Angiotensin-converting enzyme inhibitors, angiotensin receptor blockers and combined therapy in patients with micro-and macroalbuminuria and other cardiovascular risk factors: A systematic review of randomized controlled trials

Nephrology Dialysis Transplantation

Volumn 26, Issue 9, 2011, Pages 2827-2847

  Maione, Ausilia ^a   Navaneethan, Sankar D ^b,c   Graziano, Giusi ^a   Mitchell, Ruth ^c   Johnson, David ^d   Mann, Johannes F E ^e,f   Gao, Peggy ^e   Craig, Jonathan C ^c,g   Tognoni, Giovanni ^a   Perkovic, Vlado ^h   Nicolucci, Antonio ^a   De Cosmo, Salvatore ⁱ   Sasso, Antonio ^j   Lamacchia, Olga ^k   Cignarelli, Mauro ^k   Maria Manfreda, Valeria ^l   Gentile, Giorgio ^m,n   Strippoli, Giovanni F M ^a,c,g,n,o  

^a Mario Negri Sud Consortium ^*  (Italy)

^b LERNER RESEARCH INSTITUTE   (United States)

^c CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e MCMASTER UNIVERSITY   (Canada)

^f Schwabing General Hospital   (Germany)

^g UNIVERSITY OF SYDNEY   (Australia)

^h UNIVERSITY OF SYDNEY   (Australia)

ⁱ CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^j Ospedale Trani ASL BAT   (Italy)

^k UNIVERSITY OF FOGGIA   (Italy)

^l Ospedale A Perrino   (Italy)

^m UNIVERSITY OF PERUGIA   (Italy)

ⁿ Diaverum Italy Medical Office   (Italy)

^o Diaverum Medical Scientific Office   (Sweden)

more..

Author keywords

angiotensin receptor blockers; angiotensin converting enzyme inhibitors; macroalbuminuria; microalbuminuria

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; BENAZEPRIL; CANDESARTAN; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; FOSINOPRIL; IMIDAPRIL; IRBESARTAN; LISINOPRIL; LOSARTAN; PERINDOPRIL; PLACEBO; RAMIPRIL; TELMISARTAN; TRANDOLAPRIL; VALSARTAN;

ANGIONEUROTIC EDEMA; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CEREBROVASCULAR DISEASE; COUGHING; DISEASE COURSE; DRUG EFFECT; DRUG INDUCED HEADACHE; HUMAN; HYPERKALEMIA; HYPOTENSION; KIDNEY FAILURE; MACROALBUMINURIA; MICROALBUMINURIA; MONOTHERAPY; MORTALITY; NAUSEA; PERIPHERAL EDEMA; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK BENEFIT ANALYSIS; RISK REDUCTION; SYSTEMATIC REVIEW; TREATMENT RESPONSE;

ALBUMINURIA; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; CARDIOVASCULAR DISEASES; DIABETES COMPLICATIONS; DIABETES MELLITUS; HUMANS; KIDNEY; PROGNOSIS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK FACTORS; SURVIVAL RATE;

EID: 79959866121     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfq792     Document Type: Article

References (146)

