Progressive renal decline as the major feature of diabetic nephropathy in type 1 diabetes

Clinical and Experimental Nephrology

Volumn 18, Issue 4, 2014, Pages 571-583

  Krolewski, Andrzej S ^a,b   Gohda, Tomohito ^a,b,c   Niewczas, Monika A ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Kidney complications; Progressive renal decline; Proteinuria; Type 1 diabetes

Indexed keywords

ALBUMIN;

CLINICAL EFFECTIVENESS; CLINICAL FEATURE; DIABETIC NEPHROPATHY; DISEASE COURSE; EARLY DIAGNOSIS; END STAGE RENAL DISEASE; GLOMERULUS FILTRATION RATE; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY DYSFUNCTION; MICROALBUMINURIA; PROTEIN URINE LEVEL; PROTEINURIA; REVIEW; ANIMAL; BIOLOGICAL MODEL; COMPLICATION; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; KIDNEY; KIDNEY FAILURE, CHRONIC; PATHOPHYSIOLOGY; PREDICTIVE VALUE; PROGNOSIS; RISK ASSESSMENT; RISK FACTOR;

ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; HUMANS; KIDNEY; KIDNEY FAILURE, CHRONIC; MODELS, BIOLOGICAL; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROTEINURIA; RISK ASSESSMENT; RISK FACTORS;

EID: 84906937762     PISSN: 13421751     EISSN: 14377799     Source Type: Journal    
DOI: 10.1007/s10157-013-0900-y     Document Type: Review

References (59)

