The American Journal of Medicine
Volume 122, Issue 1 , Pages 62-72 , January 2009

The Natural Course of Microalbuminuria among African Americans with Type 2 Diabetes: A 3-Year Study

Data related to this manuscript were presented during the International Congress of Nephrology at Rio de Janeiro, Brazil in April 2007.

  • Mohamed G. Atta, MD, MPH

      Affiliations

    • Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Md
    • Corresponding Author InformationRequests for reprints should be addressed to Mohamed G. Atta, MD, MPH, 1830 E. Monument Street, Suite 416, Baltimore, MD 21287
  • ,
  • Kesha Baptiste-Roberts, PhD, MPH

      Affiliations

    • Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Md
  • ,
  • Frederick L. Brancati, MD, MHS

      Affiliations

    • Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Md
    • Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Md
  • ,
  • Tiffany L. Gary, PhD

      Affiliations

    • Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Md
    • Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Md

References 

  1. Rostand SG, Kirk KA, Rutsky EA, Pate BA. Racial differences in the incidence of treatment for end-stage renal disease. N Engl J Med. 1982;306(21):1276–1279
  2. Klag MJ, Whelton PK, Randall BL, et al. End-stage renal disease in African-American and white men (16-year MRFIT findings). JAMA. 1997;277(16):1293–1298
  3. U.S. Renal Data System. USRDS 2007 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. Available at: http://www.usrds.org. Accessed February 6, 2008.
  4. Brancati FL, Whelton PK, Randall BL, et al. Risk of end-stage renal disease in diabetes mellitus: a prospective cohort study of men screened for MRFIT (Multiple Risk Factor Intervention Trial). JAMA. 1997;278(23):2069–2074
  5. Finne P, Reunanen A, Stenman S, et al. Incidence of end-stage renal disease in patients with type 1 diabetes. JAMA. 2005;294(14):1782–1787
  6. Krakoff J, Lindsay RS, Looker HC, et al. Incidence of retinopathy and nephropathy in youth-onset compared with adult-onset type 2 diabetes. Diabetes Care. 2003;26(1):76–81
  7. Burrows NR, Narva AS, Geiss LS, et al. End-stage renal disease due to diabetes among southwestern American Indians, 1990-2001. Diabetes Care. 2005;28(5):1041–1044
  8. Pavkov ME, Bennett PH, Knowler WC, et al. Effect of youth-onset type 2 diabetes mellitus on incidence of end-stage renal disease and mortality in young and middle-aged Pima Indians. JAMA. 2006;296(4):421–426
  9. Viberti GC, Jarrett RJ, Mahmud U, et al. Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus. Lancet. 1982;319(8287):1430–1432
  10. Parving HH, Oxenboll B, Svendsen PA, et al. Early detection of patients at risk of developing diabetic nephropathy (A longitudinal study of urinary albumin excretion). Acta Endocrinologica (Copenh). 1982;100(4):550–555
  11. Mogensen CE. Microalbuminuria predicts clinical proteinuria and early mortality in maturity-onset diabetes. N Engl J Med. 1984;310(6):356–360
  12. Gall MA, Borch-Johnsen K, Hougaard P, et al. Albuminuria and poor glycemic control predict mortality in NIDDM. Diabetes. 1995;44(11):1303–1309
  13. Miettinen H, Haffner SM, Lehto S, et al. Proteinuria predicts stroke and other atherosclerotic vascular disease events in nondiabetic and non-insulin-dependent diabetic subjects. Stroke. 1996;27(11):2033–2039
  14. Rossing P, Hougaard P, Borch-Johnsen K, Parving H-H. Predictors of mortality in insulin dependent diabetes: 10-year observational follow-up study. BMJ. 1996;313(7060):779–784
  15. Mattock MB, Barnes DJ, Viberti G, et al. Microalbuminuria and coronary heart disease in NIDDM: an incidence study. Diabetes. 1998;47(11):1786–1792
  16. Borch-Johnsen K, Feldt-Rasmussen B, Strandgaard S, et al. Urinary albumin excretion (An independent predictor of ischemic heart disease). Arterioscler Thromb Vasc Biol. 1999;19(8):1992–1997
  17. Gerstein HC, Mann JFE, Yi Q, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286(4):421–426