1. Coresh J, Selvin E, Stevens LA et al. Prevalence of chronic kidney disease in the United States. JAMA 2007; 298: 2038-2047 (Pubitemid 350074801)
2. Hillege HL, Janssen WM, Bak AA et al. Microalbuminuria is common, also in a nondiabetic, nonhypertensive population, and an independent indicator of cardiovascular risk factors and cardiovascular morbidity. J Intern Med 2001; 249: 519-526 (Pubitemid 32823860)
3. Atkins RC, Polkinghorne KR, Briganti EM et al. Prevalence of albuminuria in Australia: the AusDiab Kidney Study. Kidney Int Suppl 2004; 11: S22-S24
4. Yuyun MF, Khaw KT, Luben R 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 2004; 159: 284-293 (Pubitemid 38141658)
5. Ninomiya T, Perkovic V, de Galan BE et al. Albuminuria and kidney function independently predict cardiovascular and renal outcomes in diabetes. J Am Soc Nephrol 2009; 20: 1813-1821
6. Casiglia E, Zanette G, Mazza A et al. Cardiovascular mortality in non-insulin-dependent diabetes mellitus. A controlled study among 683 diabetics and 683 age-and sex-matched normal subjects. Eur J Epidemiol 2000; 16: 677-684
7. Mattock MB, Morrish NJ, Viberti G et al. Prospective study of microalbuminuria as predictor of mortality in NIDDM. Diabetes 1992; 41: 736-741
8. Jensen JS, Feldt-Rasmussen B, Strandgaard S et al. Arterial hypertension, microalbuminuria, and risk of ischemic heart disease. Hypertension 2000; 35: 898-903 (Pubitemid 30303947)
9. Ostgren CJ, Lindblad U, Melander A et al. Survival in patients with type 2 diabetes in a Swedish community: skaraborg hypertension and diabetes project. Diabetes Care 2002; 25: 1297-1302 (Pubitemid 41071135)
10. Esteghamati A, Rashidi A, Khalilzadeh O et al. Metabolic syndrome is independently associated with microalbuminuria in type 2 diabetes. Acta Diabetol 2010; 47: 125-130
11. Thoenes M, Reil JC, Khan BV et al. Abdominal obesity is associated with microalbuminuria and an elevated cardiovascular risk profile in patients with hypertension. VascHealth RiskManag 2009; 5: 577-585
12. Chobanian AV, Bakris GL, Black HR et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 2003; 289: 2560-2572 (Pubitemid 37430158)
13. National KF. K/DOQI clinical practice guidelines on hypertension and antihypertensive agents in chronic kidney disease. Am J Kidney Dis 2004; 43: S1-S290
14. European Society of Hypertension-European Society of Cardiology, Guidelines Committee. European Society of Hypertension-European Society of Cardiology guidelines for the management of arterial hypertension. J Hypertens 2003; 21: 1011-1053
15. Williams B, Poulter NR, Brown MJ et al. British Hypertension Society guidelines for hypertension management 2004 (BHS-IV): summary. BMJ 2004; 328: 634-640 (Pubitemid 38340037)
16. Strippoli GF, Craig M, Deeks JJ et al. Effects of angiotensin converting enzyme inhibitors and angiotensin II receptor antagonists on mortality and renal outcomes in diabetic nephropathy: systematic review. BMJ 2004; 329: 828
17. Unger T, Stoppelhaar M. Rationale for double renin-angiotensinaldosterone system blockade. Am J Cardiol 2007; 100: 25J-31J
18. ONTARGET Investigators. Yusuf S, Teo KK et al. Telmisartan, ramipril, or both in patients at high risk for vascular events. N Engl J Med 2008; 358: 1547-1559 (Pubitemid 351522739)
19. Mann JF, Schmieder RE, McQueen M 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 2008; 372: 547-553
20. Liberati A, Altman DG, Tetzlaff J et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med 2009; 151: W65-W94
21. Higgins JP, Thompson SG, Deeks JJ et al. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560 (Pubitemid 37088507)
22. Estacio RO, Schrier RW. Antihypertensive therapy in type 2 diabetes: implications of the appropriate blood pressure control in diabetes (ABCD) trial. Am J Cardiol 1998; 82: 9R-14R
23. Ahmad J, Siddiqui MA, Ahmad H. Effective postponement of diabetic nephropathy with enalapril in normotensive type 2 diabetic patients with microalbuminuria. Diabetes Care 1997; 20: 1576-1581 (Pubitemid 27415037)
24. Ahmad J, Shafique S, Abidi SM et al. Effect of 5-year enalapril therapy on progression of microalbuminuria and glomerular structural changes in type 1 diabetic subjects. Diabetes Res Clin Pract 2003; 60: 131-138 (Pubitemid 36434265)