1. Rosolowsky ET, Skupien J, Smiles AM, Niewczas MA, Roshan B, Stanton R, Eckfeldt JH, Warram JH, Krolewski AS. Risk of ESRD in type 1 diabetes remains high in spite of renoprotection. J Am Soc Nephrol. 2011;22(3):545-53.
2. Bright R. Cases and observations illustrative of renal disease accompanied with the secretion of albuminous urine. Guy Hosp Rep. 1836;1:338-400.
3. Kimmelstiel P, Wilson C. Intercapillary lesions in the glomeruli of the kidney. Am J Pathol. 1936;12:83-96.
4. Miles DW, Mogensen CE, Gundersen HJG. Radioimmunoassay for urinary albumin using a single antibody. Scand J Clin Lab Invest. 1970;26:5-11.
5. Parving HH, Oxenbøll B, Svendsen PA, Christiansen JS, Andersen AR. Early detection of patients at risk of developing diabetic nephropathy. A longitudinal study of urinary albumin excretion. Acta Endocrinol (Copenh). 1982;100(4):550-5. (Pubitemid 12089232)
6. Viberti GC, Jarrett RJ, Keen H. Microalbuminuria as prediction of nephropathy in diabetics. Lancet. 1982;2(8298):611.
7. Mogensen CE, Christensen CK. Predicting diabetic nephropathy in insulin-dependent patients. N Engl J Med. 1984;311(2):89-93. (Pubitemid 14084080)
8. Parving HH, Mauer M, Ritz E. Diabetic nephropathy. In: Brenner BM, editor. The kidney. 7th ed. Philadelphia: Elsevier; 2004. p. 1777-818.
9. Caramori ML, Fioretto P, Mauer M. The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient? Diabetes. 2000;49:1399-408.
10. Tabaei BP, Al-Kassab AS, Ilag LL, Zawacki CM, Herman WH. Does microalbuminuria predict diabetic nephropathy? Diabetes Care. 2001;24(9):1560-6. (Pubitemid 33716449)
11. Perkins BA, Ficociello LH, Silva KH, Finkelstein DM, Warram JH, Krolewski AS. Regression of microalbuminuria in type 1 diabetes. N Engl J Med. 2003;348(23):2285-93. (Pubitemid 36638102)
12. Giorgino F, Laviola L, Cavallo Perin P, Solnica B, Fuller J, Chaturvedi N. Factors associated with progression to macroalbuminuria in microalbuminuric Type 1 diabetic patients: the EURODIAB Prospective Complications Study. Diabetologia. 2004;47(6):1020-8. (Pubitemid 38918161)
13. de Boer IH, Rue TC, Cleary PA, Lachin JM, Molitch ME, Steffes MW, Sun W, Zinman B, Brunzell JD, DCCT/EDIC Research Group. Long-term renal outcomes of patients with type 1 diabetes mellitus and microalbuminuria: an analysis of the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications cohort. Arch Intern Med. 2011;171(5):412-20.
14. Forsblom CM, Groop PH, Ekstrand A, Groop LC. Predictive value of microalbuminuria in patients with insulin-dependent diabetes of long duration. BMJ. 1992;305(6861):1051-3.
15. Rudberg S, Persson B, Dahlquist G. Increased glomerular filtration rate as a predictor of diabetic nephropathy-an 8-year prospective study. Kidney Int. 1992;41(4):822-8.
16. Ficociello L, Perkins BA, Silva KH, Finkelstein DM, Ignatowska-Switalska H, Gaciong Z, Cupples LA, Aschengrau A, Warram JH, Krolewski AS. Progression from microalbuminuria to proteinuria in individuals with type 1 diabetes treated with angiotensin converting enzyme inhibitors. Clin J Am Soc Nephrol. 2007;2(3):461-9.
17. Mathiesen ER, Hommel E, Giese J, Parving HH. Efficacy of captopril in postponing nephropathy in normotensive insulin dependent diabetic patients with microalbuminuria. BMJ. 1991;303(6794):81-7.
18. Viberti G, Mogensen CE, Groop LC, Pauls JF. 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(4):275-9. (Pubitemid 24030753)
19. Laffel LM, McGill JB, Gans DJ. The beneficial effect of angiotensin-converting enzyme inhibition with captopril on diabetic nephropathy in normotensive IDDM patients with microalbuminuria. North American Microalbuminuria Study Group. Am J Med. 1995;99(5):497-504.
20. Randomised placebo-controlled trial of lisinopril in normotensive patients with insulin-dependent diabetes and normoalbuminuria or microalbuminuria. The EUCLID Study Group. Lancet. 1997;349(9068):1787-92.
21. O'Hare P, Bilbous R, Mitchell T, O' Callaghan CJ, Viberti GC, Ace-Inhibitor Trial to Lower Albuminuria in Normotensive Insulin-Dependent Subjects Study Group. Low-dose ramipril reduces microalbuminuria in type 1 diabetic patients without hypertension: results of a randomized controlled trial. Diabetes Care. 2000;23(12):1823-9.
