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ARTICLE |

The Natural History and Epidemiology of Diabetic Nephropathy: Title and subTitle BreakImplications for Prevention and Control FREE

Joseph V. Selby, MD; Stacey C. Fitz-Simmons, PhD; Jeffrey M. Newman, MD; Patricia P. Katz, PhD; Stephen Sepe, MPH; Jonathan Showstack, MPH
[+] Author Affiliations

Reprint requests to Division of Research, Kaiser Permanente Medical Care Program, 3451 Piedmont Ave, Oakland, CA 94611-5463 (Dr Selby).


JAMA. 1990;263(14):1954-1960. doi:10.1001/jama.1990.03440140080036
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Published online

PERSONS with diabetes are at increased risk for several types of kidney disease,1 but the predominant cause of end-stage renal disease (ESRD) in this disorder is diabetic nephropathy—a complication unique to diabetes. Since the initiation of Medicare coverage for treatment of ESRD in 1972, the proportion of new ESRD cases attributed to diabetic nephropathy has increased from approximately 10% in 19732 to 30% in 1987.3 Diabetes is now the single most frequent reason for beginning treatment of ESRD, with 10 025 new cases caused by diabetic nephropathy in 1987.3

In this article, we review the natural history and epidemiology of diabetic nephropathy and the evidence for efficacy of preventive and therapeutic measures. From this review, a strategy for preventing and controlling this important cause of morbidity is outlined.

NATURAL HISTORY OF DIABETIC KIDNEY DISEASE  Diabetic nephropathy is currently defined by the presence of a persistently positive

REFERENCES

Friedman EA.  Diabetic renal disease . In: Ellenberg M, Rifkin H, eds. Diabetes Mellitus: Theory and Practice . New York, NY: Medical Examination Publishing Co Inc; 1983;:759-776.
Sugimoto T, Rosansky SJ.  The incidence of treated end-stage renal disease in the eastern United States: 1973-1979 . Am J Public Health. 1984;; 74:14-17.
US Renal Data System. 1989 Annual Data Report . Bethesda, Md: National Institute of Diabetes and Digestive and Kidney Diseases; 1989;.
Mogensen CE, Christensen CK, Vittinghus E.  The stages in diabetic nephropathy: with emphasis on the stage of incipient diabetic nephropathy . Diabetes. 1983;;32( (suppl 2) ):64-78.
Mogensen CE.  Renal function changes in diabetes . Diabetes. 1976;;25( (suppl 2) ):872-879.
Osterby R, Gundersen HJG.  Glomerular size and structure in diabetes mellitus, I: early abnormalities . Diabetologia. 1975;;11:225-229.
Hirose K, Tsuchida H, Osterby R, Gundersen JHG.  A strong correlation between glomerular filtration rate and filtration surface in diabetic kidney hyperfunction . Lab Invest. 1980;;43:434-437.
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.
Anderson S, Brenner BM.  Influence of antihypertensive therapy on development and progression of diabetic glomerulopathy . Diabetes Care. 1988;;11:846-849.
Parving H-H, Noer I, Deckert T, et al.  The effect of metabolic regulation on microvascular permeability to small and large molecules in short-term juvenile diabetics . Diabetologia. 1976;;12:161-166.
Osterby R.  Early phases in the development of diabetic glomerulopathy: a quantitative electron microscopic study . Acta Med Scand Suppl. 1974;; ( (574) ):1-82.
Steffes MW, Ellis EN, Mauer SM.  Complications of diabetes mellitus and factors affecting their progression . Clin Chem. 1986;;32( (suppl B) ):B54-B61.
Mauer SM, Steffes MW, Goetz FC, Sutherland DER, Brown DM.  Diabetic nephropathy: a perspective . Diabetes. 1983;;32( (suppl 2) ):52-55.
Steffes MW, Osterby R, Chavers B, Mauer SM.  Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients . Diabetes. 1989;;38:1077-1081.
Ellis D, Becker DJ, Dameron D, Lobes L, Drash AL.  Proteinuria in children with insulindependent diabetes: relationship to duration of disease, metabolic control, and retinal changes . J Pediatr. 1983;;102:673-680.