25. Maschio G, Alberti D, Janin G et al. Effect of the angiotensinconverting- 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 1996; 334: 939-945 (Pubitemid 26114159)
26. Chan JC, Ko GT, Leung DH et al. Long-term effects of angiotensinconverting enzyme inhibition and metabolic control in hypertensive type 2 diabetic patients. Kidney Int 2000; 57: 590-600 (Pubitemid 30430651)
27. Bakris GL, Slataper R, Vicknair N et al. ACE inhibitor mediated reductions in renal size and microalbuminuria in normotensive, diabetic subjects. J Diabetes Complications 1994; 8: 2-6 (Pubitemid 24371434)
28. Bauer JH, Reams GP, Hewett J et al. A randomized, double-blind, placebo-controlled trial to evaluate the effect of enalapril in patients with clinical diabetic nephropathy. Am J Kidney Dis 1992; 20: 443-457
29. Bilo H, Kluitman E, van Ballegooie E et al. Long term use of captopril or nifedipine in normotensive microalbuminuric patients with insulin-dependent diabetes mellitus. Diabetes Res 1993; 23: 115-122
30. Bojestig M, Karlberg BE, Lindstrom T et al. Reduction in ACE activity is insufficient to decrease microalbuminuria in normotensive patients with type 1 diabetes. Diabetes Care 2001; 24: 924
31. Capek M, Schnack C, Ludvik B et al. Effects of captopril treatment versus placebo on renal function in type 2 diabetic patients with microalbuminuria: a long-term study. Clin Investig 1994; 72: 961-966
32. Lewis EJ, Hunsicker LG, Bain RP et al. The effects of angiotension converting enzyme inhibition to diabetic nephropathy. N Engl J Med 1993; 329: 1456-1462 (Pubitemid 23335891)
33. Carella MJ, Gossain VV, Jones J. The effects of a low-dose regimen of fosinopril on elevated urinary albumin excretion in normotensive type 1 diabetic patients. J Med 1999; 30: 305-320 (Pubitemid 30366335)
34. Chase HP, Garg SK, Harris S et al. Angiotensin-converting enzyme inhibitor treatment for young normotensive diabetic subjects: a twoyear trial. Ann Ophthalmol 1993; 25: 284-289
35. Cordonnier DJ, Pinel N, Barro C et al. Expansion of cortical interstitium is limited by converting enzyme inhibition in type 2 diabetic patients with glomerulosclerosis. The Diabiopsies Group. J Am Soc Nephrol 1999; 10: 1253-1263 (Pubitemid 29246990)
36. Crepaldi G, Carta Q, Deferrari G et al. Effects of lisinopril and nifedipine on the progression to overt albuminuria in IDDM patients with incipient nephropathy and normal blood pressure. The Italian Microalbuminuria Study Group in IDDM. Diabetes Care 1998; 21: 104-110 (Pubitemid 28030395)
37. Marre M, Lievre M, Chatellier G et al. 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 2004; 328: 495
38. Durruty P, Krause P, Perez F et al. [Microalbuminuria in insulindependent diabetics: the prevention of diabetic nephropathy]. Rev Med Chil 1990; 118: 1319-1325
39. Baines LA. for the ESPRIT Study. Effect of 3 years of antihypertensive therapy on renal structure in type 1 diabetic patients with albuminuria: the European Study for the Prevention of Renal Disease in Type 1 Diabetes (ESPRIT). Diabetes 2001; 50: 843-850 (Pubitemid 32242643)
40. Euclid SG. Randomised placebo-controlled trial of lisinopril in normotensive patients with insulin-dependent diabetes and normoalbuminuria or microalbuminuria. The EUCLID Study Group. Lancet 1997; 349: 1787-1792
41. Garg SK, Chase HP, Jackson WE et al. Renal and retinal changes after treatment with ramipril and pentoxifyline in subjects with IDDM. Ann Ophthalmol-Glauc 1998; 30: 33-37 (Pubitemid 28128821)
42. Giri S, Mahajan SK, Sen R et al. Effects of angiotensin converting enzyme inhibitor on renal function in patients of membranoproliferative glomerulonephritis with mild to moderate renal insufficiency. J Assoc Physicians India 2002; 50: 1245-1249
43. Group 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. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia). Lancet 1997; 349: 1857-1863
44. Yusuf S, Sleight P, Pogue J et al. Effects of an angiotensinconverting- enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 2000; 342: 145-153
45. Hansen KW, Klein F, Christensen PD et al. Effects of captopril on ambulatory blood pressure, renal and cardiac function in microalbuminuric type 1 diabetic patients. Diabetes Metab 1994; 20: 485-493
46. Hou FF, Zhang X, Zhang GH et al. Efficacy and safety of benazepril for advanced chronic renal insufficiency. N Engl J Med 2006; 354: 131-140 (Pubitemid 43076710)
