Cardiovascular implications of proteinuria: An indicator of chronic kidney disease

Nature Reviews Cardiology

Volumn 6, Issue 4, 2009, Pages 301-311

  Agrawal, Varun ^a   Marinescu, Victor ^a   Agarwal, Mohit ^b   McCullough, Peter A ^a  

^a WILLIAM BEAUMONT HOSPITAL   (United States)

^b Marion General Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMLODIPINE; ATORVASTATIN; BEVACIZUMAB; COLESTYRAMINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IRBESARTAN; LISINOPRIL; LOSARTAN; NITRIC OXIDE; PLACEBO; PRAVASTATIN; RAMIPRIL; SIMVASTATIN; TELMISARTAN; VASCULOTROPIN;

ALBUMINURIA; ARTERY CALCIFICATION; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CHRONIC KIDNEY DISEASE; CLINICAL TRIAL; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; INFLAMMATION; KIDNEY FAILURE; MORTALITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN URINE LEVEL; PROTEINURIA; REVIEW; RISK ASSESSMENT; RISK FACTOR; RISK REDUCTION; THROMBOGENESIS; URINARY EXCRETION; ADULT; AGED; CHRONIC DISEASE; DISEASE COURSE; GLOMERULUS FILTRATION RATE; KIDNEY DISEASE; MIDDLE AGED; PREDICTION AND FORECASTING;

ADULT; AGED; AGED, 80 AND OVER; CARDIOVASCULAR DISEASES; CHRONIC DISEASE; DISEASE PROGRESSION; GLOMERULAR FILTRATION RATE; HUMANS; KIDNEY DISEASES; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROTEINURIA; RISK ASSESSMENT; RISK FACTORS; YOUNG ADULT;

EID: 67649652168     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2009.11     Document Type: Review

References (101)

