655-666.
[20]
Luo, M.H.; Li, Y.S.; Yang, K.P. Fibrosis of collagen I and remodeling of connexin 43 in atrial myocardium of patients with atrial fibrillation. Cardiology, 2006, 107(4), 248-253.
[21]
Pham, T.D.; Fenoglio, J.J., Jr Right atrial ultrastructural in chronic rheumatic heart disease. Int. J. Cardiol., 1982, 1(3-4), 289-304.
[22]
Ohtani, K.; Yutani, C.; Nagata, S.; Koretsune, Y.; Hori, M.; Kamada, T. High prevalence of atrial fibrosis in patients with dilated cardiomyopathy. J. Am. Coll. Cardiol., 1995, 25(5), 1162-1169.
[23]
Lie, J.T.; Hammond, P.I. Pathology of the senescent heart: anatomic observations on 237 autopsy studies of patients 90 to 105 years old. Mayo Clin. Proc., 1988, 63(6), 552-564.
[24]
Bugnicourt, J-M.; Rogez, V.; Guillaumont, M.P.; Rogez, J.C.; Canaple, S.; Godefroy, O. Troponin levels help predict new-onset atrial fibrillation in ischaemic stroke patients: a retrospective study. Eur. Neurol., 2010, 63(1), 24-28.
[25]
Hijazi, Z.; Oldgren, J.; Andersson, U.; Connolly, S.J.; Ezekowitz, M.D.; Hohnloser, S.H.; Reilly, P.A.; Vinereanu, D.; Siegbahn, A.; Yusuf, S.; Wallentin, L. Cardiac biomarkers are associated with an increased risk of stroke and death in patients with atrial fibrillation: A Randomized Evaluation of Long-term Anticoagulation Therapy (RE-LY) substudy. Circulation, 2012, 125(13), 1605-1616.
[26]
Kumagai, K.; Nakashima, H.; Urata, H.; Gondo, N.; Arakawa, K.; Saku, K. Effects of angiotensin II type 1 receptor antagonist on electrical and structural remodeling in atrial fibrillation. J. Am. Coll. Cardiol., 2003, 41(12), 2197-2204.
[27]
Lee, K.W.; Everett, T.H., IV; Rahmutula, D.; Guerra, J.M.; Wilson, E.; Ding, C.; Olgin, J.E. Pirfenidone prevents the development of a vulnerable substrate for atrial fibrillation in a canine model of heart failure. Circulation, 2006, 114(16), 1703-1712.
[28]
Li, D.; Shinagawa, K.; Pang, L.; Leung, T.K.; Cardin, S.; Wang, Z.; Nattel, S. Effects of angiotensin-converting enzyme inhibition on the development of the atrial fibrillation substrate in dogs with ventricular tachypacing-induced congestive heart failure. Circulation, 2001, 104(21), 2608-2614.
[29]
Milliez, P.; Deangelis, N.; Rucker-Martin, C.; Leenhardt, A.; Vicaut, E.; Robidel, E.; Beaufils, P.; Delcayre, C.; Hatem, S.N. Spironolactone reduces fibrosis of dilated atria during heart failure in rats with myocardial infarction. Eur. Heart J., 2005, 26(20), 2193-2199.
[30]
Sakabe, M.; Fujiki, A.; Nishida, K.; Sugao, M.; Nagasawa, H.; Tsuneda, T.; Mizumaki, K.; Inoue, H. Enalapril prevents perpetuation of atrial fibrillation by suppressing atrial fibrosis and over-expression of connexin43 in a canine model of atrial pacing-induced left ventricular dysfunction. J. Cardiovasc. Pharmacol., 2004, 43(6), 851-859.
[31]
Sakabe, M.; Shiroshita-Takeshita, A.; Maguy, A.; Dumesnil, C.; Nigam, A.; Leung, T.K.; Nattel, S. Omega-3 polyunsaturated fatty acids prevent atrial fibrillation associated with heart failure but not atrial tachycardia remodeling. Circulation, 2007, 116(19), 2101-2109.
[32]
Shiroshita-Takeshita, A.; Brundel, B.J.; Burstein, B.; Leung, T.K.; Mitamura, H.; Ogawa, S.; Nattel, S. Effects of simvastatin on the development of the atrial fibrillation substrate in dogs with congestive heart failure. Cardiovasc. Res., 2007, 74(1), 75-84.