Mathiesen ER, Saurbrey N, Hommel E, Parving H-H.  Prevalence of microalbuminuria in children with insulin-dependent diabetes . Acta Endocrinol Suppl (Copenh) . 1986;;275:14.
Niazy S, Feldt-Rasmussen B, Deckert T.  Microalbuminuria in insulin-dependent diabetes: prevalence and practical consequences . J Diabetic Complications. 1987;;1:76-80.
Damsgaard EM, Mogensen CE.  Microalbuminuria in elderly hyperglycemic patients and controls . Diabetic Med. 1986;;3:430-435.
Uusitupa M, Siitonen O, Penttila I, Antti A, Pyorala K.  Proteinuria in newly diagnosed type II diabetic patients . Diabetes Care. 1987;;10:191-194.
Parving H-H, Oxenboll B, Svendsen PA, Christensen JS, Andersen AR.  Early detection of patients at risk of developing diabetic nephropathy: a longitudinal study of urinary albumin excretion . Acta Endocrinol (Copenh) . 1982;;100:550-555.
Viberti GC, Hill RD, Jarrett RJ, Argyropoulous A, Mahmud U, Keen H.  Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus . Lancet. 1982;;1:1430-1432.
Mathiesen ER, Oxenboll B, Johansen K, Svendsen PAA, Deckert T.  Incipient nephropathy in type I (insulin-dependent) diabetes . Diabetologia. 1984;;26:406-410.
Mogensen CE, Christensen CK.  Predicting diabetic nephropathy in insulin-dependent patients . N Engl J Med. 1984;;311:89-93.
Bennett PH.  'Microalbuminuria' and diabetes: a critique—assessment of urinary albumin excretion and its role in screening for diabetic nephropathy . Am J Kidney Dis. 1989;;13:29-34.
Chavers BM, Bilous RW, Ellis EN, Steffes MW, Mauer SM.  Glomerular lesions and urinary albumin excretion in type I diabetes without overt proteinuria . N Engl J Med. 1989;;320:966-970.
Mogensen CE.  Microalbuminuria predicts clinical proteinuria and early mortality in maturityonset diabetes . N Engl J Med. 1984;;310:356-360.
Jarrett RJ, Viberti BC, Argyropoulous A, Hill RD, Mahmud U, Murrells TJ.  Microalbuminuria predicts mortality in non-insulin-dependent diabetes . Diabetic Med. 1984;;1:17-19.
Andersen AR, Christiansen JK, Andersen JK, Kreiner S, Deckert T.  Diabetic nephropathy in type I (insulin-dependent) diabetes: an epidemiological study . Diabetologia. 1983;;25:496-501.
Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR.  The changing natural history of nephropathy in type I diabetes . Am J Med. 1985;;78:785-794.
Parving H-H, Andersen AR, Smidt UM, Christensen JS, Oxenboll B, Svendsen PAA.  Diabetic nephropathy and arterial hypertension: the effect of antihypertensive treatment . Diabetes. 1983;;32( (suppl 2) ):83-87.
Deckert T, Poulsen JE, Larsen M.  Prognosis of diabetics with diabetes onset before the age of thirty-one, II: factors influencing the prognosis . Diabetologia . 1978;;14:371-377.
Hasslacher C, Stech W, Wahl P, Ritz E.  Blood pressure and metabolic control as risk factors for nephropathy in type I (insulin-dependent) diabetes . Diabetologia. 1985;;28:6-11.
Borch-Johnsen K, Andersen PK, Deckert T.  The effect of proteinuria on relative mortality in type I (insulin-dependent) diabetes mellitus . Diabetologia. 1985;;28:590-596.
Deckert T, Poulsen JE, Larsen M.  Prognosis of diabetics with diabetes onset before the age of thirty one, I: survival, causes of death, and complications . Diabetologia. 1978;;14:363-370.
Fabre J, Balant LP, Dayer PG, Fox HM, Vernet AT.  The kidney in maturity onset diabetes mellitus: a clinical study of 510 patients . Kidney Int. 1982;;21:730-738.
Ballard DJ, Humphrey LL, Melton LJ III, et al.  Epidemiology of persistent proteinuria in type II diabetes mellitus . Diabetes. 1988;;37:405-412.