47. Ihle BU, Whitworth JA, Shahinfar S et al. Angiotensin-converting enzyme inhibition in nondiabetic progressive renal insufficiency: a controlled double-blind trial. Am J Kidney Dis 1996; 27: 489-495 (Pubitemid 26106596)
48. Ishimitsu T, Akashiba A, Kameda T et al. Benazepril slows progression of renal dysfunction in patients with non-diabetic renal disease. Nephrology (Carlton) 2007; 12: 294-298 (Pubitemid 46718204)
49. Katayama S, Kikkawa R, Isogai S et al. Effect of captopril or imidapril on the progression of diabetic nephropathy in Japanese with type 1 diabetes mellitus: a randomized controlled study (JAPANIDDM). Diabetes Res Clin Pract 2002; 55: 113-121 (Pubitemid 34048699)
50. Jerums G, Allen TJ, Campbell DJ et al. Long-term comparison between perindopril and nifedipine in normotensive patients with type 1 diabetes and microalbuminuria. Am J Kidney Dis 2001; 37: 890-899 (Pubitemid 32471847)
51. Jerums G, Allen TJ, Campbell DJ et al. Long-term renoprotection by perindopril or nifedipine in non-hypertensive patients with Type 2 diabetes and microalbuminuria. Diabetes Med 2004; 21: 1192-1199 (Pubitemid 39472374)
52. Laffel LM, McGill JB, Gans DJ. The beneficial effect of angiotensinconverting enzyme inhibition with captopril on diabetic nephropathy in normotensive IDDM patients with microalbuminuria. North American Microalbuminuria Study Group. Am J Med 1995; 99: 497-504
53. Lebovitz HE, Wiegmann TB, Cnaan A et al. Renal protective effects of enalapril in hypertensive NIDDM: role of baseline albuminuria. Kidney Int Suppl 1994; 45: S150-S155
54. Marre M, Leblanc H, Suarez L et al. Converting enzyme inhibition and kidney function in normotensive diabetic patients with persistent microalbuminuria. Br Med J (Clin Res Ed) 1987; 294: 1448-1452 (Pubitemid 17079620)
55. Nankervis A, Nicholls K, Kilmartin G et al. Effects of perindopril on renal histomorphometry in diabetic subjects with microalbuminuria: a 3-year placebo-controlled biopsy study. Metabolism 1998; 47: 12-15
56. O'Donnell MJ, Rowe BR, Lawson N et al. Placebo-controlled trial of lisinopril in normotensive diabetic patients with incipient nephropathy. J Hum Hypertens 1993; 7: 327-332 (Pubitemid 23243378)
57. Parving HH, Hommel E, Jensen BR et al. Long-term beneficial effect of ACE inhibition on diabetic nephropathy in normotensive type 1 diabetic patients. Kidney Int 2001; 60: 228-234 (Pubitemid 32587558)
58. Phillips PJ, Phillipou G, Bowen KM et al. Diabetic microalbuminuria and cilazapril. Am J Med 1993; 94: 58S-60S
59. Poulsen PL, Ebbehoj E, Nosadini R et al. Early ACE-i intervention in microalbuminuric patients with type 1 diabetes: effects on albumin excretion, 24 h ambulatory blood pressure, and renal function. Diabetes Metab 2001; 27: 123-128 (Pubitemid 32416869)
60. Preston RA, Materson BJ, Reda DJ et al. Proteinuria in mild to moderate hypertension: results of the VA cooperative study of six antihypertensive agents and placebo. Department of Veterans Affairs Cooperative Study Group on Antihypertensive Agents. Clin Nephrol 1997; 47: 310-315 (Pubitemid 27230628)
61. Ravid M, Savin H, Jutrin I et al. Long-term stabilizing effect of angiotensin-converting enzyme inhibition on plasma creatinine and on proteinuria in normotensive type II diabetic patients. Ann Intern Med 1993; 118: 577-581 (Pubitemid 23102690)
62. Ruggenenti PF, Perna AF, Gherardi GF et al. Renoprotective properties of ACE-inhibition in non-diabetic nephropathies with nonnephrotic proteinuria. Lancet 1999; 354: 359-364
63. Sano T, Kawamura T, Matsumae H et al. Effects of long-term enalapril treatment on persistent micro-albuminuria in well-controlled hypertensive and normotensive NIDDM patients. Diabetes Care 1994; 17: 420-424 (Pubitemid 24145216)
64. Sano T, Hotta N, Kawamura T et al. Effects of long-term enalapril treatment on persistent microalbuminuria in normotensive type 2 diabetic patients: results of a 4-year, prospective, randomized study. Diabetes Med 1996; 13: 120-124 (Pubitemid 26074289)
65. Semetkowska-Jurkiewicz E, Milewski J, Krupa-Wojciechowska B et al. [Blood pressure and blood lipids in normotensive patients with diabetes mellitus type I with microalbuminuria]. Pol Tyg Lek 1992; 47: 1042-1044