[33]
Hussein, A.A.; Bartz, T.M.; Gottdiener, J.S. Serial measures of cardiac troponin T levels by a highly sensitive assay and incident atrial fibrillation in a prospective cohort of ambulatory older adults. Heart Rhythm, 2015, 12(5), 879-885.
[34]
Wallentin, L.; Hijazi, Z.; Siegbahn, A.; Schollin, M.; Alexander, J.H.; Atar, D. on behalf of the ARISTOTLE Investigators. High sensitivity troponin-T for risk stratification in atrial fibrillation during treatment with apixaban or warfarin. European Heart J., 2012. 33 (Abstract Supplement 53).
[35]
Daniels, L.B.; Maisel, A.S. Natriuretic peptides. J. Am. Coll. Cardiol., 2007, 50(25), 2357-2368.
[36]
Johnston, N.; Jernberg, T.; Lindahl, B.; Lindbäck, J.; Stridsberg, M.; Larsson, A.; Venge, P.; Wallentin, L. Biochemical indicators of cardiac and renal function in a healthy elderly population. Clin. Biochem., 2004, 37(3), 210-216.
[37]
Redfield, M.M.; Rodeheffer, R.J.; Jacobsen, S.J.; Mahoney, D.W.; Bailey, K.R.; Burnett, J.C., Jr Plasma brain natriuretic peptide concentration: impact of age and gender. J. Am. Coll. Cardiol., 2002, 40(5), 976-982.
[38]
Silvet, H.; Young-Xu, Y.; Walleigh, D.; Ravid, S. Brain natriuretic peptide is elevated in outpatients with atrial fibrillation. Am. J. Cardiol., 2003, 92(9), 1124-1127.
[39]
Olsen, M.H.; Hansen, T.W.; Christensen, M.K.; Gustafsson, F.; Rasmussen, S.; Wachtell, K.; Borch-Johnsen, K.; Ibsen, H.; Jørgensen, T.; Hildebrandt, P. N-terminal pro brain natriuretic peptide is inversely related to metabolic cardiovascular risk factors and the metabolic syndrome. Hypertension, 2005, 46(4), 660-666.
[40]
Clerico, A.; Giannoni, A.; Vittorini, S.; Emdin, M. The paradox of low BNP levels in obesity. Heart Fail. Rev., 2012, Jan 17(1), 81-96.
[41]
Boerrigter, G.; Burnett, J.C., Jr Recent advances in natriuretic peptides in congestive heart failure. Expert Opin. Investig. Drugs, 2004, 13(6), 643-652.
[42]
Garbers, D.L.; Chrisman, T.D.; Wiegn, P.; Katafuchi, T.; Albanesi, J.P.; Bielinski, V.; Barylko, B.; Redfield, M.M.; Burnett, J.C., Jr Membrane guanylyl cyclase receptors: An update. Trends Endocrinol. Metab., 2006, 17(6), 251-258.
[43]
Sengenès, C.; Berlan, M.; De Glisezinski, I.; Lafontan, M.; Galitzky, J. Natriuretic peptides: A new lipolytic pathway in human adipocytes. FASEB J., 2000, 14(10), 1345-1351.
[44]
Addisu, A.; Gower, W.R., Jr; Landon, C.S.; Dietz, J.R. B-type natriuretic peptide decreases gastric emptying and absorption. Exp. Biol. Med. (Maywood), 2008, 233(4), 475-482.
[45]
Taylor, J.A.; Christenson, R.H.; Rao, K.; Jorge, M.; Gottlieb, S.S. B-type natriuretic peptide and N-terminal pro B-type natriuretic peptide are depressed in obesity despite higher left ventricular end diastolic pressures. Am. Heart J., 2006, 152(6), 1071-1076.
[46]
Hanna, N.; Cardin, S.; Leung, T.K.; Nattel, S. Differences in atrial versus ventricular remodeling in dogs with ventricular tachypacing-induced congestive heart failure. Cardiovasc. Res., 2004, 63(2), 236-244.
[47]
Li, D.; Fareh, S.; Leung, T.K.; Nattel, S. Promotion of atrial fibrillation by heart failure in dogs: Atrial remodeling of a different sort. Circulation, 1999, 100(1), 87-95.