Klein R, Klein BEK, Moss S, DeMets DL.  Proteinuria in diabetes . Arch Intern Med. 1988;; 148:181-186.
Kamenetzky SA, Bennett PH, Dippe SE, Miller M, LeCompte PM.  A clinical and histological study of diabetic nephropathy in the Pima Indians . Diabetes. 1974;;23:61-68.
Rate RG, Knowler WC, Morse HG, et al.  Diabetes mellitus in Hopi and Navajo Indians: prevalence of microvascular complications . Diabetes. 1983;;32:894-899.
Schmitz A, Gundersen HJG, Mogensen CE, et al.  Diabetic glomerulopathy in type II patients—is it different from type I? Acta Endocrinol Suppl (Copenh). 1986;;275:13.
Humphrey LL, Ballard DJ, Frohnert PP, Chu C-P, O'Fallon WM, Palumbo PJ.  Chronic renal failure in non-insulin-dependent diabetes mellitus: a population-based study in Rochester, Minnesota . Ann Intern Med. 1989;;111:788-796.
Kofoed-Enevoldson A, Borch-Johnson K, Kreiner S, Nerup J, Deckert T.  Declining incidence of persistent proteinuria in type I (insulin-dependent) diabetic patients in Denmark . Diabetes. 1987;;36:205-209.
Christensen JS, Gammelgaard J, Tronier B, Svenden PA, Parving H-H.  Kidney function and size in diabetics before and during initial insulin treatment . Kidney Int. 1982;;21:683-688.
Rasch R.  Prevention of diabetic glomerulopathy in streptozotocin diabetic rats by insulin treatment: the mesangial regions . Diabetologia. 1979;;17:243-248.
Mauer SM, Sutherland DER, Steffes MW, et al.  Pancreatic islet transplantation: effect on the glomerular lesions of experimental diabetes in the rat . Diabetes. 1974;;23:748-753.
Bilous RW, Mauer SM, Sutherland DER, Najarian JS, Goetz FC, Steffes MW.  The effects of pancreas transplantation on the glomerular structure of renal allografts in patients with insulindependent diabetes . N Engl J Med. 1989;;321:80-85.
The Kroc Collaborative Study Group.  Blood glucose control and the evolution of diabetic retinopathy and albuminuria: a preliminary multicenter trial . N Engl J Med. 1984;;311:365-372.
Feldt-Rasmussen B, Mathiesen ER, Deckert T.  Effect of two years of strict metabolic control on progression of incipient nephropathy in insulin-dependent diabetes . Lancet. 1986;;2:1300-1304.
Holman RR, Dornan TL, Mayon-White V, et al.  Prevention of deterioration of renal and sensorynerve function by more intensive management of insulin-dependent diabetic patients . Lancet. 1983;;1:204-208.
Dahl-Jorgensen K, Brinchmann-Hansen O, Hanssen KF, et al.  Effect of near normoglycaemia for two years on progression of early diabetic retinopathy, nephropathy, and neuropathy: The Oslo Study . Br Med J. 1986;;293:1195-1199.
The DCCT Research Group.  The Diabetes Control and Complications Trial (DCCT): design and methodologic considerations for the feasibility phase . Diabetes. 1986;;35:530-545.
The DCCT Research Group.  Are continuing studies of metabolic control of microvascular complications in insulin-dependent diabetes mellitus justified? N Engl J Med. 1988;;318:246-250.
Tamborlane WV, Puklin JE, Bergman M, et al.  Long-term improvement of metabolic control with the insulin pump does not reverse diabetic microangiopathy . Diabetes Care. 1982;;5:58-64.
Miller DG, Hampton L, Fredricka V, et al.  The use of an open-loop pump in type I diabetics with renal insufficiency . Diabetic Nephropathy. 1984;; 3:19-21.
Simonson DC.  Etiology and prevalence of hypertension in diabetic patients . Diabetes Care. 1988;;11:821-827.
Christlieb AR, Warram JH, Krolewski AS, et al.  Hypertension: the major risk factor in juvenileonset insulin-dependent diabetics . Diabetes. 1981;; 30( (suppl 2) ):90-96.