1. sarnak, M. J. et al. American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure research, Clinical Cardiology, and epidemiology and Prevention. 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 108, 2154-2169 (2003).
2. vassalotti, J. A., stevens, L. A. & Levey, A. s. Testing for chronic kidney disease: a position statement from the National Kidney Foundation. Am. J. Kidney Dis. 50, 169-180 (2007).
3. Garg, A. X., Kiberd, B. A., Clark, w. F., Haynes, r. B. & Clase, C. M. Albuminuria and renal insufficiency prevalence guides population screening: results from the NHANes iii. Kidney Int. 61, 2165-2175 (2002).
4. segura, J., Campo, C. & ruilope, L. M. effect of proteinuria and glomerular filtration rate on cardiovascular risk in essential hypertension. Kidney Int. Suppl. 92, s45-s49 (2004).
5. weir, M. r. Microalbuminuria and cardiovascular disease. Clin. J. Am. Soc. Nephrol. 2, 581-590 (2007).
6. Boulware, L. e., Jaar, B. G., Tarver-Carr, M. e., Brancati, F. L. & Powe, N. r. screening for proteinuria in Us adults: a cost-effectiveness analysis. JAMA 290, 3101-3114 (2003).
7. National Kidney Foundation. K/DOQi clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am. J. Kidney Dis. 39 (2 Suppl. 1), s1-s266 (2002).
8. Kashif, w., siddiqi, N., Dincer, A. P., Dincer, H. e. & Hirsch, s. Proteinuria: how to evaluate an important finding. Cleve. Clin. J. Med. 70, 535-537, 541-544, 546-547 (2003).
9. Tonelli, M. et al. Chronic kidney disease and mortality risk: a systematic review. J. Am. Soc. Nephrol. 17, 2034-2047 (2006).
10. Keith, D. s., Nichols, G. A., Gullion, C. M., Brown, J. B. & smith, D. H. Longitudinal follow-up and outcomes among a population with chronic kidney disease in a large managed care organization. Arch. Intern. Med. 164, 659-663 (2004).
11. Go, A. s., Chertow, G. M., Fan, D., McCulloch, C. e. & Hsu, C. Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 351, 1296-1305 (2004).
12. Agarwal, r., Bunaye, Z., Bekele, D. M. & Light, r. P. Competing risk factor analysis of end-stage renal disease and mortality in chronic kidney disease. Am. J. Nephrol. 28, 569-575 (2008).
13. de Zeeuw, D. et al. Albuminuria, a therapeutic target for cardiovascular protection in type 2 diabetic patients with nephropathy. Circulation 110, 921-927 (2004). (Pubitemid 39128617)
14. Maschio, G. et al. effect of the angiotensin-converting-enzyme inhibitor benazepril on the progression of chronic renal insufficiency. The Angiotensin-Converting-enzyme inhibition in Progressive renal insufficiency study Group. N. Engl. J. Med. 334, 939-945 (1996).
15. [No authors listed.] randomised placebocontrolled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. The GiseN Group (Gruppo italiano di studi epidemiologici in Nefrologia). Lancet 349, 1857-1863 (1997).
16. Ordonez, J. D., Hiatt, r. A., Killebrew, e. J. & Fireman, B. H. The increased risk of coronary heart disease associated with nephrotic syndrome. Kidney Int. 44, 638-642 (1993).
17. Liu, J. e., robbins, D. C., Palmieri, v., Bella, J. N., roman, M. J., Fabsitz, r., Howard, B. v., welty, T. K., Lee, e. T., Devereux, r. B. Association of albuminuria with systolic and diastolic left ventricular dysfunction in type 2 diabetes: the strong Heart Study. J. Am. Coll. Cardiol. 41, 2022-2028 (2003). (Pubitemid 36677126)
18. Miettinen, H., Haffner, s. M., Lehto, s., ronnemaa, T., Pyorala, K., Laakso, M. Proteinuria predicts stroke and other atherosclerotic vascular disease events in nondiabetic and non-insulin-dependent diabetic subjects. Stroke 27, 2033-2039 (1996).
19. Zhang, Y. et al. incidence and risk factors for stroke in American indians: the strong Heart study. Circulation 118, 1577-1584 (2008).
20. eddy, A. A. Proteinuria and interstitial injury. Nephrol. Dial. Transplant. 19, 277-281 (2004).
21. Abbate, M., Zoja, C. & remuzzi, G. How does proteinuria cause progressive renal damage? J. Am. Soc. Nephrol. 17, 2974-2984 (2006).
22. Fort, J. Chronic renal failure: a cardiovascular risk factor. Kidney Int. 68, s25-s29 (2005).
23. ridao, N. et al. Prevalence of hypertension in renal disease. Nephrol. Dial. Transplant. 16 (Suppl. 1), 70-73 (2001).
24. inoue, T. et al. Proteinuria as a significant determinant of hypertension in a normotensive screened cohort in Okinawa, Japan. Hypertens. Res. 29, 687-693 (2006).
25. Agarwal, r. & Andersen, M. J. Correlates of systolic hypertension in patients with chronic kidney disease. Hypertension 46, 514-520 (2005). (Pubitemid 41376831)
26. Ohya, Y. et al. increased pulse wave velocity is associated with low creatinine clearance and proteinuria in a screened cohort. Am. J. Kidney Dis. 47, 790-797 (2006).
