Proteinuria should be used as a surrogate in CKD

Nature Reviews Nephrology

Volumn 8, Issue 5, 2012, Pages 301-306

  Cravedi, Paolo ^a   Ruggenenti, Piero ^a   Remuzzi, Giuseppe ^a  

^a OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; BIOLOGICAL MARKER; PROTEIN;

CHRONIC KIDNEY DISEASE; DISEASE COURSE; DISEASE EXACERBATION; GLOMERULUS FILTRATION RATE; HUMAN; KIDNEY FAILURE; KIDNEY FUNCTION; MICROALBUMINURIA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; REVIEW;

ACUTE-PHASE PROTEINS; BIOLOGICAL MARKERS; DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; FATTY ACID-BINDING PROTEINS; GLOMERULAR FILTRATION RATE; HUMANS; KIDNEY FAILURE, CHRONIC; LIPOCALINS; PROTEINURIA; PROTO-ONCOGENE PROTEINS;

EID: 84860273272     PISSN: 17595061     EISSN: 1759507X     Source Type: Journal    
DOI: 10.1038/nrneph.2012.42     Document Type: Review

References (63)

1. United States Renal Data System Annual Data Report. United States Renal Data System [online], http://www.usrds.org/(2010).
2. Ruggenenti, P. & Remuzzi, G. Kidney failure stabilizes after a two-decade increase: impact on global (renal and cardiovascular) health. Clin. J. Am. Soc. Nephrol. 2, 146-150 (2007).
3. Cravedi, P., Ruggenenti, P. & Remuzzi, G. Kidney failure stabilizes after an increase over 2 decades. J. Ren. Care 33, 100-104 (2007).
4. Piantadosi, S. Clinical Trials: a Methodologic Perspective (John Wiley and Sons, New York, 1997).
5. Waller, K. V., Ward, K. M., Mahan, J. D. & Wismatt, D. K. Current concepts in proteinuria. Clin. Chem. 35, 755-765 (1989) (Pubitemid 19162067)
6. Kim, M. S. Proteinuria. Clin. Lab. Med. 8, 527-540 (1988).
7. Ruggenenti, P. & Remuzzi, G. Time to abandon microalbuminuria? Kidney Int. 70, 1214-1222 (2006). (Pubitemid 44435172)
8. Gerstein, H. C. et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286, 421-426 (2001). (Pubitemid 32681484)
9. Wachtell, K. et al. Albuminuria and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE study. Ann. Intern. Med. 139, 901-906 (2003).
10. Adler, A. I. et al. Development and progression of nephropathy in type 2 diabetes: the United Kingdom Prospective Diabetes Study (UKPDS 64). Kidney Int. 63, 225-232 (2003). (Pubitemid 35463925)
11. Lemley, K. V et al. Glomerular permselectivity at the onset of nephropathy in type 2 diabetes mellitus. J. Am. Soc. Nephrol. 11, 2095-2105 (2000).
12. Bazzi, C., Petrini, C., Rizza, V., Arrigo, G. & D'Amico, G. A modern approach to selectivity of proteinuria and tubulointerstitial damage in nephrotic syndrome. Kidney Int 58, 1732-1741 (2000).
13. Remuzzi, G., Benigni, A. & Remuzzi, A. Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J. Clin. Invest. 116, 288-296 (2006). (Pubitemid 43228342)
14. Pavkov, M. E. et al. Early renal function decline in type 2 diabetes. Clin. J. Am. Soc. Nephrol. 7, 78-84 (2012).
15. Ruggenenti, P. & Remuzzi, G. Angiotensin-converting enzyme inhibitor therapy for non-diabetic progressive renal disease. Curr. Opin. Nephrol. Hypertens. 6, 489-495 (1997). (Pubitemid 27397885)
16. Barnes, J. L. & Gorin, Y. Myofibroblast differentiation during fibrosis: role of NAD(P)H oxidases. Kidney Int. 79, 944-956 (2011).
17. Zoja, C. et al. Proximal tubular cell synthesis and secretion of endothelin-1 on challenge with albumin and other proteins. Am. J. Kidney Dis. 26, 934-941 (1995).
18. Drumm, K., Bauer, B., Freudinger, R. & Gekle, M. Albumin induces NF-kappaB expression in human proximal tubule-derived cells (IHKE-1). Cell Physiol. Biochem. 12, 187-196 (2002).
19. Tang, S. et al. Albumin stimulates interleukin-8 expression in proximal tubular epithelial cells in vitro and in vivo. J. Clin. Invest. 111, 515-527 (2003). (Pubitemid 36228009)
20. Abbate, M., Zoja, C. & Remuzzi, G. How does proteinuria cause progressive renal damage? J. Am. Soc. Nephrol. 17, 2974-2984 (2006). (Pubitemid 44707757)
21. Rudnicki, M. et al. Gene expression profiles of human proximal tubular epithelial cells in proteinuric nephropathies. Kidney Int. 71, 325-335 (2007). (Pubitemid 46227092)