[48]
Ellinor, P.T.; Low, A.F.; Patton, K.K.; Shea, M.A.; Macrae, C.A. Discordant atrial natriuretic peptide and brain natriuretic peptide levels in lone atrial fibrillation. J. Am. Coll. Cardiol., 2005, 45(1), 82-86.
[49]
Shelton, R.J.; Clark, A.L.; Goode, K.; Rigby, A.S.; Cleland, J.G. The diagnostic utility of N-terminal pro-B-type natriuretic peptide for the detection of major structural heart disease in patients with atrial fibrillation. Eur. Heart J., 2006, 27(19), 2353-2361.
[50]
Silvet, H.; Young-Xu, Y.; Walleigh, D.; Ravid, S. Brain natriuretic peptide is elevated in outpatients with atrial fibrillation. Am. J. Cardiol., 2003, 92(9), 1124-1127.
[51]
Shibazaki, K.; Kimura, K.; Fujii, S.; Sakai, K.; Iguchi, Y. Brain natriuretic peptide levels as a predictor for new atrial fibrillation during hospitalization in patients with acute ischemic stroke. Am. J. Cardiol., 2012, 109(9), 1303-1307.
[52]
Suissa, L.; Bresch, S.; Lachaud, S.; Mahagne, M.H. Brain natriuretic peptide: a relevant marker to rule out delayed atrial fibrillation in stroke patient. J. Stroke Cerebrovasc. Dis., 2012.
[53]
Jourdain, P.; Bellorini, M.; Funck, F.; Fulla, Y.; Guillard, N.; Loiret, J.; Thebault, B.; Sadeg, N.; Desnos, M. Short-term effects of sinus rhythm restoration in patients with lone atrial fibrillation: a hormonal study. Eur. J. Heart Fail., 2002, 4(3), 263-267.
[54]
Wozakowska-Kapłon, B. Effect of sinus rhythm restoration on plasma brain natriuretic peptide in patients with atrial fibrillation. Am. J. Cardiol., 2004, 93(12), 1555-1558.
[55]
Yamada, T.; Murakami, Y.; Okada, T.; Okamoto, M.; Shimizu, T.; Toyama, J.; Yoshida, Y.; Tsuboi, N.; Ito, T.; Muto, M.; Kondo, T.; Inden, Y.; Hirai, M.; Murohara, T. Plasma atrial natriuretic Peptide and brain natriuretic peptide levels after radiofrequency catheter ablation of atrial fibrillation. Am. J. Cardiol., 2006, 97(12), 1741-1744.
[56]
Beck-da-Silva, L.; de Bold, A.; Fraser, M.; Williams, K.; Haddad, H. Brain natriuretic peptide predicts successful cardioversion in patients with atrial fibrillation and maintenance of sinus rhythm. Can. J. Cardiol., 2004, 20(12), 1245-1248.
[57]
Freynhofer, M.K.; Jarai, R.; Höchtl, T.; Bruno, V.; Vogel, B.; Aydinkoc, K.; Nürnberg, M.; Wojta, J.; Huber, K. Predictive value of plasma Nt-proBNP and body mass index for recurrence of atrial fibrillation after cardioversion. Int. J. Cardiol., 2011, 149(2), 257-259.
[58]
Lellouche, N.; Berthier, R.; Mekontso-Dessap, A.; Braconnier, F.; Monin, J.L.; Duval, A.M.; Dubois-Randé, J.L.; Guéret, P.; Garot, J. Usefulness of plasma B-type natriuretic peptide in predicting recurrence of atrial fibrillation one year after external cardioversion. Am. J. Cardiol., 2005, 95(11), 1380-1382.
[59]
Patton, K.K.; Ellinor, P.T.; Heckbert, S.R.; Christenson, R.H.; DeFilippi, C.; Gottdiener, J.S.; Kronmal, R.A. N-terminal pro-B-type natriuretic peptide is a major predictor of the development of atrial fibrillation: The cardiovascular health study. Circulation, 2009, 120(18), 1768-1774.
