The angiotensin-converting enzyme gene and its inhibition in diabetic nephropathy

Current Opinion in Endocrinology and Diabetes

Volumn 3, Issue 4, 1996, Pages 315-321

  Parving, Hans Henrik ^a   Tarnow, Lise ^a   Rossing, Peter ^a  

^a STENO DIABETES CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0002092673     PISSN: 10683097     EISSN: None     Source Type: Journal    
DOI: 10.1097/00060793-199608000-00006     Document Type: Article

References (75)

1. Parving H-H, Oxenbøll B, Svendsen PA, Christiansen JS, Andersen AR: Early detection of patients at risk of developing diabetic nephropathy. Acta Endocrinol 1982, 100:550-555.
2. Viberti GC, Hill RD, Jarrett RJ, Argyropoulos A, Mahmud U, Keen H: Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus. Lancet 1982, i:1430-1432.
3. Mogensen CE, Christensen CK: Predicting diabetic nephropathy in insulin-dependent patients. N Engl J Med 1984, 311:89-93.
4. Mathiesen ER, Oxenbøll B, Johansen K, Svendsen PA, Decken T: Incipient nephropathy in Type 1 (insulin-dependent) diabetes. Diabetologia 1984, 26:406-410.
5. Mogensen CE: Microalbuminuria predicts clinical proteinuria and early mortality in maturity onset diabetes. N Engl J Med 1984, 310:356-360.
6. Nelson RG, Knowler WC, Pettitt DJ, Saad MF, Charles MA, Bennett PH: Assessing risk of overt nephropathy in diabetic patients from albumin excretion in untimed urine specimens. Arch Intern Med 1991, 151:1761-1765.
7. Ballard DJ, Humphrey LL, Melton III LJ, Frohnert PP, Chu C-P, O'Fallon WM, Palumbo PJ: Epidemiology of persistent proteinuria in type II diabetes mellitus: population-based study in Rochester, Minnesota. Diabetes 1988, 37:405-412.
8. Gall M-A, Rossing P, Skøtt P, Damsbo P, Vaag A, Bech K, Dejgaard A, Lauritzen M, Lauritzen E, Hougaard P, Beck-Nielsen H, Parving HH: Prevalence of micro- and macroalbuminuria, arterial hypertension, retinopathy and large vessel disease in European type 2 (non-insulin dependent) diabetic patients. Diabetologia 1991, 34:655-661.
9. Parving H-H, Hommel E, Mathiesen ER, Skøtt P, Edsberg B, Bahnsen M, Lauritzen M, Hougaard P, Lauritzen E: Prevalence of microalbuminuria, arterial hypertension, retinopathy and neuropathy in patients with insulin-dependent diabetes. BMJ 1988, 296:156-160.
10. Rossing P, Rossing K, Jacobsen P, Parving H-H: Unchanged incidence of diabetic nephropathy in IDDM patients. Diabetes 1995, 44:739-743. This prospective observational study revealed no evidence of a calender effect (ie, declining incidence of diabetic nephropathy with increasing calender year of diabetes onset) in patients with onset of IDDM between 1965 and 1979.
11. Parving H-H, Østerby R, Anderson PW, Hsueh WA: Diabetic nephropathy. In The Kidney, 5th edn. Edited by Brenner BM. Philadelphia: WB Saunders; 1996:1864-1892.
12. Hostetter TH, Rennke HG, Brenner BM: The case for intrarenal hypertension in the initiation and progression of diabetic and other glomerulopathies. Am J Med 1982, 72:375-380.
13. Marre M, Bernadet P, Gallois Y, Savagner F, Guyenne T-T, Hallab M, Cambien F, Passa P, Alhenc-Gelas F: Relationships between angiotensin I converting enzyme gene polymorphism, plasma levels, and diabetic retinal and renal complications. Diabetes 1994, 43:384-388.
14. Hallab M, Bled F, Ebran JM, Suraniti S, Girault A, Fressinaud P, Marre M: Elevated serum angiotensin I converting enzyme activity in type I, insulin-dependent diabetic subjects with persistent microalbuminuria. Acta Diabetol 1992, 29:82-85.