22. Johnson, D. W., Saunders, H. J., Baxter, R. C., Field, M. J. & Pollock, C. A. Paracrine stimulation of human renal fibroblasts by proximal tubule cells. Kidney Int. 54, 747-757 (1998). (Pubitemid 28397392)
23. Biancone, L. et al. Alternative pathway activation of complement by cultured human proximal tubular epithelial cells. Kidney Int. 45, 451-460 (1994). (Pubitemid 24065080)
24. Nangaku, M., Pippin, J. & Couser, W. G. Complement membrane attack complex (C5b-9) mediates interstitial disease in experimental nephrotic syndrome. J. Am. Soc. Nephrol. 10, 2323-2331 (1999). (Pubitemid 29501465)
25. Rangan, G. K., Pippin, J. W., Coombes, J. D. & Couser, W. G. C5b-9 does not mediate chronic tubulointerstitial disease in the absence of proteinuria. Kidney Int. 67, 492-503 (2005). (Pubitemid 40139841)
26. Iseki, K., Iseki, C., Ikemiya, Y. & Fukiyama, K. Risk of developing end-stage renal disease in a cohort of mass screening. Kidney Int. 49, 800-805 (1996). (Pubitemid 26093091)
27. Ruggenenti, P. et al. Proteinuria predicts end-stage renal failure in non-diabetic chronic nephropathies. The "Gruppo Italiano di Studi Epidemiologici in Nefrologia" (GISEN). Kidney Int. Suppl. 63, S54-S57 (1997). (Pubitemid 28020433)
28. Ruggenenti, P., Perna, A., Mosconi, L., Pisoni, R. & Remzzi, G. Urinary protein excretion rate is the best independent predictor of ESRF in non-diabetic proteinuric chronic nephropathies. "Gruppo Italiano di Studi Epidemiologici in Nefrologia" (GISEN). Kidney Int. 53, 1209-1216 (1998). (Pubitemid 28316881)
29. Peterson, J. C. et al. Blood pressure control, proteinuria, and the progression of renal disease. The Modification of Diet in Renal Disease study. Ann. Intern. Med. 123, 754-762 (1995).
30. Wright, J. T. Jr et al. Effect of blood pressure lowering and antihypertensive drug class on progression of hypertensive kidney disease: results from the AASK trial. JAMA 288, 2421-2431 (2002). (Pubitemid 35340538)
31. Retnakaran, R., Cull, C. A., Thorne, K. I., Adler, A. I. & Holman, R. R. Risk factors for renal dysfunction in type 2 diabetes: U. K. Prospective Diabetes Study 74. Diabetes 55, 1832-1839 (2006). (Pubitemid 44324140)
32. Keane, W. F. et al. Risk scores for predicting outcomes in patients with type 2 diabetes and nephropathy: the RENAAL study. Clin. J. Am. Soc. Nephrol. 1, 761-767 (2006).
33. Atkins, R. C. et al. Proteinuria reduction and progression to renal failure in patients with type 2 diabetes mellitus and overt nephropathy Am. J. Kidney Dis. 45, 281-287 (2005). (Pubitemid 40431053)
34. De Zeeuw, D. et al. Renal risk and renoprotection among ethnic groups with type 2 diabetic nephropathy: a post hoc analysis of RENAAL. Kidney Int. 69, 1675-1682 (2006).
35. Remuzzi, G. & Bertani, T. Pathophysiology of progressive nephropathies. N. Engl. J. Med. 339, 1448-1456 (1998). (Pubitemid 28516069)
36. Group, T. G. Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. Lancet 349, 1857-1863 (1997).
37. Ruggenenti, P., Perna, A. & Remuzzi, G. Retarding progression of chronic renal disease: the neglected issue of residual proteinuria. Kidney Int. 63, 2254-2261 (2003). (Pubitemid 36605839)
38. Bjorck, S., Mulec, H., Johnsen, S. A., Norden, G. & Aurell, M. Renal protective effect of enalapri in diabetic nephropathy. BMJ 304, 339-343 (1992).
39. Lewis, E. J., Hunsicker, L. G., Bain, R. P. & Rohde, R. D. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N. Engl. J. Med. 329, 1456-1462 (1993). (Pubitemid 23335891)
40. Jafar, T. H. et al. Angiotensin-converting enzyme inhibitors and progression of nondiabetic renal disease. A meta-analysis of patient-level data. Ann. Intern. Med. 135, 73-87 (2001). (Pubitemid 32661190)
41. Ruggenenti, P., Schieppati, A. & Remuzzi, G. Progression, remission, regression of chronic renal diseases. Lancet 357, 1601-1608 (2001). (Pubitemid 32488830)
42. Vegter, S. et al. Sodium Intake, ACE Inhibition, and Progression to ESRD. J. Am. Soc. Nephrol. 23, 165-173 (2012).