22. Crepaldi G, Carta Q, Deferrari G, Mangili R, Navalesi R, Santeusanio F, Spalluto A, Vanasia A, Villa GM, Nosadini R. 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(1):104-10. (Pubitemid 28030395)
23. Bojestig M, Karlberg BE, Lindström T, Nystrom FH. Reduction of ACE activity is insufficient to decrease microalbuminuria in normotensive patients with type 1 diabetes. Diabetes Care. 2001;24(5):919-24. (Pubitemid 33636070)
24. Tsalamandris C, Allen TJ, Gilbert RE, Sinha A, Panagiotopoulos S, Cooper MF, Jerums G. Progressive decline in renal function in diabetic patients with and without albuminuria. Diabetes. 1994;43:649-55. (Pubitemid 24138777)
25. Retnakaran R, Cull CA, Thorne KI, Adler AI, Holman RR, UKPDS Study Group. Risk factors for renal dysfunction in type 2 diabetes. U.K. Prospective Diabetes Study 74. Diabetes. 2006;55:1832-9. (Pubitemid 44324140)
26. Perkins BA, Ficociello LH, Roshan B, Warram JH, Krolewski AS. In patients with Type 1 diabetes and new onset microalbuminuria the development of advanced chronic kidney disease may not require progression to proteinuria. Kidney Int. 2010;77:57-64.
27. Krolewski AS, Niewczas MA, Skupien J, Gohda T, Smiles A, Eckfeldt JH, Doria A, Warram JH. Early progressive renal decline precedes the onset of microalbuminuria and its progression to macroalbuminuria. Diabetes Care. 2013 (Epub ahead of print).
28. Merchant ML, Perkins BA, Boratyn GM, Ficociello LH, Wilkey DW, Barati MT, Bertram CC, Page GP, Rovin BH, Warram JH, Krolewski AS, Klein JB. Urinary peptidome may predict renal function decline in type 1 diabetes and microalbuminuria. J Am Soc Nephrol. 2009;20(9):2065-74.
29. Skupien J, Warram JH, Smiles AM, Niewczas MA, Gohda G, Pezzolesi MG, Cantarovich D, Stanton R, Krolewski AS. Early renal function decline predicts risk of ESRD: 5-18 year follow-up of patients with type 1 diabetes and proteinuria. Kidney Int. 2012;82(5):589-97.
30. Krolewski M, Eggers PW, Warram JH. Magnitude of end-stage renal disease in IDDM: a 35 year follow-up study. Kidney Int. 1996;50(6):2041-6. (Pubitemid 26417548)
31. Yu MA, Sánchez-Lozada LG, Johnson RJ, Kang DH. Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid-induced endothelial dysfunction. J Hypertens. 2010;28(6):1234-42.
32. Mazzali M, Kanellis J, Han L, Feng L, Xia YY, Chen Q, Kang DH, Gordon KL, Watanabe S, Nakagawa T, Lan HY, Johnson RJ. Hyperuricemia induces a primary renal arteriolopathy in rats by a blood pressure-independent mechanism. Am J Physiol Renal Physiol. 2002;282(6):F991-7. (Pubitemid 34654464)
33. Talbott JH, Terplan KL. The kidney in gout. Medicine. 1960;39:405-67.
34. Siu YP, Leung KT, Tong MK, Kwan TH. Use of allopurinol in slowing the progression of renal disease through its ability to lower serum uric acid level. Am J Kidney Dis. 2006;47:51-9. (Pubitemid 41828266)
35. Doria A, Niewczas M, Fiorina P. Can existing drugs approved for other indications retard renal function decline in patients with Type 1 diabetes and nephropathy. Semin Nephrol. 2012;32(5):437-44.
36. Gohda T, Niewczas MA, Ficociello LH, Walker WH, Skupien J, Rosetti F, Cullere X, Johnson AC, Crabtree G, Smiles AM, Mayadas TN, Warram JH, Krolewski AS. Circulating TNF receptors 1 and 2 predict stage 3 of CKD in Type 1 diabetes. J Am Soc Nephrol. 2012;23(3):516-24.
37. Niewczas MA, Gohda T, Skupien J, Smiles AM, Walker WH, Rosetti F, Cullere X, Eckfeldt JH, Doria A, Mayadas TN, Warram JH, Krolewski AS. Circulating TNF receptors 1 and 2 predict ESRD in type 2 diabetes. J Am Soc Nephrol. 2012;23(3):507-15.
38. Mauer SM, Steffes MW, Ellis EN, Sutherland DE, Brown DM, Goetz FC. Structural-functional relationships in diabetic nephropathy. J Clin Invest. 1984;74:1143-55. (Pubitemid 15210185)
39. Gilbert RE, Cooper ME. The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney Int. 1999;56:1627-37. (Pubitemid 29518163)