Jensen T, Borch-Johnsen K, Deckert T.  Changes in blood pressure and renal function in patients with type I (insulin-dependent) diabetes mellitus prior to clinical diabetes nephropathy . Diabetes Res. 1987;;4:159-162.
Mauer SM, Steffes MW, Azar S, Kupcho-Sandberg S, Brown DM.  The effects of Goldblatt hypertension on development of the glomerular lesions of diabetes mellitus in the rat . Diabetes. 1978;;27:738-744.
Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, Brenner BM.  Prevention of diabetic glomerulopathy by pharmacologic amelioration of glomerular capillary hypertension . J Clin Invest. 1986;;77:1925-1930.
Mathiesen ER, Ronn B, Jensen T, Storm B, Deckert T.  Relationship between blood pressure and urinary albumin excretion in development of micoralbuminuria . Diabetes. 1990;;39:345-349.
Viberti GC, Keen H. Wiseman MJ.  Raised arterial pressure in parents of proteinuric insulindependent diabetics . Br Med J. 1987;;295:515-517.
Krolewski AS, Canessa M, Warram JH, et al.  Predispostion to hypertension and susceptibility to renal disease in insulin-dependent diabetes mellitus . N Engl J Med. 1988;;318:140-145.
Krolewski AS.  The natural history of diabetic nephropathy in type I diabetes and the role of hypertension . Ann Intern Med. 1989;;110:795-798.
Knowler WC, Bennett PH, Nelson RG.  Prediabetic blood pressure predicts albuminuria after development of NIDDM . Diabetes. 1988;;37( (suppl 1) ):120a. Abstract.
Wiseman M, Viberti GC, Mackintosh D, Jarrett RF, Keen H.  Glycemia, arterial pressure and microalbuminuria in type 1 (insulin-dependent) diabetes mellitus . Diabetologia. 1984;;26:401-405.
Keen H, Chlouverakis C, Fuller JH, Jarrett RJ.  The concomitants of raised blood sugar: studies in newly detected hyperglycemics, II: urinary albumin excretion, blood pressure and their relation to blood sugar levels . Guy's Hosp Rep. 1969;;118:247-252.
Viberti GC, Bending JJ.  Early diabetic nephropathy . Adv Nephrol. 1988;;17:101-112.
Mimran A, Insua A, Ribstein J, Bringer J, Monnier L.  Comparative effect of captopril and nifedipine in normotensive patients with incipient diabetic nephropathy . Diabetes Care. 1988;;11:850-853.
Parving H-H, Smidt UM, Andersen AR, Svendsen PA.  Early aggressive antihypertensive treatment reduces rate of decline in kidney function in diabetic nephropathy . Lancet. 1983;;1:1175-1178.
Bjorck S, Nyberg G, Mulec H, Granerus G, Herlitz H, Aurell M.  Beneficial effects of angiotensin-converting enzyme inhibition on renal function in patients with diabetic nephropathy . Br Med J. 1986;;293:471-474.
Taguma AC, Kitamoto UY, Futaki G, et al.  Effect of captopril on heavy proteinuria in azotemic diabetes . N Engl J Med. 1985;;313:1617-1620.
The Working Group on Hypertension in Diabetes.  Statement on hypertension in diabetes mellitus . Arch Intern Med. 1987;;147:830-842.
The Working Group on Hypertension in Diabetes.  Statement on hypertension in diabetes mellitus . Arch Intern Med. 1987;;147:1165-1166.
Rosenstock J, Raskin P.  Early diabetic nephropathy: assessment and potential therapeutic interventions . Diabetes Care. 1986;;9:529-545.
Hawthorne V, Herman WH, eds.  International Symposium on Preventing the Kidney Disease of Diabetes Mellitus: public health perspectives . Am J Kidney Dis. 1989;;13:2-6.
Kaplan NM, Rosenstock J, Raskin P.  A differing view of treatment of hypertension in patients with diabetes mellitus . Arch Intern Med. 1987;;147: 1160-1162.
Keane WF, Anderson S, [ill]urell M, de Zeeuw D, Narins RG, Povar G.  Angiotension-converting enzyme inhibitors and progressive renal insufficiency . Ann Intern Med. 1989;;111:503-516.