66. Tong PC, Ko GT, Chan WB et al. The efficacy and tolerability of fosinopril in Chinese type 2 diabetic patients with moderate renal insufficiency. Diabetes Obes Metab 2006; 8: 342-347
67. Trevisan R, Tiengo A. Effect of low-dose ramipril on microalbuminuria in normotensive or mild hypertensive non-insulin-dependent diabetic patients. North-East Italy Microalbuminuria Study Group. Am J Hypertens 1995; 8: 876-883
68. Viberti G, Mogensen CE, Groop LC et al. Effect of captopril on progression to clinical proteinuria in patients with insulin-dependent diabetes mellitus and microalbuminuria. European Microalbuminuria Captopril Study Group. JAMA 1994; 271: 275-279 (Pubitemid 24030753)
69. Yao B, Hu G, Li Y et al. [The effect of perindopril in treatment of early diabetic nephropathy with normal blood pressure and microalbuminuria]. Zhonghua Nei Ke Za Zhi 2001; 40: 826-828
70. Bedigian MP. Improving the prognosis of diabetic patients: evaluating the role of intensive versus moderate blood pressure control with selective angiotensin II receptor blocker (ARB) therapy. J Renin Angiotensin Aldosterone Syst 2000; 1: S25-S28
71. Dragovic T, Hrvacevic R, Ajdinovic B et al. [Efficacy of valsartan in the treatment of persistent microalbuminuria in normotensive patients with type 1 diabetes]. Vojnosanit Pregl 2003; 60: 555-564
72. Parving HH, Lehnert H, Brochner-Mortensen J et al. The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med 2001; 345: 870-878
73. Makino H, Haneda M, Babazono T et al. Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care 2007; 30: 1577-1578 (Pubitemid 46871174)
74. Lewis EJ, Hunsicker LG, Clarke WR et al. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 2001; 345: 851-860
75. Plum J, Bunten B, Nemeth R et al. Effects of the angiotensin II antagonist valsartan on blood pressure, proteinuria, and renal hemodynamics in patients with chronic renal failure and hypertension. J Am Soc Nephrol 1998; 9: 2223-2234 (Pubitemid 28543800)
76. Brenner BM, Cooper ME, de Zeeuw D et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 2001; 345: 861-869
77. Tan KC, Chow WS, Ai VH et al. Effects of angiotensin II receptor antagonist on endothelial vasomotor function and urinary albumin excretion in type 2 diabetic patients with microalbuminuria. Diabetes Metab Res Rev 2002; 18: 71-76 (Pubitemid 34257369)
78. Telmisartan Randomised AssessmeNt Study in ACE iNtolerant subjects with cardiovascular Disease (TRANSCEND) Investigators. Yusuf S, Teo K et al. Effects of the angiotensin-receptor blocker telmisartan on cardiovascular events in high-risk patients intolerant to angiotensin-converting enzyme inhibitors: a randomised controlled trial. Lancet 2008; 372: 1174-1183
79. Abe H, Minatoguchi S, Ohashi H et al. Renoprotective effect of the addition of losartan to ongoing treatment with an angiotensin converting enzyme inhibitor in type-2 diabetic patients with nephropathy. Hypertens Res 2007; 30: 929-935 (Pubitemid 350120970)
80. Altiparmak MR, Trablus S, Apaydin S et al. Is losartan as effective as enalapril on posttransplant persistent proteinuria? Transplant Proc 2001; 33: 3368-3369 (Pubitemid 34042608)
81. Barnett AH, Bain SC, Bouter P et al. Angiotensin-receptor blockade versus converting-enzyme inhibition in type 2 diabetes and nephropathy. N Engl J Med 2004; 351: 1952-1961 (Pubitemid 39447136)
82. Kavgaci H, Sahin A, Onder EH et al. The effects of losartan and fosinopril in hypertensive type 2 diabetic patients. Diabetes Res Clin Pract 2002; 58: 19-25 (Pubitemid 34823621)
83. Ko GT, Tsang CC, Chan HC. Stabilization and regression of albuminuria in Chinese patients with type 2 diabetes: a one-year randomized study of valsartan versus enalapril. Adv Ther 2005; 22: 155-162 (Pubitemid 40874909)
84. Lacourciere Y, Belanger A, Godin C et al. Long-term comparison of losartan and enalapril on kidney function in hypertensive type 2 diabetics with early nephropathy. Kidney Int 2000; 58: 762-769 (Pubitemid 30620026)
85. Matsuda H, Hayashi K, Homma K et al. Differing anti-proteinuric action of candesartan and losartan in chronic renal disease. Hypertens Res 2003; 26: 875-880 (Pubitemid 37508964)
86. Matsuda H, Hayashi K, Saruta T. Distinct time courses of renal protective action of angiotensin receptor antagonists and ACE inhibitors in chronic renal disease. J Hum Hypertens 2003; 17: 271-276 (Pubitemid 36592019)