15. Tarnow L, Cambien F, Rossing P, Nielsen FS, Hansen BV, Lecerf L, Poirier O, Danilov S, Parving H-H: Lack of relationship between an insertion/deletion polymorphism in the angiotensin-I-converting enzyme gene and diabetic nephropathy and proliferative retinopathy in IDDM patients. Diabetes 1995, 44:489-494. The largest association study addressing the ACE I/D polymorphism in IDDM patients with and without diabetic nephropathy. The genetic susceptibility to diabetic nephropathy and proliferative retinopathy could not be shown to be associated with the ACE I/D polymorphism, whereas the elevated plasma ACE concentration may play a role in the initiation and progression of diabetic nephropathy in white IDDM patients.
16. Rigat B, Hubert C, Alhenc-Gelas F, Cambien F, Corvol P, Soubrier F: An insertion/deletion polymorphism in angiotensin I converting enzyme gene accounting for half the variance of serum enzyme levels. J Clin Invest 1990, 86:1343-1346.
17. Cambien F, Poirier O, Lecerf L, Evans A, Cambou JP, Arveiler D, Luc G, Bard JM, Bara L, Ricard S, Tiret L, Amouyel P, Alhenc-Gelas F, Soubrier F: Deletion polymorphism in the gene for angiotensin-converting enzyme is a potent risk factor for myocardial infarction. Nature 1992, 359:641-644.
18. Parving H-H, Tarnow L, Rossing P: Genetics of diabetic nephropathy. J Am Soc Nephrol 1996, in press.
19. Doria A, Warram JH, Krolewski AS: Genetic predisposition to diabetic nephropathy: evidence for a role of the angiotensin I-converting enzyme gene. Diabetes 1994, 43:690-695.
20. Fogarty DG, Hughes AE, Nevin NC, Doherty CC, Maxwell AP: Functional genetic markers of the renin-angiotensin system and the risk of diabetic nephropathy (DN) in insulin-dependent diabetes mellitus (IDDM) [abstract]. J Am Soc Nephrol 1994, 5:376.
21. Schmidt S, Schöne N, Ritz E, the Diabetic Nephropathy Study Group: Association of ACE gene polymorphism and diabetic nephropathy? Kidney Int 1995, 47:1176-1181. No significant association between the ACE I/D polymorphism and nephropathy was demonstrated in this large study of NIDDM patients.
22. Powrie JK, Watts GF, Ingham JN, Taub NA, Talmud PJ, Shaw KM: Role of glycaemic control in development of microalbuminuria in patients with insulin dependent diabetes. BMJ 1994, 309:1608-1612.
23. Rabensteiner D, Mayer G, Abrahamian H, Illievich A, Schmid A, Irsigler K, Prager R: Relationship between angiotensin-I-converting enzyme polymorphism and microangiopathy in IDDM subjects [abstract]. Diabetologia 1995, 38:A227.
24. Hibberd ML, Millward BA, Demaine AG: Angiotensin converting enzyme genotypes and complications in type 1 diabetes [abstract]. Diabetologia 1995, 38:A227.
25. Chaturvedi N, Talmud P, Fuller JH: Angiotensin converting enzyme (ACE) gene polymorphisms and complications in insulin dependent diabetes mellitus (IDDM) [abstract]. Diabetologia 1995, 38:A227.
26. Bilo HJG, Thijssen S, de Knijff P, Stehouwer CDA, Kluft C: ACE and ANG gene polymorphism and diabetic nephropathy [abstract]. J Am Soc Nephrol 1995, 6:1037.
27. Jagger C, Kilpatnck ES, Small M, Spooner RJ: Angiotensin converting enzyme I/D polymorphism may not be associated with diabetic disease [abstract]. Diabet Med 1995, 12:S50.
28. Mizuiri S, Hemmi H, Inoue A, Yoshikawa H, Tanegashima M, Fushimi T, Ishigami M, Amagasaki Y, Ohara T, Shimatake H, Hasegawa A: Angiotensin-converting enzyme polymorphism and development of diabetic nephropathy in non-insulin-dependent diabetes mellitus. Nephron 1995, 70:455-459.
29. Fujisawa T, Ikegami H, Shen G-Q, Yamato E, Takekawa K, Nakagawa Y, Hamada Y, Ueda H, Rakugi H, Higaki J, Ohishi M, Jujii K, Fukuda M, Ogihara T: Angiotensin I-converting enzyme gene polymorphism is associated with myocardial infarction, but not with retinopathy or nephropathy, in NIDDM. Diabetes Care 1995, 18:983-985.