Feig PU, Rutan GH.  Angiotension-converting enzyme inhibitors: the end of end-stage renal disease? Ann Intern Med. 1989;;111:451-452.
Hostetter TH, Meyer TW, Rennke HG, Brenner BM.  Chronic effects of dietary protein on renal structure and function in the rat with intact and reduced renal mass . Kidney Int. 1986;;30:509-517.
Don BR, Schambelan M.  Diabetes, dietary protein and glomerular hyperfiltration . West J Med. 1987;;147:449-455.
Wiseman MJ, Bogneth E, Dodds R, Keen H, Viberti GC.  Changes in renal function in response to protein restricted diet in type I diabetes . Diabetologia. 1987;;30:154-159.
Cohen DL, Dodds R, Viberti GC.  Reduction of microalbuminuria and glomerular filtration rate by dietary protein restriction in type I (insulin-dependent) diabetic patients: an effect independent of blood glucose control and arterial pressure changes . Diabetologia. 1986;;29:528a. Abstract.
Evanoff GV, Thompson CS, Brown J, Weinman EJ.  The effect of dietary protein restriction on the progression of diabetic nephropathy: a 12-month follow-up . Arch Intern Med. 1987;;147:492-495.
Bending JJ, Dodds RA, Keen H, Viberti GC.  Renal responses to restricted protein intake in diabetic nephropathy . Diabetes. 1988;;37:1641-1646.
American Diabetes Association.  Nutritional recommendations and principles for individuals with diabetes mellitus: 1986 . Diabetes Care . 1987;; 10:126-132.
Keane WF, Kasiske BL, O'Donnell MP.  Hyperlipidemia and the progression of renal disease . Am J Clin Nutr. 1988;;47:157-160.
Pettitt DJ, Saad MF.  Inheritance of predisposition to renal insufficiency in diabetic men . Diabetes. 1988;;37( (suppl 1) ):51A. Abstract.
Seaquist ER, Goetz FC, Rich S, Barbosa J.  Familial clustering of diabetic kidney disease . N Engl J Med. 1989;;320:1161-1165.
Barnett AH, Pyke DA.  The genetics of diabetic complications . Clin Endocrinol Metab. 1986;;15: 715-726.
Rettig BS, Teutsch SM.  The incidence of endstage renal disease in type I and type II diabetes mellitus . Diabetic Nephropathy. 1984;;3:26-27.
Kappel DF, Van Tuinen M.  Trends in the incidence of treated end-stage renal disease secondary to diabetic nephropathy: 1975-84 . Am J Kidney Dis. 1986;;8:234-238.
Cowie CC, Port FK, Wolfe RA, Savage PJ, Moll PP, Hawthorne VM.  Disparities in incidence of diabetic end-stage renal disease according to race and type of diabetes . N Engl J Med. 1989;;321:1074-1079.
Nelson RG, Pettitt DJ, Carraher MJ, Baird HR, Knowler WC.  Effect of proteinuria on mortality in NIDDM . Diabetes. 1988;;37:1499-1504.
Nelson RG, Newman JM, Knowler WC, et al.  Incidence of end-stage renal disease in type 2 diabetes mellitus in Pima Indians . Diabetologia. 1988;; 31:730-736.
Pugh JA, Stern MP, Zapata M.  Excess incidence of treatment of end-stage renal disease in Mexican-Americans . Am J Epidemiol . 1988;;127: 135-144.
Newman JM, Marfin AA, Eggers PW, Helgerson SD.  End-stage renal disease among Native Americans . Am J Public Health. 1990;;80:318-319.
Haffner SM, Mitchell BD, Pugh JA, et al.  Proteinuria in Mexican-Americans and non-Hispanic whites with NIDDM . Diabetes Care. 1989;;12:530-536.
Eggers PW, Connerton R, McMullan M.  The Medicare experience with end-stage renal disease . Health Care Financ Rev. 1984;;5:69-88.
Raskin P, Rosenstock J.  Aldose-reductase inhibitors and diabetic complications . Am J Med. 1987;;83:298-306.
Nath KA.  Platelets, antiplatelet therapy, and diabetic nephropathy . Mayo Clin Proc. 1988;;63:80-85.