  18. Mogensen CE. Microalbuminuria and hypertension with focus on type 1 and type 2 diabetes. J Intern Med. 2003;254(1):45–66
  19. Mogensen CE, Poulsen PL. Microalbuminuria, glycemic control, and blood pressure predicting outcome in diabetes type 1 and type 2. Kidney Int Suppl. 2004;66(S92):S40–S41
  20. 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(1):32–35
  21. de Zeeuw D, Parving HH, Henning RH. Microalbuminuria as an early marker for cardiovascular disease. J Am Soc Nephrol. 2006;17(8):2100–2105
  22. Parving HH, Lewis JB, Ravid M, et al. Prevalence and risk factors for microalbuminuria in a referred cohort of type II diabetic patients: a global perspective. Kidney Int. 2006;69(11):2057–2063
  23. Dasmahapatra A, Bale A, Raghuwanshi MP, et al. Incipient and overt diabetic nephropathy in African Americans with NIDDM. Diabetes Care. 1994;17(4):297–304
  24. Goldschmid MG, Domin WS, Ziemer DC, et al. Diabetes in urban African-Americans (II. High prevalence of microalbuminuria and nephropathy in African-Americans with diabetes). Diabetes Care. 1995;18(7):955–961
  25. 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):2285–2293
  26. Gary TL, Bone LR, Hill MN, et al. Randomized controlled trial of the effects of nurse case manager and community health worker interventions on risk factors for diabetes-related complications in urban African Americans. Prev Med. 2003;37(1):23–32
  27. Gaede P, Vedel P, Larsen N, et al. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med. 2003;348(5):383–393
  28. Levey AS, Greene T, Kusek JW, Beck G MDRD Study Group. A simplified equation to predict glomerular filtration rate from serum creatinine (abstract). J Am Soc Nephrol. 2000;11:155A
  29. Olsen S, Mogensen CE. How often is NIDDM complicated with non-diabetic renal disease? (An analysis of renal biopsies and the literature). Diabetologia. 1996;39(12):1638–1645
  30. Warram JH, Gearin G, Laffel L, Krolewski AS. Effect of duration of type I diabetes on the prevalence of stages of diabetic nephropathy defined by urinary albumin/creatinine ratio. J Am Soc Nephrol. 1996;7(6):930–937
  31. Fioretto P, Mauer M, Brocco E, et al. Patterns of renal injury in NIDDM patients with microalbuminuria. Diabetologia. 1996;39(12):1569–1576
  32. Cowie CC, Port FK, Wolfe RA, et al. Disparities in incidence of diabetic end-stage renal disease according to race and type of diabetes. N Engl J Med. 1989;321(16):1074–1079
  33. Freedman BI, Tuttle AB, Spray BJ. Familial predisposition to nephropathy in African-Americans with non-insulin-dependent diabetes mellitus. Am J Kidney Dis. 1995;25(5):710–713
  34. Seaquist ER, Goetz FC, Rich S, Barbosa J. Familial clustering of diabetic kidney disease (Evidence for genetic susceptibility to diabetic nephropathy). N Engl J Med. 1989;320(18):1161–1165
  35. Quinn M, Angelico MC, Warram JH, Krolewski AS. Familial factors determine the development of diabetic nephropathy in patients with IDDM. Diabetologia. 1996;39(8):940–945
  36. Doria A, Lee J, Warram JH, Krolewski AS. Diabetes susceptibility at IDDM2 cannot be positively mapped to the VNTR locus of the insulin gene. Diabetologia. 1996;39(5):594–599
  37. Clustering of long-term complications in families with diabetes in the diabetes control and complications trial (The Diabetes Control and Complications Trial Research Group). Diabetes. 1997;46(11):1829–1839
  38. Patrick AW, Leslie PJ, Clarke BF, Frier BM. The natural history and associations of microalbuminuria in type 2 diabetes during the first year after diagnosis. Diabet Med. 1990;7(10):902–908
  39. Remuzzi G, Bertani T. Is glomerulosclerosis a consequence of altered glomerular permeability to macromolecules?. Kidney Int. 1990;38(3):384–394
  40. Rossing P, Hommel E, Smidt UM, Parving HH. Impact of arterial blood pressure and albuminuria on the progression of diabetic nephropathy in IDDM patients. Diabetes. 1993;42(5):715–719
  41. Stehouwer CA, Zeldenrust GC, den Ottolander GH, et al. Urinary albumin excretion, cardiovascular disease, and endothelial dysfunction in non-insulin-dependent diabetes mellitus. Lancet. 1992;340(8815):319–323