[60]
Hijazi, Z.; Wallentin, L.; Siegbahn, A.; Andersson, U.; Christersson, C.; Ezekowitz, J.; Gersh, B.J.; Hanna, M.; Hohnloser, S.; Horowitz, J.; Huber, K.; Hylek, E.H.; Lopes, E.D.; McMurray, J.J.V.; Granger, C.B. NT-proBNP for risk stratification in atrial fibrillation during treatment with apixaban or warfarin. Eur. Heart J., 2012, 33.
[61]
Hijazi, Z.; Wallentin, L.; Siegbahn, A.; Andersson, U.; Christersson, C.; Ezekowitz, J.; Gersh, B.J.; Hanna, M.; Hohnloser, S.; Horowitz, J.; Huber, K.; Hylek, E.H.; Lopes, E.D.; McMurray, J.J.V.; Granger, C.B. NT-proBNP for risk stratification in atrial fibrillation during treatment with apixaban or warfarin. Eur. Heart J., 2012. 33. (Abstract Supplement, 51).
[62]
Wisse, B.E. The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity. J. Am. Soc. Nephrol., 2004, 15(11), 2792-2800.
[63]
Wolf, G.; Hamann, A.; Han, D.C.; Helmchen, U.; Thaiss, F.; Ziyadeh, F.N.; Stahl, R.A. Leptin stimulates proliferation and TGF-beta expression in renal glomerular endothelial cells: potential role in glomerulosclerosis. Kidney Int., 1999, 56(3), 860-872.
[64]
Hall, J.E.; Brands, M.W.; Henegar, J.R. Mechanisms of hypertension and kidney disease in obesity. Ann. N. Y. Acad. Sci., 1999, 892, 91-107.
[65]
Hoehner, C.M.; Greenlund, K.J.; Rith-Najarian, S.; Casper, M.L.; McClellan, W.M. Association of the insulin resistance syndrome and microalbuminuria among nondiabetic native Americans. The inter-tribal heart project. J. Am. Soc. Nephrol., 2002, 13(6), 1626-1634.
[66]
Chen, J.; Muntner, P.; Hamm, L.L.; Jones, D.W.; Batuman, V.; Fonseca, V.; Whelton, P.K.; He, J. The metabolic syndrome and chronic kidney disease in U.S. adults. Ann. Intern. Med., 2004, 140(3), 167-174.
[67]
Parikh, N.I.; Hwang, S-J.; Larson, M.G.; Meigs, J.B.; Levy, D.; Fox, C.S. Cardiovascular disease risk factors in chronic kidney disease: Overall burden and rates of treatment and control. Arch. Intern. Med., 2006, 166(17), 1884-1891.
[68]
Sarnak, M.J.; Levey, A.S.; Schoolwerth, A.C.; Coresh, J.; Culleton, B.; Hamm, L.L.; McCullough, P.A.; Kasiske, B.L.; Kelepouris, E.; Klag, M.J.; Parfrey, P.; Pfeffer, M.; Raij, L.; Spinosa, D.J.; Wilson, P.W. Kidney disease as a risk factor for development of cardiovascular disease: A statement from the american heart association councils on kidney in cardiovascular disease, high blood pressure research, clinical cardiology, and epidemiology and prevention. Circulation, 2003, 108(17), 2154-2169.
[69]
Vaziri, S.M.; Larson, M.G.; Benjamin, E.J.; Levy, D. Echocardiographic predictors of nonrheumatic atrial fibrillation. The Framingham Heart Study. Circulation, 1994, 89(2), 724-730.
[70]
Siragy, H.M.; Carey, R.M. Role of the intrarenal renin-angiotensin-aldosterone system in chronic kidney disease. Am. J. Nephrol., 2010, 31(6), 541-550.
[71]
Li, D.; Shinagawa, K.; Pang, L.; Leung, T.K.; Cardin, S.; Wang, Z.; Nattel, S. Effects of angiotensin-converting enzyme inhibition on the development of the atrial fibrillation substrate in dogs with ventricular tachypacing-induced congestive heart failure. Circulation, 2001, 104(21), 2608-2614.
[72]
Wolf, G. Renal injury due to renin-angiotensin-aldosterone system activation of the transforming growth factor-beta pathway. Kidney Int., 2006, 70(11), 1914-1919.