30. Dudley CRK, Keavney BD, Stratton IM, Turner RC, Ratcliffe PJ: U.K. Prospective Diabetes Study XV: relationship of renin-angiotensin system gene polymorphisms with microalbuminuria in NIDDM. Kidney Int 1995, 48:1907-1911. No significant association between the ACE/ID polymorphism and microalbuminuria in NIDDM patients was demonstrated. But in patients with microalbuminuria those with the DD genotype had a greater urinary albumin excretion than individuals with a non-DD genotype.
31. Doi Y, Yoshizumi H, Yoshinari M, Iino K, Yamamoto M, Ichikawa K, Iwase M, Fujishima M: Association between a polymorphism in the angiotensin-converting enzyme gene and microvascular complications in Japanese patients with NIDDM. Diabetologia 1996, 39:97-102.
32. Panagiotopoulos S, Smith TJ, Aldred GP, Baker EJ, Jacklin CJ, Jerums G: Angiotensin converting enzyme (ACE) gene polymorphism in type II diabetic patients with increased albumin excretion rate. J Diabetes Comp 1995, 9:272-276.
33. Marre M, Chatellier G, Leblanc H, Guyenne T-T, Ménard J, Passa P: Prevention of diabetic nephropathy with enalapril in normotensive diabetics with microalbuminuria. BMJ 1988, 297:1092-1095.
34. Mathiesen ER, Hommel E, Giese J, Parving H-H: Efficacy of captopril in postponing nephropathy in normotensive diabetic patients with microalbuminuria. BMJ 1991, 303:81-87.
35. Viberti GC, Mogensen CE, Groop L, Pauls JF, the European Microalbuminuria Captopril Study Group: Effect of captopril on progression to clinical proteinuria in patients with insulin-dependent diabetes mellitus and microalbuminuria. JAMA 1994, 271:275-279.
36. Laffel L, McGill JB, Gans DJ: The beneficial effect of angiotensin-converting enzyme Inhibition with captopril on diabetic nephropathy in normotensive IDDM patients with microalbuminuria. Am J Med 1995, 99:497-504. This study was a prospective, randomized, double-blind, placebo-controlled trial of captopril, 50 mg, versus placebo twice daily in 143 IDDM patients with persistent microalbuminuria. A significantly lower rate of progression of microalbuminuria to clinical proteinuria, reduced urinary albumin excretion, and a preserved creatinine clearance rate were observed in the captopril-treated group.
37. Mathiesen ER, Hommel E, Smidt UM, Parving H-H: Efficacy of captopril in normotensive diabetic patients with microalbuminuria: 8 years follow-up [abstract]. Diabetologia 1995, 38:452. This prospective randomized study demonstrated for the first time that the beneficial effect of ACE inhibition in postponing the development of diabetic nephropathy is long-lasting (8 years) in normotensive IDDM patients with persistent microalbuminuria.
38. Ravid M, Savin H, Jutrin I, Bental T, Katz B, Lishner M: 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.
39. Ravid M, Lang R, Rachman R, Lishner M: Long-term renoprotective effect of angiotensin-converting enzyme inhibition in non-insulin-dependent diabetes mellitus. Arch Intern Med 1996, 156:286-289.
40. Sano T, Kawamura T, Matsumae H, Sasaki H, Nakayama M, Hara T, Matsuo S, Hotta N, Sakamoto N: Effects of long-term enalapril treatment on persistent microalbuminuria in well-controlled hypertensive and normotensive NIDDM patients. Diabetes Care 1994, 7:420-424.
41. Borch-Johnsen K, Wenzel H, Viberti GC, Mogensen CE: Is screening and intervention for microalbuminuria worthwhile in patients with insulin dependent diabetes. BMJ 1993, 306:1722-1725.
42. Kiberd BA, Jindal KK: Screening to prevent renal failure in insulin dependent diabetic patients: an economic evaluation. BMJ 1995, 311:1595-1599. An economic analysis of the value of screening for microalbuminuria to prevent renal failure in IDDM patients.
43. Mogensen CE, Keane WF, Bennett PH, Jerums G, Parving H-H, Passa P, Steffes MW, Striker GE, Viberti GC: Prevention of diabetic renal disease with special reference to microalbuminuria. Lancet 1995, 346:1080-1084. A comprehensive review, suggesting a unifying global strategy for the detection, prevention, and treatment of diabetic nephropathy.