  42. Yusuf S, Sleight P, Pogue J, et al. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients (The Heart Outcomes Prevention Evaluation Study Investigators). N Engl J Med. 2000;342(3):145–153
  43. Romundstad S, Holmen J, Hallan H, et al. Microalbuminuria and all-cause mortality in treated hypertensive individuals: does sex matter?: the Nord-Trondelag Health Study (HUNT), Norway. Circulation. 2003;108(22):2783–2789
  44. Gaede P, Vedel P, Parving HH, Pedersen O. Intensified multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: the Steno type 2 randomised study. Lancet. 1999;353(9153):617–622
  45. Shichiri M, Kishikawa H, Ohkubo Y, Wake N. Long-term results of the Kumamoto Study on optimal diabetes control in type 2 diabetic patients. Diabetes Care. 2000;23(Suppl 2):B21–B29
  46. 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(12):870–878
  47. 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(12):861–869
  48. Crook ED, Harris J, Oliver B, et al. Endstage renal disease owing to diabetic nephropathy in Mississippi: an examination of factors influencing renal survival in a population prone to late referral. J Investig Med. 2001;49(3):284–291
  49. 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(8):577–581
  50. Schrier RW, Estacio RO, Esler A, Mehler P. Effects of aggressive blood pressure control in normotensive type 2 diabetic patients on albuminuria, retinopathy and strokes. Kidney Int. 2002;61(3):1086–1097
  51. Wang PH, Lau J, Chalmers TC. Meta-analysis of effects of intensive blood-glucose control on late complications of type I diabetes. Lancet. 1993;341(8856):1306–1309
  52. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993;329(14):977–986
  53. Breyer JA, Bain RP, Evans JK, et al. Predictors of the progression of renal insufficiency in patients with insulin-dependent diabetes and overt diabetic nephropathy (The Collaborative Study Group). Kidney Int. 1996;50(5):1651–1658
  54. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA. 2002;287(19):2563–2569
  55. Gall MA, Nielsen FS, Smidt UM, Parving HH. The course of kidney function in type 2 (non-insulin-dependent) diabetic patients with diabetic nephropathy. Diabetologia. 1993;36(10):1071–1078
  56. Ritz E, Stefanski A. Diabetic nephropathy in type II diabetes. Am J Kidney Dis. 1996;27(2):167–194
  57. Ballard DJ, Humphrey LL, Melton LJ, et al. Epidemiology of persistent proteinuria in type II diabetes mellitus (Population-based study in Rochester, Minnesota). Diabetes. 1988;37(4):405–412
  58. Klein R, Klein BE, Moss SE. Incidence of gross proteinuria in older-onset diabetes (A population-based perspective). Diabetes. 1993;42(3):381–389
  59. Lipton R, LaPorte RE, Becker DJ, et al. Cyclosporin therapy for prevention and cure of IDDM (Epidemiological perspective of benefits and risks). Diabetes Care. 1990;13(7):776–784
  60. Orchard TJ, Dorman JS, Maser RE, et al. Factors associated with avoidance of severe complications after 25 yr of IDDM (Pittsburgh Epidemiology of Diabetes Complications Study I). Diabetes Care. 1990;13(7):741–747
  61. Krolewski AS, Warram JH, Freire MB. Epidemiology of late diabetic complications (A basis for the development and evaluation of preventive programs). Endocrinol Metab Clin North Am. 1996;25(2):217–242
  62. Ruggenenti P, Fassi A, Ilieva AP, et al. Preventing microalbuminuria in type 2 diabetes. N Engl J Med. 2004;351(19):1941–1951

 Funding: The project was funded by grants from the National Institutes of Health (R01-DK48117 and R00052). Dr. Gary was funded by a grant from the NHLBI (K01-HL084700) and Dr. Brancati was funded by a grant from the NIDDK (K24-DK6222).

 Conflict of Interest: None.

 Authorship: All authors had access to the data and a role in writing the manuscript.

PII: S0002-9343(08)00850-4

doi: 10.1016/j.amjmed.2008.07.023

The American Journal of Medicine
Volume 122, Issue 1 , Pages 62-72 , January 2009