87. Cheung R, Lewanczuk RZ, Rodger NW et al. The effect of valsartan and captopril on lipid parameters in patients with type II diabetes mellitus and nephropathy. Int J Clin Pract 1999; 53: 584-592
88. Rizzoni D, Porteri E, De Ciuceis C et al. Effect of treatment with candesartan or enalapril on subcutaneous small artery structure in hypertensive patients with noninsulin-dependent diabetes mellitus. Hypertension 2005; 45: 659-665 (Pubitemid 40418362)
89. Hou FF, Xie D, Zhang X 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 2007; 18: 1889-1898 (Pubitemid 46870325)
90. Rutkowski P, Tylicki L, Renke M et al. Low-dose dual blockade of the renin-angiotensin system in patients with primary glomerulonephritis. Am J Kidney Dis 2004; 43: 260-268 (Pubitemid 38146324)
91. Atmaca A, Gedik O. Effects of angiotensin-converting enzyme inhibitors, angiotensin II receptor blockers, and their combination on microalbuminuria in normotensive patients with type 2 diabetes. Adv Ther 2006; 23: 615-622 (Pubitemid 44747441)
92. Andersen NH, Poulsen PL, Knudsen ST et al. Long-term dual blockade with candesartan and lisinopril in hypertensive patients with diabetes: the CALM II study. Diabetes Care 2005; 28: 273-277 (Pubitemid 40170925)
93. Shoda J, Kanno Y, Suzuki H. A five-year comparison of the renal protective effects of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in patients with non-diabetic nephropathy. Intern Med 2006; 45: 193-198
94. Nakamura T, Ushiyama C, Suzuki S et al. Comparison between the angiotensin II receptor antagonist candesartan cilexetil and the angiotensin-converting enzyme inhibitor trandolapril in microalbuminuria of patients with early diabetic nephropathy. Nephron 2000; 86: 247
95. Ogawa S, Mori T, Nako K et al. Angiotensin II type 1 receptor blockers reduce urinary oxidative stress markers in hypertensive diabetic nephropathy. Hypertension 2006; 47: 699-705 (Pubitemid 43740241)
96. Renke M, Tylicki L, Rutkowski P et al. Low-dose angiotensin II receptor antagonists and angiotensin II-converting enzyme inhibitors alone or in combination for treatment of primary glomerulonephritis. Scand J Urol Nephrol 2004; 38: 427-433 (Pubitemid 39551354)
97. Segura J, Praga M, Campo C et al. Combination is better than monotherapy with ACE inhibitor or angiotensin receptor antagonist at recommended doses. J Renin Angiotensin Aldosterone Syst 2003; 4: 43-47 (Pubitemid 36443386)
98. Sengul AM, Altuntas YF, Kurklu AF et al. Beneficial effect of lisinopril plus telmisartan in patients with type 2 diabetes, microalbuminuria and hypertension. Diabetes Res Clin Pract 2006; 71: 210-219 (Pubitemid 43112114)
99. Mori-Takeyama U, Minatoguchi S, Murata I et al. Dual blockade of the rennin-angiotensin system versus maximal recommended dose of angiotensin II receptor blockade in chronic glomerulonephritis. Clin Exp Nephrol 2008; 12: 33-40
100. Tutuncu NB, Gurlek A, Gedik O. Efficacy of ACE inhibitors and ATII receptor blockers in patients with microalbuminuria: a prospective study. Acta Diabetol 2001; 38: 157-161 (Pubitemid 34145694)
101. Menne J, Farsang C, Deak L et al. Valsartan in combination with lisinopril versus the respective high dose monotherapies in hypertensive patients with microalbuminuria: the VALERIA trial. J Hypertens 2008; 26: 1860-1867
102. Durruty P, Tapia JC, Ugarte C et al. [Urinary albumin excretion in non-insulin-dependent diabetic patients. Effects of an angiotensinconverting enzyme inhibitor]. Rev Med Chil 1996; 124: 1036-1044
103. Stornello M, Valvo EV, Puglia N et al. Angiotensin converting enzyme inhibition with a low dose of enalapril in normotensive diabetics with persistent proteinuria. J Hypertens Suppl 1988; 6: S464-S466 (Pubitemid 19067375)
104. Stornello M, Valvo EV, Scapellato L. Hemodynamic, renal, and humoral effects of the calcium entry blocker nicardipine and converting enzyme inhibitor captopril in hypertensive type II diabetic patients with nephropathy. J Cardiovasc Pharmacol 1989; 14: 851-855 (Pubitemid 20008843)
105. Romero R, Salinas I, Lucas A et al. Renal function changes in microalbuminuric normotensive type II diabetic patients treated with angiotensin-converting enzyme inhibitors. Diabetes Care 1993; 16: 597-600 (Pubitemid 23097208)