44. Björck S, Mulec H, Johnsen SA, Nordén G, Aurell M: Renal protective effect of enalapril in diabetic nephropathy. BMJ 1992, 304:339-343.
45. Parving H-H, Andersen AR, Smidt UM, Hommel E, Mathiesen ER, Svendsen PA: Effect of antihypertensive treatment on kidney function in diabetic nephropathy. BMJ 1987, 294:1443-1447.
46. Lebovitz HE, Wiegmann TB, Cnaan A, Shahinfar S, Sica D, Broadstone V, Schwartz SL, Mengel MC, Segal R, Versaggi JA, Bolten WK: Renal protective effects of enalapril in hypertensive NIDDM: role of baseline albuminuria. Kidney Int 1994, 45(suppl 4):150-155.
47. Klahr S, Levey AS, Beck GJ, Caggiula AW, Hunsicker L, Kusek JW, Striker G, for the Modification Of Diet In Renal Disease Study Group: The effects of dietary protein restriction and blood-pressure control on the progression of chronic renal disease. N Engl J Med 1994, 330:877-884.
48. Hansen HP, Rossing P, Tarnow L, Nielsen FS, Jensen BR, Parving H-H: Increased glomerular filtration rate after withdrawal of long term anti-hypertensive treatment in diabetic nephropathy. Kidney Int 1995, 47:1726-1731. This study provides support for the hypothesis that the initially faster decline that is observed in GFR is due to a functional (hemodynamic) effect of ACE inhibition that does not attenuate over time, whereas the subsequent slower decline reflects the beneficial effect on progression of diabetic nephropathy.
49. Apperloo AJ, de Zeeuw D, van Essen G, de Jong PE: The initial GFR decline on antihypertensive treatment in long-term intervention studies is reversible after withdrawal of treatment [abstract]. J Am Soc Nephrol 1994, 5:324.
50. Watkins PJ, Blainey JD, Brewer DB, Fitzgerald MG, Malins JM, O'Sullivan DJ, Pinto J: The natural history of diabetic renal disease: a follow-up study of series of renal biopsies. Q J Med 1972, 41:437-456.
51. Rossing P, Hommel E, Smidt UM, Parving H-H: Impact of arterial blood pressure and albuminuria on the progression of diabetic nephropathy in IDDM patients. Diabetes 1993, 42:715-719.
52. Williams PS, Foss G, Bone JM: Renal pathology and proteinuria determine progression in untreated mild/moderate chronic renal failure. Q J Med 1988, 252:343-354.
53. Brenner BM: Hemodynamically mediated glomerular injury and the progressive nature of kidney disease. Kidney Int 1983, 23:647-655.
54. Anderson S, Rennke HG, Garcia DL, Brenner BM: Short and long term effects of antihypertensive therapy in the diabetic rat. Kidney Int 1989, 36:526-536.
55. Mogensen CE: Long-term antihypertensive treatment inhibiting progression of diabetic nephropathy. BMJ 1982, 285:685-688.
56. Parving H-H, Hommel E, Smidt UM: Protection of kidney function and decrease in albuminuria by captopril in insulin dependent diabetics with nephropathy. BMJ 1988, 297:1086-1091.
57. Walker JD, Bending JJ, Dodds RA, Mattock MB, Murrells TJ, Keen H, Viberti GC: Restriction of dietary protein and progression of renal failure in diabetic nephropathy. Lancet 1989, ii:1411-1415.
58. Rossing P, Hommel E, Smidt UM, Parving H-H: Reduction in albuminuria predicts a beneficial effect on diminishing the progression of human diabetic nephropathy during antihypertensive treatment. Diabetologia 1994, 37:511-516.
59. Apperloo AJ, de Zeeuw D, de Jong PE: Short-term antiproteinuric response to antihypertensive treatment predicts long-term GFR decline in patients with non-diabetic renal disease. Kidney Int 1994, 45(suppl 4):174-178.
60. Kasiske BL, Kalil R, Ma JZ, Liao M, Keane WF: Effect of antihypertensive therapy on the kidney in patients with diabetes: a meta-regression analysis. Ann Intern Med 1993, 118:129-138.