27. Brenner, B. M. et al. reNAAL study. effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N. Engl. J. Med. 345, 861-869 (2001).
28. Lewis, e. J. et al. Collaborative study Group. renoprotective effect of the angiotensinreceptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N. Engl. J. Med. 345, 851-860 (2001).
29. so, w. Y. et al. effect of angiotensin-converting enzyme inhibition on survival in 3773 Chinese type 2 diabetic patients. Hypertension 44, 294-299 (2004).
30. Marre, M. et al. DiABHYCAr study investigators. effects of low dose ramipril on cardiovascular and renal outcomes in patients with type 2 diabetes and raised excretion of urinary albumin: randomised, double blind, placebo controlled trial (the DiABHYCAr study). BMJ 328, 495 (2004).
31. ONTArGeT investigators et al. Telmisartan, ramipril, or both in patients at high risk for vascular events. N. Engl. J. Med. 358, 1547-1559 (2008).
32. Mann, J. F. et al. renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTArGeT study): a multicentre, randomised, double-blind, controlled trial. Lancet 372, 547-553 (2008).
33. Tylicki, L. et al. Triple pharmacological blockade of the renin-angiotensin-aldosterone system in nondiabetic CKD: an open-label crossover randomized controlled trial. Am. J. Kidney Dis. 52, 486-493 (2008).
34. Barraclough, K. A. et al. Coronary artery calcification scores in patients with chronic kidney disease prior to dialysis: reliability as a trial outcome measure. Nephrol. Dial. Transplant. 23, 3199-3205 (2008).
35. Haydar, A. A. et al. Coronary artery calcification is related to coronary atherosclerosis in chronic renal disease patients: a study comparing eBCTgenerated coronary artery calcium scores and coronary angiography. Nephrol. Dial. Transplant. 19, 2307-2312 (2004).
36. Olson, J. C., edmundowicz, D., Becker, D. J., Kuller, L. H. & Orchard, T. J. Coronary calcium in adults with type 1 diabetes: a stronger correlate of clinical coronary artery disease in men than in women. Diabetes 49, 1571-1578 (2000).
37. wagenknecht, L. e. et al. Familial aggregation of coronary artery calcium in families with type 2 diabetes. Diabetes 50, 861-866 (2001).
38. Mehrotra, r. et asl. Determinants of coronary artery calcification in diabetics with and without nephropathy. Kidney Int. 66, 2022-2031 (2004).
39. Kasiske, B. L. Hyperlipidemia in patients with chronic renal disease. Am. J. Kidney Dis. 32 (Suppl. 3), s142-s156 (1998).
40. Lee, T. M., su, s. F. & Tsai, C. H. effect of pravastatin on proteinuria in patients with wellcontrolled hypertension. Hypertension 40, 67-73 (2002).
41. Lee, T. M., Lin, M. s., Tsai, C. H. & Chang, N. C. Add-on and withdrawal effect of pravastatin on proteinuria in hypertensive patients treated with AT receptor blockers. Kidney Int. 68, 779-787 (2005).
42. Bianchi, s., Bigazzi, r., Caiazza, A. & Campese, v. M. A controlled, prospective study of the effects of atorvastatin on proteinuria and progression of kidney disease. Am. J. Kidney Dis. 41, 565-570 (2003).
43. Hommel, e. et al. Plasma lipoproteins and renal function during simvastatin treatment in diabetic nephropathy. Diabetologia 35, 447-451 (1992).
44. Thomas, M. e. et al. simvastatin therapy for hypercholesterolemic patients with nephrotic syndrome or significant proteinuria. Kidney Int. 44, 1124-1129 (1993).
45. rabelink, A. J., Hene, r. J., erkelens, D. w., Joles, J. A. & Koomans, H. A. effects of simvastatin and cholestyramine on lipoprotein profile in hyperlipidaemia of nephrotic syndrome. Lancet 2, 1335-1338 (1988).
46. strippoli, G. F. et al. effects of statins in patients with chronic kidney disease: meta-analysis and meta-regression of randomised controlled trials. BMJ 336, 645-651 (2008).
47. Agarwal, r. statin induced proteinuria: renal injury or renoprotection? J. Am. Soc. Nephrol. 15, 2502-2503 (2004).
48. Brunzell, J. D. et al. Lipoprotein management in patients with cardiometabolic risk: consensus statement from the American Diabetes Association and the American College of Cardiology Foundation. Diabetes Care 31, 811-822 (2008).
49. Myers, G. L. et al. CDC/AHA workshop on Markers of inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: report from the laboratory science discussion group. Circulation 110, 545-549 (2004).
50. Caglar, K. et al. ADMA, proteinuria, and insulin resistance in non-diabetic stage i chronic kidney disease. Kidney Int. 70, 781-787 (2006).
51. Yilmaz, M. i. et al. ADMA levels correlate with proteinuria, secondary amyloidosis, and endothelial dysfunction. J. Am. Soc. Nephrol. 19, 388-395 (2008).