[73]
Wachtell, K.; Lehto, M.; Gerdts, E.; Olsen, M.H.; Hornestam, B.; Dahlöf, B.; Ibsen, H.; Julius, S.; Kjeldsen, S.E.; Lindholm, L.H.; Nieminen, M.S.; Devereux, R.B. Angiotensin II receptor blockade reduces new-onset atrial fibrillation and subsequent stroke compared to atenolol: The Losartan Intervention for End Point Reduction in Hypertension (LIFE) study. J. Am. Coll. Cardiol., 2005, 45(5), 712-719.
[74]
Haywood, L.J.; Ford, C.E.; Crow, R.S.; Davis, B.R.; Massie, B.M.; Einhorn, P.T.; Williard, A. for the ALLHAT Collaborative Research Group. Atrial fibrillation at baseline and during follow-up in ALLHAT (Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial). J. Am. Coll. Cardiol., 2009, 54(22), 2023-2031.
[75]
Astor, B.C.; Coresh, J.; Heiss, G.; Pettitt, D.; Sarnak, M.J. Kidney function and anemia as risk factors for coronary heart disease and mortality: the Atherosclerosis Risk in Communities (ARIC) Study. Am. Heart J., 2006, 151(2), 492-500.
[76]
Kottgen, A.; Russell, S.D.; Loehr, L.R.; Crainiceanu, C.M.; Rosamond, W.D.; Chang, P.P.; Chambless, L.E.; Coresh, J. Reduced kidney function as a risk factor for incident heart failure: The atherosclerosis risk in communities (ARIC) study. J. Am. Soc. Nephrol., 2007, 18(4), 1307-1315.
[77]
Schlaich, MP; Socratous, F; Hennebry, S; Eikelis, N; Lambert, EA; Straznicky, N; Esler, MD; Lambert, GW
[78]
Schlaich, M.P.; Socratous, F.; Hennebry, S.; Eikelis, N.; Lambert, E.A.; Straznicky, N.; Esler, M.D.; Lambert, G.W. Sympathetic activation in chronic renal failure. J. Am. Soc. Nephrol., 2009, 20(5), 933-939.
[79]
Go, A.S.; Fang, M.C.; Udaltsova, N.; Chang, Y.; Pomernacki, N.K.; Borowsky, L.; Singer, D.E. Impact of proteinuria and glomerular filtration rate on risk of thromboembolism in atrial fibrillation: the anticoagulation and risk factors in atrial fibrillation (ATRIA) study. Circulation,, 2009, 119(10), 1363-1369.
[80]
Hohnloser, S.H.; Hijazi, Z.; Thomas, L.; Alexander, J.H.; Amerena, J.; Hanna, M.; Keltai, M.; Lanas, F.; Lopes, R.D.; Lopez-Sendon, J.; Granger, C.B.; Wallentin, L. Efficacy of apixaban when compared with warfarin in relation to renal function in patients with atrial fibrillation: insights from the ARISTOTLE trial. Eur. Heart J., 2012, 33(22), 2821-2830.
[81]
Piccini, J.P.; Hernandez, A.F.; Zhao, X.; Patel, M.R.; Lewis, W.R.; Peterson, E.D.; Fonarow, G.C. Quality of care for atrial fibrillation among patients hospitalized for heart failure. J. Am. Coll. Cardiol., 2009, 54(14), 1280-1289.
[82]
Reinecke, H.; Brand, E.; Mesters, R.; Schäbitz, W.R.; Fisher, M.; Pavenstädt, H.; Breithardt, G. Dilemmas in the management of atrial fibrillation in chronic kidney disease. J. Am. Soc. Nephrol., 2009, 20(4), 705-711.
[83]
Abrahamson, M.; Olafsson, I.; Palsdottir, A.; Ulvsbäck, M.; Lundwall, A.; Jensson, O.; Grubb, A. Structure and expression of the human cystatin C gene. Biochem. J., 1990, 268(2), 287-294.
[84]
Laterza, O.F.; Price, C.P.; Scott, M.G. Cystatin C: an improved estimator of glomerular filtration rate? Clin. Chem., 2002, 48(5), 699-707.
[85]
Newman, D.J.; Thakkar, H.; Edwards, R.G.; Wilkie, M.; White, T.; Grubb, A.O.; Price, C.P. Serum cystatin C measured by automated immunoassay: a more sensitive marker of changes in GFR than serum creatinine. Kidney Int., 1995, 47(1), 312-318.