Watts GF, Hodgson B, Morris RW, Shaw KM, Polak A.  Side-room tests to screen for microalbuminuria in diabetes mellitus . Diabetes Med. 1988;;5:298-303.
Linton AS, Rowe DJF.  Ames' 'Microbumintest' evaluated, and its correlation with total protein and albumin concentration in urine . Clin Chem. 1988;;34:1927-1928.
Coonrod BA, Ellis D, Becker DJ, et al.  Assessment of Albusure and its usefulness in identifying IDDM subjects at increased risk for developing clinical diabetic nephropathy . Diabetes Care. 1989;; 12:389-393.
Drury TF, Montgomery LE, Cohen BB.  Health insurance and health care coverage of adult diabetics . In: Harris MI, Hamman RF, eds. Diabetes in America . Bethesda, Md: US Dept of Health and Human Services; 1985;:XXXI-1-XXXI-14. Publication NIH 85-1468.
 Poor's access to care has declined markedly, new Robert Wood Johnson study reveals . Am Hosp Assoc News . (May) 1987;.
Pugh JA.  End-stage renal disease in Mexican-Americans . Presented at the Annual Meeting, American Public Health Association; November 15,1988 ; Boston, Mass.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

Friedman EA.  Diabetic renal disease . In: Ellenberg M, Rifkin H, eds. Diabetes Mellitus: Theory and Practice . New York, NY: Medical Examination Publishing Co Inc; 1983;:759-776.
Sugimoto T, Rosansky SJ.  The incidence of treated end-stage renal disease in the eastern United States: 1973-1979 . Am J Public Health. 1984;; 74:14-17.
US Renal Data System. 1989 Annual Data Report . Bethesda, Md: National Institute of Diabetes and Digestive and Kidney Diseases; 1989;.
Mogensen CE, Christensen CK, Vittinghus E.  The stages in diabetic nephropathy: with emphasis on the stage of incipient diabetic nephropathy . Diabetes. 1983;;32( (suppl 2) ):64-78.
Mogensen CE.  Renal function changes in diabetes . Diabetes. 1976;;25( (suppl 2) ):872-879.
Osterby R, Gundersen HJG.  Glomerular size and structure in diabetes mellitus, I: early abnormalities . Diabetologia. 1975;;11:225-229.
Hirose K, Tsuchida H, Osterby R, Gundersen JHG.  A strong correlation between glomerular filtration rate and filtration surface in diabetic kidney hyperfunction . Lab Invest. 1980;;43:434-437.
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.
Anderson S, Brenner BM.  Influence of antihypertensive therapy on development and progression of diabetic glomerulopathy . Diabetes Care. 1988;;11:846-849.
Parving H-H, Noer I, Deckert T, et al.  The effect of metabolic regulation on microvascular permeability to small and large molecules in short-term juvenile diabetics . Diabetologia. 1976;;12:161-166.
Osterby R.  Early phases in the development of diabetic glomerulopathy: a quantitative electron microscopic study . Acta Med Scand Suppl. 1974;; ( (574) ):1-82.
Steffes MW, Ellis EN, Mauer SM.  Complications of diabetes mellitus and factors affecting their progression . Clin Chem. 1986;;32( (suppl B) ):B54-B61.
Mauer SM, Steffes MW, Goetz FC, Sutherland DER, Brown DM.  Diabetic nephropathy: a perspective . Diabetes. 1983;;32( (suppl 2) ):52-55.
Steffes MW, Osterby R, Chavers B, Mauer SM.  Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients . Diabetes. 1989;;38:1077-1081.
Ellis D, Becker DJ, Dameron D, Lobes L, Drash AL.  Proteinuria in children with insulindependent diabetes: relationship to duration of disease, metabolic control, and retinal changes . J Pediatr. 1983;;102:673-680.
Mathiesen ER, Saurbrey N, Hommel E, Parving H-H.  Prevalence of microalbuminuria in children with insulin-dependent diabetes . Acta Endocrinol Suppl (Copenh) . 1986;;275:14.
Niazy S, Feldt-Rasmussen B, Deckert T.  Microalbuminuria in insulin-dependent diabetes: prevalence and practical consequences . J Diabetic Complications. 1987;;1:76-80.