52. stehouwer, C. D. et al. increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: progressive, interrelated, and independently associated with risk of death. Diabetes 51, 1157-1165 (2002).
53. Jaffa, A. A. et al. Plasma prekallikrein: a risk marker for hypertension and nephropathy in type 1 diabetes. Diabetes 52, 1215-1221 (2003).
54. Takebayashi, K., Matsumoto, s., Aso, Y. & inukai, T. Association between circulating monocyte chemoattractant protein-1 and urinary albumin excretion in nonobese type 2 diabetic patients. J. Diabetes Complications 20, 98-104 (2006). (Pubitemid 43295375)
55. Hirano, T., Kashiwazaki, K., Moritomo, Y., Nagano, s. & Adachi, M. Albuminuria is directly associated with increased plasma PAi-1 and factor vii levels in NiDDM patients. Diabetes Res. Clin. Pract. 36, 11-18 (1997).
56. Zimmermann, J. et al. Hemorheology, plasma protein composition and von willebrand factor in type i diabetic nephropathy. Clin. Nephrol. 46, 230-236 (1996).
57. Blum, M. s. et al. Cytoskeletal rearrangement mediates human microvascular endothelial tight junction modulation by cytokines. Am. J. Physiol. 273, H286-H294 (1997).
58. Michel, C. C. Transport of macromolecules through microvascular walls. Cardiovasc. Res. 32, 644-653 (1996).
59. vogel, s. M. et al. evidence of transcellular permeability pathway in microvessels. Microvasc. Res. 61, 87-101 (2001).
60. stocker, r. & Keaney, J. F. Jr role of oxidative modifications in atherosclerosis. Physiol. Rev. 84, 1381-1478 (2004).
61. Parving, H. H. et al. Macro-microangiopathy and endothelial dysfunction in NiDDM patients with and without diabetic nephropathy. Diabetologia 39, 1590-1597 (1996).
62. Paisley, K. e. et al. endothelial dysfunction and inflammation in asymptomatic proteinuria. Kidney Int. 63, 624-633 (2003).
63. wever, r. M., Luscher, T. F., Cosentino, F. & rabelink, T. J. Atherosclerosis and the two faces of endothelial nitric oxide synthase. Circulation 97, 108-112 (1998).
64. stroes, e. s., Koomans, H. A., de Bruin, T. w. & rabelink, T. J. vascular function in the forearm of hypercholesterolaemic patients off and on lipidlowering medication. Lancet 346, 467-471 (1995).
65. vuong, T. D. et al. Hypoalbuminemia increases lysophosphatidylcholine in low-density lipoprotein of normocholesterolemic subjects. Kidney Int. 55, 1005-1010 (1999).
66. Kougias, P. et al. Lysophosphatidylcholine and secretory phospholipase A2 in vascular disease: mediators of endothelial dysfunction and atherosclerosis. Med. Sci. Monit. 12, rA5-rA16 (2006).
67. Zhu, X., wu, s., Dahut, w. L. & Parikh, C. r. risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: systematic review and meta-analysis. Am. J. Kidney Dis. 49, 186-193 (2007).
68. Yang, J. C. et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 349, 427-434 (2003).
69. stokes, M. B., erazo, M. C. & D'Agati, v. D. Glomerular disease related to anti-veGF therapy. Kidney Int. 74, 1487-1491 (2008).
70. Anavekar, N. s. et al. Predictors of cardiovascular events in patients with type 2 diabetic nephropathy and hypertension: a case for albuminuria. Kidney Int. Suppl. 92, s50-s55 (2004).
71. Halbesma, N. et al. Macroalbuminuria is a better risk marker than low estimated GFr to identify individuals at risk for accelerated GFr loss in population screening. J. Am. Soc. Nephrol. 17, 2582-2590 (2006).
72. Borch-Johnsen, K., Andersen, P. K. & Deckert, T. The effect of proteinuria on relative mortality in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 28, 590-596 (1985). (Pubitemid 15017393)
73. Cardoso, C. r. & salles, G. F. Gross proteinuria is a strong risk predictor for cardiovascular mortality in Brazilian type 2 diabetic patients. Braz. J. Med. Biol. Res. 41, 674-680 (2008).
74. Kannel, w. B., stampfer, M. J., Castelli, w. P. & verter, J. The prognostic significance of proteinuria: the Framingham study. Am. Heart J. 108, 1347-1352 (1984).
75. Astor, B. C., Hallan, s. i., Miller, e. r. 3rd, Yeung, e. & Coresh, J. Glomerular filtration rate, albuminuria, and risk of cardiovascular and allcause mortality in the Us population. Am. J. Epidemiol. 167, 1226-1234 (2008).
76. Hillege, H. L. et al. Prevention of renal and vascular end stage Disease (PreveND) study Group. Urinary albumin excretion predicts cardiovascular and noncardiovascular mortality in general population. Circulation 106, 1777-1782 (2002).
77. Howard, B. v. et al. rising tide of cardiovascular disease in American indians. The strong Heart study. Circulation 99, 2389-2395 (1999).