106. Schrier RW, Estacio RO, Esler A et al. Effects of aggressive blood pressure control in normotensive type 2 diabetic patients on albuminuria, retinopathy and strokes. Kidney Int 2002; 61: 1086-1097 (Pubitemid 34175478)
107. Estacio RO, Coll JR, Tran ZV et al. Effect of intensive blood pressure control with valsartan on urinary albumin excretion in normotensive patients with type 2 diabetes. Am J Hypertens 2006; 19: 1241-1248 (Pubitemid 44856249)
108. Gerstein HC, Mann JF, Yi Q et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 2001; 286: 421-426 (Pubitemid 32681484)
109. Hallan SI, Ritz E, Lydersen S et al. Combining GFR and albuminuria to classify CKD improves prediction of ESRD. J Am Soc Nephrol 2009; 20: 1069-1077
110. Klausen K, Borch-Johnsen K, Feldt-Rasmussen B et al. Very low levels of microalbuminuria are associated with increased risk of coronary heart disease and death independently of renal function, hypertension, and diabetes. Circulation 2004; 110: 32-35 (Pubitemid 38880131)
111. Hillege HL, Fidler V, Diercks GF et al. Urinary albumin excretion predicts cardiovascular and noncardiovascular mortality in general population. Circulation 2002; 106: 1777-1782
112. Yuyun MF, Khaw KT, Luben R et al. Microalbuminuria, cardiovascular risk factors and cardiovascular morbidity in a British population: the EPIC-Norfolk population-based study. Eur J Cardiovasc Prev Rehabil 2004; 11: 207-213 (Pubitemid 38870067)
113. Yuyun MF, Khaw KT, Luben R et al. Microalbuminuria independently predicts all-cause and cardiovascular mortality in a British population: The European Prospective Investigation into Cancer in Norfolk (EPIC-Norfolk) population study. Int J Epidemiol 2004; 33: 189-198 (Pubitemid 38500176)
114. Yuyun MF, Khaw KT, Luben R et al. Microalbuminuria and stroke in a British population: the European Prospective Investigation into Cancer in Norfolk (EPIC-Norfolk) population study. J Intern Med 2004; 255: 247-256 (Pubitemid 38241369)
115. Brown MJ, Palmer CR, Castaigne A et al. Morbidity and mortality in patients randomised to double-blind treatment with a long-acting calcium-channel blocker or diuretic in the International Nifedipine GITS study: Intervention as a Goal in Hypertension Treatment (INSIGHT). Lancet 2000; 356: 366-372 (Pubitemid 30487492)
116. Hallan S, Astor B, Romundstad S et al. Association of kidney function and albuminuria with cardiovascular mortality in older vs. younger individuals: The HUNT II Study. Arch Intern Med 2007; 167: 2490-2496 (Pubitemid 350254909)
117. Irie F, Iso H, Sairenchi T et al. The relationships of proteinuria, serum creatinine, glomerular filtration rate with cardiovascular disease mortality in Japanese general population. Kidney Int 2006; 69: 1264-1271
118. Madison JR, Spies C, Schatz IJ et al. Proteinuria and risk for stroke and coronary heart disease during 27 years of follow-up: the Honolulu Heart Program. Arch Intern Med 2006; 166: 884-889
119. Gullion CM, Keith DS, Nichols GA et al. Impact of comorbidities on mortality in managed care patients with CKD. Am J Kidney Dis 2006; 48: 212-220 (Pubitemid 44051728)
120. Kunz R, Friedrich C, Wolbers M et al. Meta-analysis: effect of monotherapy and combination therapy with inhibitors of the renin angiotensin system on proteinuria in renal disease. Ann Intern Med 2008; 148: 30-48 (Pubitemid 351688350)
121. American Diabetes Association. Standards of medical care in diabetes-2006. Diabetes Care 2006; 29 (Suppl 1): S4-S42
122. Balamuthusamy S, Srinivasan L, Verma M et al. Renin angiotensin system blockade and cardiovascular outcomes in patients with chronic kidney disease and proteinuria: a meta-analysis. Am Heart J 2008; 155: 791-805 (Pubitemid 351601744)
123. Jafar TH, Schmid CH, Landa M et al. Angiotensin-converting enzyme inhibitors and progression of nondiabetic renal disease. A meta-analysis of patient-level data. Ann Intern Med 2001; 135: 73-87 (Pubitemid 32661190)
124. Kasiske BL, Kalil RS, Ma JZ et al. Effect of antihypertensive therapy on the kidney in patients with diabetes: a meta-regression analysis. Ann Intern Med 1993; 118: 129-138
125. Weidmann P, Boehlen LM, Court D. Effects of different antihypertensive drugs on human diabetic proteinuria. Nephrol Dial Transplant 1993; 8: 582-584 (Pubitemid 23231138)