43. Campbell, R. et al. Effects of combined ACE inhibitor and angiotensin II antagonist treatment in human chronic nephropathies. Kidney Int. 63, 1094-1103 (2003). (Pubitemid 36315589)
44. Hovind, P. et al. Remission of nephrotic-range albuminuria in type 1 diabetic patients. Diabetes Care 24, 1972-1977 (2001). (Pubitemid 33716511)
45. 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)
46. Ruggenenti, P. et al. Effects of verapami added-on trandolapril therapy in hypertensive type 2 diabetes patients with microalbuminuria: the BENEDICT-B randomized trial. J. Hypertens. 29, 207-216 (2011).
47. Schmieder, R. E. et al. Changes in albuminuria predict mortality and morbidity in patients with vascular disease. J. Am. Soc. Nephrol. 22, 1353-1364 (2011).
48. Sandhu, S., Wiebe, N., Fried, L. F. & Tonelli, M. Statins for improving renal outcomes: a meta-analysis. J. Am. Soc. Nephrol. 17, 2006-2016 (2006). (Pubitemid 44036185)
49. Conley, J., Olafsson, A. & Djamali, A. Do statins delay the incidence of ESRD in diabetic patients with moderate CKD? J. Nephrol. 23, 321-327 (2010).
50. Ruggenenti, P. et al. Effects of add-on fluvastatin therapy in patients with chronic proteinuric nephropathy on dual renin-angiotensin system blockade: The ESPLANADE Trial. Clin. J. Am. Soc. Nephrol. 5, 1928-1938 (2010).
51. Zoja, C. et al. How to fully protect the kidney in a severe model of progressive nephropathy: a multidrug approach. J. Am. Soc. Nephrol. 13, 2898-2908 (2002). (Pubitemid 35386909)
52. Ruggenenti, P. et al. Role of remission clinics in the longitudinal treatment of CKD. J. Am. Soc. Nephrol. 19, 1213-1224 (2008).
53. Ruggenenti, P. et al. Preventing microalbuminuria in type 2 diabetes. N. Engl. J. Med. 351, 1941-1951 (2004). (Pubitemid 39447135)
54. Nielsen, S. E. et al. Neutrophil gelatinase-associated lipocalin (NGAL) and kidney injury molecule 1 (KIM1) in patients with diabetic nephropathy: a cross-sectional study and the effects of lisinopril. Diabet. Med. 27, 1144-1150 (2010).
55. Nielsen, S. E. et al. Urinary liver-type fatty acid-binding protein predicts progression to nephropathy in type 1 diabetic patients. Diabetes Care 33, 1320-1324 (2010).
56. Nielsen, S. E. et al. Tubular markers do not predict the decline in glomerular filtration rate in type 1 diabetic patients with overt nephropathy. Kidney Int. 79, 1113-1118 (2011).
57. Levey, A. S. et al. Proteinuria as a surrogate outcome in CKD: report of a scientific workshop sponsored by the National Kidney Foundation and the US Food and Drug Administration. Am. J. Kidney Dis. 54, 205-226 (2009).
58. Xie, D., Hou, F. F., Fu, B. L., Zhang, X. & Liang, M. High level of proteinuria during treatment with renin-angiotensin inhibitors is a strong predictor of renal outcome in nondiabetic kidney disease. J. Clin. Pharmacol. 51, 1025-1034 (2011).
59. Lea, J. et al. The relationship between magnitude of proteinuria reduction and risk of end-stage renal disease: results of the African American study of kidney disease and hypertension. Arch. Intern. Med. 165, 947-953 (2005). (Pubitemid 40563243)
60. De Zeeuw, D. et al. Proteinuria, a target for renoprotection in patients with type 2 diabetic nephropathy: lessons from RENAAL. Kidney Int. 65, 2309-2320 (2004). (Pubitemid 38670018)
61. Hunsicker, L. G. et al. Impact of irbesartan, blood pressure control, and proteinuria on renal outcomes in the Irbesartan Diabetic Nephropathy Trial. Kidney Int. Suppl. 92, S99-S101 (2004). (Pubitemid 43361441)
62. Hellemons, M. E. et al. Initial angiotensin receptor blockade-induced decrease in albuminuria is associated with long-term renal outcome in type 2 diabetic patients with microalbuminuria: a post hoc analysis of the RMA-2 trial. Diabetes Care 34, 2078-2083 (2011).
63. Holtkamp, F. A. et al. Albuminuria and blood pressure, independent targets for cardioprotective therapy in patients with diabetes and nephropathy: a post hoc analysis of the combined RENAAL and IDNT trials. Eur. Heart J. 32, 1493-1499 (2011).