78. Xu, J. et al. Association of albuminuria with allcause and cardiovascular disease mortality in diabetes: the strong Heart study. Br. J. Diabetes Vasc. Dis. 5, 334-340 (2005).
79. Yuyun, M. F. et al. A prospective study of microalbuminuria and incident coronary heart disease and its prognostic significance in a British population: the ePiC-Norfolk study. Am. J. Epidemiol. 159, 284-293 (2004).
80. wang, Z. & Hoy, w. e. Albuminuria and incident coronary heart disease in Australian Aboriginal people. Kidney Int. 68, 1289-1293 (2005).
81. valmadrid, C. T., Klein, r., Moss, s. e. & Klein, B. e. The risk of cardiovascular disease mortality associated with microalbuminuria and gross proteinuria in persons with older-onset diabetes mellitus. Arch. Intern. Med. 160, 1093-1100 (2000).
82. Culleton, B. F., Larson, M. G., Parfrey, P. s., Kannel, w. B. & Levy, D. Proteinuria as a risk factor for cardiovascular disease and mortality in older people: a prospective study. Am. J. Med. 109, 1-8 (2000).
83. irie, F. et al. The relationships of proteinuria, serum creatinine, glomerular filtration rate with cardiovascular disease mortality in Japanese general population. Kidney Int. 69, 1264-1271 (2006).
84. Madison, J. r. et al. Proteinuria and risk for stroke and coronary heart disease during 27 years of follow-up. Arch. Int. Med. 166, 884-889 (2006).
85. Nakayama, M. et al. Kidney dysfunction as a risk factor for first symptomatic stroke events in a general Japanese population-the Ohasama study. Nephrol. Dial. Transplant. 22, 1910-1915 (2007).
86. MacKinnon, M. et al. Combination therapy with an angiotensin receptor blocker and an ACe inhibitor in proteinuric renal disease: a systematic review of the efficacy and safety data. Am. J. Kidney Dis. 48, 8-20 (2006).
87. Bakris, G. L., weir, M. r., DeQuattro, v. & McMahon, F. G. effects of an ACe inhibitor/ calcium antagonist combination on proteinuria in diabetic nephropathy. Kidney Int. 54, 1283-1289 (1998).
88. Hou, F. F. et al. renoprotection of Optimal Antiproteinuric Doses (rOAD) study: a randomized controlled study of benazepril and losartan in chronic renal insufficiency. J. Am. Soc. Nephrol. 18, 1889-1898 (2007).
89. Aranda, P. et al. Long-term renoprotective effects of standard versus high doses of telmisartan in hypertensive nondiabetic nephropathies. Am. J. Kidney Dis. 46, 1074-1079 (2005).
90. Bianchi, s., Bigazzi, r. & Campese, v. M. Longterm effects of spironolactone on proteinuria and kidney function in patients with chronic kidney disease. Kidney Int. 70, 2116-2123 (2006).
91. schjoedt, K. J. et al. Beneficial impact of spironolactone in diabetic nephropathy. Kidney Int. 68, 2829-2836 (2005).
92. Chrysostomou, A., Pedagogos, e., MacGregor, L. & Becker, G. J. Double-blind, placebo-controlled study on the effect of the aldosterone receptor antagonist spironolactone in patients who have persistent proteinuria and are on long-term angiotensin-converting enzyme inhibitor therapy, with or without an angiotensin ii receptor blocker. Clin. J. Am. Soc. Nephrol. 1, 256-262 (2006).
93. Parving, H. H. et al. Aliskiren combined with losartan in type 2 diabetes and nephropathy. N. Engl. J. Med. 358, 2433-2446 (2008).
94. Ansquer, J. C. et al. effect of fenofibrate on kidney function: a 6-week randomized crossover trial in healthy people. Am. J. Kidney Dis. 51, 904-913 (2008).
95. Bakris, G. L. & weir, M. r. salt intake and reductions in arterial pressure and proteinuria. is there a direct link? Am. J. Hypertens. 9, 200s-206s (1996).
96. Bakris, G. L. & smith, A. effects of sodium intake on albumin excretion in patients with diabetic nephropathy treated with long-acting calcium antagonists. Ann. Intern. Med. 125, 201-204 (1996).
97. Heeg, J. e., de Jong, P. e., van der Hem, G. K. & de Zeeuw, D. efficacy and variability of the antiproteinuric effect of ACe inhibition by lisinopril. Kidney Int. 36, 272-279 (1989).
98. Buter, H., Hemmelder, M. H., Navis, G., de Jong, P. e. & de Zeeuw, D. The blunting of the antiproteinuric efficacy of ACe inhibition by high sodium intake can be restored by hydrochlorothiazide. Nephrol. Dial. Transplant. 13, 1682-1685 (1998).
99. rosenberg, M. e., swanson, J. e., Thomas, B. L. & Hostetter, T. H. Glomerular and hormonal responses to dietary protein intake in human renal disease. Am. J. Physiol. 253, F1083-F1090 (1987).
100. Pan, Y., Guo, L. L. & Jin, H. M. Low-protein diet for diabetic nephropathy: a meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 88, 660-666 (2008).
101. Menon, v. et al. effect of a very low-protein diet on outcomes: long-term follow-up of the Modification of Diet in renal Disease (MDrD) study. Am. J. Kidney Dis. 53, 208-217 (2009).