[86]
Servais, A.; Giral, P.; Bernard, M.; Bruckert, E.; Deray, G.; Isnard Bagnis, C. Is serum cystatin-C a reliable marker for metabolic syndrome? Am. J. Med., 2008, 121(5), 426-432.
[87]
Vigil, L.; Lopez, M.; Condés, E.; Varela, M.; Lorence, D.; Garcia-Carretero, R.; Ruiz, J. Cystatin C is associated with the metabolic syndrome and other cardiovascular risk factors in a hypertensive population. J. Am. Soc. Hypertens., 2009, 3(3), 201-209.
[88]
Young, J.A.; Hwang, S.J.; Sarnak, M.J. Associationofvisceral and subcutaneous adiposity with kidney function. Clin. J. Am. Soc. Nephrol., 2008, 3, 1786-1791.
[89]
Fried, L.F.; Lee, J.S.; Shlipak, M.; Chertow, G.M.; Green, C.; Ding, J.; Harris, T.; Newman, A.B. Chronic kidney disease and functional limitation in older people: health, aging and body composition study. J. Am. Geriatr. Soc., 2006, 54(5), 750-756.
[90]
Magnusson, M.; Hedblad, B.; Engström, G.; Persson, M.; Nilsson, P.; Melander, O. High levels of cystatin C predict the metabolic syndrome: the prospective Malmö Diet and Cancer Study. J. Intern. Med., 2013, 274(2), 192-199.
[91]
Dubin, R.; Cushman, M.; Folsom, A.R.; Fried, L.F.; Palmas, W.; Peralta, C.A.; Wassel, C.; Shlipak, M.G. Kidney function and multiple hemostatic markers: cross sectional associations in the multi-ethnic study of atherosclerosis. BMC Nephrol., 2011, 12, 3.
[92]
Imai, A.; Komatsu, S.; Ohara, T.; Kamata, T.; Yoshida, J.; Miyaji, K.; Shimizu, Y.; Takewa, M.; Hirayama, A.; Deshpande, G.A.; Takahashi, O.; Kodama, K. Serum cystatin C is associated with early stage coronary atherosclerotic plaque morphology on multidetector computed tomography. Atherosclerosis, 2011, 218(2), 350-355.
[93]
Knight, E.L.; Verhave, J.C.; Spiegelman, D.; Hillege, H.L.; de Zeeuw, D.; Curhan, G.C.; de Jong, P.E. Factors influencing serum cystatin C levels other than renal function and the impact on renal function measurement. Kidney Int., 2004, 65(4), 1416-1421.
[94]
Wang, J.; Sim, A.S.; Wang, X.L.; Salonikas, C.; Moriatis, M.; Naidoo, D.; Wilcken, D.E. Relations between markers of renal function, coronary risk factors and the occurrence and severity of coronary artery disease. Atherosclerosis, 2008, 197(2), 853-859.
[95]
Alonso, A.; Lopez, F.L.; Matsushita, K.; Loehr, L.R.; Agarwal, S.K.; Chen, L.Y.; Soliman, E.Z.; Astor, B.C.; Coresh, J. Chronic kidney disease is associated with the incidence of atrial fibrillation: The Atherosclerosis Risk in Communities (ARIC) study. Circulation, 2011, 123(25), 2946-2953.
[96]
McManus, D.D.; Corteville, D.C.; Shlipak, M.G. Relation of kidney function and albuminuria with atrial fibrillation (from the heart and soul study). Am. J. Cardiol., 2009, 104(11), 1551-1155.
[97]
Smith, J.G.; Platonov, P.G.; Hedblad, B.; Engström, G.; Melander, O. Atrial fibrillation in the malmö diet and cancer study: A study of occurrence, risk factors and diagnostic validity. Eur. J. Epidemiol., 2010, 25(2), 95-102.
[98]
Liu, P.; Jiang, Y.; Meng, J. Clinical association of cystatin C and atrial fibrillation in Chinese elderly. Int. J. Gerontol., 2015, 3, 146-150.
[99]
Hijazi, Z.; Oldgren, J.; Andersson, U.; Connolly, S.J.; Ezekowitz, M.D.; Hohnloser, S.H.; Reilly, P.A.; Siegbahn, A.; Yusuf, S.; Wallentin, L. Cystatin C is prognostic for stroke, death and bleeding during anticoagulation of atrial fibrillation-a RELY substudy. Circulation 2011; (Abstract supplement AHA 124: A12492)., 2011.