40. Bohle A, Wehrmann M, Bogenschutz O, Batz C, Muller CA, Muller GA. The pathogenesis of chronic renal failure in diabetic nephropathy. Investigation of 488 cases of diabetic glomerulosclerosis. Pathol Res Pract. 1991;187:251-9.
41. Suzuki D, Miyazaki M, Naka R, Koji T, Yagame M, Jinde K, Endoh M, Nomoto Y, Sakai H. In situ hybridization of interleukin 6 in diabetic nephropathy. Diabetes. 1995;44:1233-8.
42. Wada T, Furuichi K, Sakai N, Iwata Y, Yoshimoto K, Shimizu M, Takeda SI, Takasawa K, Yoshimura M, Kida H, Kobayashi KI, Mukaida N, Naito T, Matsushima K, Yokoyama H. Up-regulation of monocyte chemoattractant protein-1 in tubulointerstitial lesions of human diabetic nephropathy. Kidney Int. 2000;58:1492-9.
43. Schmid H, Boucherot A, Yasuda Y, Henger A, Brunner B, Eichinger F, Nitsche A, Kiss E, Bleich M, Grone HJ, Nelson PJ, Schlondorff D, Cohen CD, Kretzler M, European Renal cDNA Bank (ERCB) Consortium. Modular activation of nuclear factor-kappaB transcriptional programs in human diabetic nephropathy. Diabetes. 2006;55:2993-3003. (Pubitemid 44923635)
44. Morcos M, Sayed AA, Bierhaus A, Yard B, Waldherr R, Merz W, Kloeting I, Schleicher E, Mentz S, Abd el Baki RF, Tritschler H, Kasper M, Schwenger V, Hamann A, Dugi KA, Schmidt AM, Stern D, Ziegler R, Haering HU, Andrassy M, van der Woude F, Nawroth PP. Activation of tubular epithelial cells in diabetic nephropathy. Diabetes. 2002;51:3532-44. (Pubitemid 35403461)
45. Wolkow PP, Niewczas MA, Perkins B, Ficociello LH, Lipinski B, Warram JH, Krolewski AS. Association of urinary inflammatory markers and renal decline in microalbuminuric type 1 diabetics. J Am Soc Nephrol. 2008;19:789-97.
46. Segerer S, Nelson PJ, Schlondorff D. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol. 2000;11:152-76. (Pubitemid 30020438)
47. Rodriguez-Iturbe B, Pons H, Herrera-Acosta J, Johnson RJ. Role of immunocompetent cells in nonimmune renal diseases. Kidney Int. 2001;59:1626-40. (Pubitemid 32336778)
48. Anders HJ, Vielhauer V, Schlondorff D. Chemokines and chemokine receptors are involved in the resolution or progression of renal disease. Kidney Int. 2003;63:401-15. (Pubitemid 36126787)
49. Grgic I, Campanholle G, Bijol V, Wang C, Sabbisetti VS, Ichimura T, Humphreys BD, Bonventre JV. Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int. 2012;82:172-83.
50. Wanic K, Krolewski B, Ju W, Placha G, Niewczas MA, Walker W, Warram JH, Kretzler M, Krolewski AS. Transcriptome analysis of proximal tubular cells (HK-2) exposed to urines of type 1 diabetes patients at risk of early progressive renal function decline. PLoS ONE. 2013;8(3):e57751.
51. Woroniecka KI, Park AS, Mohtat D, Thomas DB, Pullman JM, Susztak K. Transcriptome analysis of human diabetic kidney disease. Diabetes. 2011;60:2354-69.
52. Krolewski AS, Warram JH, Forsblom C, Smiles A, Thorn L, Skupien J, Harjutsalo V, Stanton R, Eckfeldt JH, Inker LA, Groop PH. Serum concentration of cystatin C and risk of ESRD in diabetes. Diabetes Care. 2012;35(11):2311-6.
53. Krolewski AS, Bonventre JV. High risk of ESRD in type 1 diabetes: new strategies are needed to retard progressive renal function decline. Semin Nephrol. 2012;32(5):407-14.
54. Degome EM, Rivera G, Lilly SM, Usman MH, Mohler ER. Personalized vascular medicine; individualizing drug therapy. Vasc Med. 2011;16(5):391-404.
55. Chokrungvaranon N, Deer J, Reaven PD. Intensive glycemic control and cardiovascular disease; are there patients who may benefit? Postgrad Med. 2011;123(6):114-23.
56. Higgins MJ, Baselga J. Targeted therapies for breast cancer. J Clin Invest. 2011;121(10):3797-803.
57. Cantarovich D, Perrone V. Pancreas transplant as treatment to arrest renal function decline in patients with type 1 diabetes and proteinuria. Semin Nephrol. 2012;32(5):432-6.
58. Pavlakis M, Kher A. Pre-emptive kidney transplantation to improve survival in patients with Type 1 diabetes and imminent risk of ESRD. Semin Nephrol. 2012;32(5):505-11.
59. Gilbert RE, Zhang Y, Yuen DA. Cell therapy for diabetic nephropathy: is the future, now? Semin Nephrol. 2012;32(5):486-93.