126. Weidmann P, SchneiderM, Bohlen L. Therapeutic efficacy of different antihypertensive drugs in human diabetic nephropathy: an updated meta-analysis. Nephrol Dial Transplant 1995; 10 (Suppl 9): 39-45
127. Lovell HG. Angiotensin converting enzyme inhibitors in normotensive diabetic patients with microalbuminuria. Cochrane Database Sys Rev 2001; 1: CD002183
128. Klahr S, Levey AS, Beck GJ et al. The effects of dietary protein restriction and blood-pressure control on the progression of chronic renal disease. Modification of Diet in Renal Disease Study Group. N Engl J Med 1994; 330: 877-884 (Pubitemid 24094966)
129. Ruggenenti P, Perna A, Gherardi G et al. Renal function and requirement for dialysis in chronic nephropathy patients on long-term ramipril: REIN follow-up trial. Gruppo Italiano di Studi Epidemiologici in Nefrologia (GISEN). Ramipril Efficacy in Nephropathy. Lancet 1998; 352: 1252-1256 (Pubitemid 28470337)
130. de Galan BE, Perkovic V, Ninomiya T et al. Lowering blood pressure reduces renal events in type 2 diabetes. J Am Soc Nephrol 2009; 20: 883-892
131. Sarafidis PA, Stafylas PC, Kanaki AI et al. Effects of reninangiotensin system blockers on renal outcomes and all-cause mortality in patients with diabetic nephropathy: an updated meta-analysis. Am J Hypertens 2008; 21: 922-929
132. Reboldi G, Angeli F, Cavallini C et al. Comparison between angiotensin-converting enzyme inhibitors and angiotensin receptor blockers on the risk of myocardial infarction, stroke and death: a meta-analysis. J Hypertens 2008; 26: 1282-1289
133. MacKinnon M, Shurraw S, Akbari A 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 2006; 48: 8-20
134. Jennings DL, Kalus JS, Coleman CI et al. Combination therapy with an ACE inhibitor and an angiotensin receptor blocker for diabetic nephropathy: a meta-analysis. Diabetes Med 2007; 24: 486-493 (Pubitemid 46669317)
135. Hollenberg NK, Osei SY, Lansang MC et al. Salt intake and non-ACE pathways for intrarenal angiotensin II generation in man. J Renin Angiotensin Aldosterone Syst 2001; 2: 14-18 (Pubitemid 33687414)
136. Cohen DL, Townsend RR. Is there added value to adding ARB to ACE inhibitors in the management of CKD? J Am Soc Nephrol 2009; 20: 1666-1668
137. Nakao N, Yoshimura A, Morita H et al. Combination treatment of angiotensin-II receptor blocker and angiotensin-converting-enzyme inhibitor in non-diabetic renal disease (COOPERATE): a randomised controlled trial. Lancet 2003; 361: 117-124 (Pubitemid 36092015)
138. Strippoli GF, Jonathan CC. Combined treatment with angiotensinconverting enzyme inhibitors and angiotensin-receptor blockers to prevent end-stage kidney disease in patients who do not have diabetes. Med J Aust 2004; 181: 450-451 (Pubitemid 39419755)
139. Kunz R, Wolbers M, Glass T et al. The COOPERATE trial: a letter of concern. Lancet 2008; 371: 1575-1576 (Pubitemid 351626834)
140. Retraction-Combination treatment of angiotensin-II receptor blocker and angiotensin-converting-enzyme inhibitor in non-diabetic renal disease (COOPERATE): a randomised controlled trial. Lancet 2009; 374: 1226
141. Jafar TH, Schmid CH, Stark PC et al. The rate of progression of renal disease may not be slower in women compared with men: a patient-level meta-analysis. Nephrol Dial Transplant 2003; 18: 2047-2053 (Pubitemid 37220310)
142. Schunemann HJ, Oxman AD, Vist GE et al. Interpreting results and drawing conclusions. In: Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions, Version 5.0.2 (updated September 2008). Cochrane Collaboration. www.cochranhandbook. org (14 January 2011, date last accessed)
143. Sarnak MJ, Levey AS, Schoolwerth AC et al. 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: 2154-2169 (Pubitemid 37337595)
144. Mario Negri Institute for Pharmacological Research. http:/clinical trials.gov/ct2/show/study/NCT00494715 (31 December 2009, date last accessed)
145. Fried LF, Duckworth W, Zhang JH et al. Design of combination angiotensin receptor blocker and angiotensin-converting enzyme inhibitor for treatment of diabetic nephropathy (VA NEPHRON-D). Clin J Am Soc Nephrol 2009; 4: 361-368
146. Maione A, Nicolucci A, Craig JC et al. Protocol of the Long-term Impact of RAS Inhibition on Cardiorenal Outcomes (LIRICO) randomized trial. J Nephrol 2007; 20: 646-655 (Pubitemid 351266118)