61. de Courten M, Böhlen L, Weidmann P: Comparative study of the effect of ACE-inhibitors and other antihypertensive agents on proteinuria in diabetic patients. In The Kidney and Hypertension in Diabetes Mellitus. Edited by Mogensen CE. Boston: Kluwer Academic Publishers; 1994:319-332.
62. Lewis E, Hunsicker L, Bain R, Rhode R: The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. N Engl J Med 1993, 329:1456-1462.
63. Krämer BK, Ritz E: Is inhibition of the angiotensin-converting enzyme the treatment of choice in diabetic nephropathy? J Nephrol 1994, 7:268-270.
64. Bauer JH: Are angiotensin-converting enzyme inhibitors the renal protective antihypertensive drugs of choice? Curr Opin Nephrol Hypertens 1995, 4:427-431. A critical review of ACE inhibition versus non-ACE inhibition in NIDDM and IDDM patients with elevated urinary albumin excretion rates.
65. Hommel E, Jensen B, Parving H-H: Long term effect of captopril on kidney function in normotensive insulin dependent diabetic patients (IDDM) with diabetic nephropathy [abstract]. J Am Soc Nephrol 1995, 6:450.
66. Parving H-H, Rossing P: The use of antihypertensive agents in prevention and treatment of diabetic nephropathy. Curr Opin Nephrol Hypertens 1994, 3:292-300.
67. Nielsen FS, Rossing P, Gall M-A, Skøtt P, Smidt UM, Parving H-H: Impact of lisinopril and atenolol on kidney function in hypertensive NIDDM subjects with diabetic nephropathy. Diabetes 1994, 43:1108-1113.
68. Bakris GL, Copley JB, Vicknair N, Leugans S: Effect of nondihydropyridine calcium antagonists (NDCAs) on progression of nephropathy from non-insulin dependent diabetes (NIDDM): a five year follow-up study [abstract]. J Am Soc Nephrol 1995, 6:446. Open, randomized, 5-year follow-up study in proteinuric NIDDM patients comparing use of ACE inhibition, calcium antagonists, and sympatholytic drugs.
69. Parving H-H, Rossing P, Hommel E, Smidt UM: Angiotensin converting enzyme inhibition in diabetic nephropathy: ten years experience. Am J Kidney Dis 1995, 26:99-107. Ten-year prospective study of putative progression promoters, kidney function, and prognosis during ACE inhibition in IDDM patients with diabetic nephropathy.
70. Jacobsen P, Tarnow L, Rossing P, Cambien F, Lecerf L, Poirier O, Parving H-H: The insertion/deletion (I/D) polymorphism in the angiotensin I-converting enzyme (ACE) gene predicts the progression of diabetic nephropathy during ACE inhibition (ACEI) in insulin dependent diabetic (IDDM) patients [abstract]. J Am Soc Nephrol 1995, 6:450. An observational follow-up study of IDDM patients with nephropathy treated with ACE inhibition for 7 years (range, 3 to 9 years). The study suggests that the deletion polymorphism in the ACE gene reduces the long-term beneficial effect of ACE inhibition on progression of diabetic nephropathy.
71. Yoshida H, Hamaguchi A, Mitarai T, Kuriyama S, Kawamura T, Tomonari H, Eto T, Kubo H, Kawaguchi Y, Matsuoka K, Atsumi Y, Ichikawa I, Sakai O: Accelerated progression to renal failure in NIDDM patients with the deletion polymorphism of the angiotensin converting enzyme (ACE) gene [abstract]. J Am Soc Nephrol 1995, 6:409. The authors showed an accelerated progression to renal failure in proteinuric NIDDM patients with the deletion polymorphism of the ACE gene.
72. Knowles HCJ: Long term juvenile diabetes treated with unmeasured diet. Trans Assoc Am Physicians 1971, 84:95-101.
73. Andersen AR, Christiansen JS, Andersen JK, Kreiner S, Deckert T: Diabetic nephropathy in type 1 (insulin-dependent) diabetes: an epidemiological study. Diabetologia 1983, 25:496-501.
74. Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR: The changing natural history of nephropathy in type 1 diabetes. Am J Med 1985, 78:785-794.
75. Parving H-H, Hommel E: Prognosis in diabetic nephropathy. BMJ 1989, 299:230-233.