[100]
Fichtlscherer, S.; Zeiher, A.M. Endothelial dysfunction in acute coronary syndromes: Association with elevated C-reactive protein levels. Ann. Med., 2000, 32(8), 515-518.
[101]
Kishimoto, T. Interleukin-6: Discovery of a pleiotropic cytokine. Arthritis Res. Ther., 2006, 8(Suppl. 2), S2.
[102]
Libby, P.; Ridker, P.M. Novel inflammatory markers of coronary risk: theory versus practice. Circulation, 1999, 100(11), 1148-1150.
[103]
Blake, G.J.; Ridker, P.M. C-reactive protein and other inflammatory risk markers in acute coronary syndromes. J. Am. Coll. Cardiol., 2003, 41(4)(Suppl. S), 37S-42S.
[104]
Boos, C.J.; Anderson, R.A.; Lip, G.Y. Is atrial fibrillation an inflammatory disorder? Eur. Heart J., 2006, 27(2), 136-149.
[105]
Aroor, A.R.; McKarns, S.; Demarco, V.G.; Jia, G.; Sowers, J.R. Maladaptive immune and inflammatory pathways lead to cardiovascular insulin resistance. Metabolism, 2013, 62(11), 1543-1552.
[106]
Indulekha, K.; Surendar, J.; Mohan, V. High sensitivity C-reactive protein, tumor necrosis factor-α, interleukin-6, and vascular cell adhesion molecule-1 levels in Asian Indians with metabolic syndrome and insulin resistance (CURES-105). J. Diabetes Sci. Technol., 2011, 5(4), 982-988.
[107]
Chedraui, P.; Escobar, G.S.; Pérez-López, F.R.; Palla, G.; Montt-Guevara, M.; Cecchi, E.; Genazzani, A.R.; Simoncini, T. Angiogenesis, inflammation and endothelial function in postmenopausal women screened for the metabolic syndrome. Maturitas, 2014, 77(4), 370-374.
[108]
Sugiura, K.; Tamakoshi, K.; Yatsuya, H.; Otsuka, R.; Wada, K.; Matsushita, K.; Kondo, T.; Hotta, Y.; Mitsuhashi, H.; Murohara, T.; Toyoshima, H. Contribution of adipocytokines to low-grade inflammatory state as expressed by circulating C-reactive protein in Japanese men: Comparison of leptin and adiponectin. Int. J. Cardiol., 2008, 130(2), 159-164.
[109]
Marcus, G.M.; Smith, L.M.; Ordovas, K.; Scheinman, M.M.; Kim, A.M.; Badhwar, N.; Lee, R.J.; Tseng, Z.H.; Lee, B.K.; Olgin, J.E. Intracardiac and extracardiac markers of inflammation during atrial fibrillation. Heart Rhythm, 2010, 7(2), 149-154.
[110]
Chang, S.N.; Tsai, C.T.; Wu, C.K.; Lee, J.K.; Lai, L.P.; Huang, S.W.; Huang, L.Y.; Tseng, C.D.; Lin, J.L.; Chiang, F.T.; Hwang, J.J. A functional variant in the promoter region regulates the C-reactive protein gene and is a potential candidate for increased risk of atrial fibrillation. J. Intern. Med., 2012, 272(3), 305-315.
[111]
Narducci, M.L.; Pelargonio, G.; Dello Russo, A.; Casella, M.; Biasucci, L.M.; La Torre, G.; Pazzano, V.; Santangeli, P.; Baldi, A.; Liuzzo, G.; Tondo, C.; Natale, A.; Crea, F. Role of tissue C-reactive protein in atrial cardiomyocytes of patients undergoing catheter ablation of atrial fibrillation: pathogenetic implications. Europace, 2011, 13(8), 1133-1140.
[112]
Marott, S.C.; Nordestgaard, B.G.; Zacho, J.; Friberg, J.; Jensen, G.B.; Tybjaerg-Hansen, A.; Benn, M. Does elevated C-reactive protein increase atrial fibrillation risk? A Mendelian randomization of 47,000 individuals from the general population. J. Am. Coll. Cardiol., 2010, 56(10), 789-795.
[113]
Psychari, S.N.; Apostolou, T.S.; Sinos, L.; Hamodraka, E.; Liakos, G.; Kremastinos, D.T. Relation of elevated C-reactive protein and interleukin-6 levels to left atrial size and duration of episodes in patients with atrial fibrillation. Am. J. Cardiol., 2005, 95(6), 764-767.
[114]
Luckett, L.R.; Gallucci, R.M. Interleukin-6 (IL-6) modulates migration and matrix metalloproteinase function in dermal fibroblasts from IL-6KO mice. Br. J. Dermatol., 2007, 156(6), 1163-1171.
[115]
Marcus, G.M.; Whooley, M.A.; Glidden, D.V.; Pawlikowska, L.; Zaroff, J.G.; Olgin, J.E. Interleukin-6 and atrial fibrillation in patients with coronary artery disease: Data from the heart and soul study. Am. Heart J., 2008, 155(2), 303-309.
[116]
Kaireviciute, D.; Blann, A.D.; Balakrishnan, B.; Lane, D.A.; Patel, J.V.; Uzdavinys, G.; Norkunas, G.; Kalinauskas, G.; Sirvydis, V.; Aidietis, A.; Lip, G.Y. Characterisation and validity of inflammatory biomarkers in the prediction of post-operative atrial fibrillation in coronary artery disease patients. Thromb. Haemost., 2010, 104(1), 122-127.
[117]
Conway, D.S.; Therkelsen, S.K.; Bruunsgaard, H.; Krabbe, K.S.; Pedersen, B.K.; Svendsen, J.H. Prognostic impact of hs-CRP and IL-6 in patients with persistent atrial fibrillation treated with electrical cardioversion. Scand. J. Clin. Lab. Invest., 2009, 69(3), 425-432.
[118]
Henningsen, K.M.; Nilsson, B.; Bruunsgaard, H.; Chen, X.; Pedersen, B.K.; Svendsen, J.H. Prognostic impact of hs-CRP and IL-6 in patients undergoing radiofrequency catheter ablation for atrial fibrillation. Scand. Cardiovasc. J., 2009, 43(5), 285-291.
[119]
Loricchio, M.L.; Cianfrocca, C.; Pasceri, V.; Bianconi, L.; Auriti, A.; Calo, L.; Lamberti, F.; Castro, A.; Pandozi, C.; Palamara, A.; Santini, M. Relation of C-reactive protein to long-term risk of recurrence of atrial fibrillation after electrical cardioversion. Am. J. Cardiol., 2007, 99(10), 1421-1424.
[120]
Conway, D.S.; Buggins, P.; Hughes, E.; Lip, G.Y. Prognostic significance of raised plasma levels of interleukin-6 and C-reactive protein in atrial fibrillation. Am. Heart J., 2004, 148(3), 462-466.
[121]
Lip, G.Y.; Patel, J.V.; Hughes, E.; Hart, R.G. High-sensitivity C-reactive protein and soluble CD40 ligand as indices of inflammation and platelet activation in 880 patients with nonvalvular atrial fibrillation: relationship to stroke risk factors, stroke risk stratification schema, and prognosis. Stroke, 2007, 38(4), 1229-1237.
[122]
Roldán, V.; Marín, F.; Díaz, J.; Gallego, P.; Jover, E.; Romera, M.; Manzano-Fernández, S.; Casas, T.; Valdés, M.; Vicente, V.; Lip, G.Y. High sensitivity cardiac troponin T and interleukin-6 predict adverse cardiovascular events and mortality in anticoagulated patients with atrial fibrillation. J. Thromb. Haemost., 2012, 10(8), 1500-1507.
[123]
Aulin, J.K.E.M.; Andersson, U.; Connolly, S.J.; Huber, K.; Reilly, P.A.; Siegbahn, A.; Wallentin, L.; Yusuf, S.; Oldgren, J. Interleukin-6 and C-reactive protein and risk for death and cardiovascular events in patients with atrial fibrillation. J. Am. Coll. Cardiol., 2011, 57, E91.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 26
ISSUE: 5
Year: 2019
Page: [898 - 908]
Pages: 11
DOI: 10.2174/0929867324666171012105528
Price: $58

Article Metrics

PDF: 14
HTML: 3