Damsgaard EM, Mogensen CE.  Microalbuminuria in elderly hyperglycemic patients and controls . Diabetic Med. 1986;;3:430-435.
Uusitupa M, Siitonen O, Penttila I, Antti A, Pyorala K.  Proteinuria in newly diagnosed type II diabetic patients . Diabetes Care. 1987;;10:191-194.
Parving H-H, Oxenboll B, Svendsen PA, Christensen JS, Andersen AR.  Early detection of patients at risk of developing diabetic nephropathy: a longitudinal study of urinary albumin excretion . Acta Endocrinol (Copenh) . 1982;;100:550-555.
Viberti GC, Hill RD, Jarrett RJ, Argyropoulous A, Mahmud U, Keen H.  Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus . Lancet. 1982;;1:1430-1432.
Mathiesen ER, Oxenboll B, Johansen K, Svendsen PAA, Deckert T.  Incipient nephropathy in type I (insulin-dependent) diabetes . Diabetologia. 1984;;26:406-410.
Mogensen CE, Christensen CK.  Predicting diabetic nephropathy in insulin-dependent patients . N Engl J Med. 1984;;311:89-93.
Bennett PH.  'Microalbuminuria' and diabetes: a critique—assessment of urinary albumin excretion and its role in screening for diabetic nephropathy . Am J Kidney Dis. 1989;;13:29-34.
Chavers BM, Bilous RW, Ellis EN, Steffes MW, Mauer SM.  Glomerular lesions and urinary albumin excretion in type I diabetes without overt proteinuria . N Engl J Med. 1989;;320:966-970.
Mogensen CE.  Microalbuminuria predicts clinical proteinuria and early mortality in maturityonset diabetes . N Engl J Med. 1984;;310:356-360.
Jarrett RJ, Viberti BC, Argyropoulous A, Hill RD, Mahmud U, Murrells TJ.  Microalbuminuria predicts mortality in non-insulin-dependent diabetes . Diabetic Med. 1984;;1:17-19.
Andersen AR, Christiansen JK, Andersen JK, Kreiner S, Deckert T.  Diabetic nephropathy in type I (insulin-dependent) diabetes: an epidemiological study . Diabetologia. 1983;;25:496-501.
Krolewski AS, Warram JH, Christlieb AR, Busick EJ, Kahn CR.  The changing natural history of nephropathy in type I diabetes . Am J Med. 1985;;78:785-794.
Parving H-H, Andersen AR, Smidt UM, Christensen JS, Oxenboll B, Svendsen PAA.  Diabetic nephropathy and arterial hypertension: the effect of antihypertensive treatment . Diabetes. 1983;;32( (suppl 2) ):83-87.
Deckert T, Poulsen JE, Larsen M.  Prognosis of diabetics with diabetes onset before the age of thirty-one, II: factors influencing the prognosis . Diabetologia . 1978;;14:371-377.
Hasslacher C, Stech W, Wahl P, Ritz E.  Blood pressure and metabolic control as risk factors for nephropathy in type I (insulin-dependent) diabetes . Diabetologia. 1985;;28:6-11.
Borch-Johnsen K, Andersen PK, Deckert T.  The effect of proteinuria on relative mortality in type I (insulin-dependent) diabetes mellitus . Diabetologia. 1985;;28:590-596.
Deckert T, Poulsen JE, Larsen M.  Prognosis of diabetics with diabetes onset before the age of thirty one, I: survival, causes of death, and complications . Diabetologia. 1978;;14:363-370.
Fabre J, Balant LP, Dayer PG, Fox HM, Vernet AT.  The kidney in maturity onset diabetes mellitus: a clinical study of 510 patients . Kidney Int. 1982;;21:730-738.
Ballard DJ, Humphrey LL, Melton LJ III, et al.  Epidemiology of persistent proteinuria in type II diabetes mellitus . Diabetes. 1988;;37:405-412.
Klein R, Klein BEK, Moss S, DeMets DL.  Proteinuria in diabetes . Arch Intern Med. 1988;; 148:181-186.
Kamenetzky SA, Bennett PH, Dippe SE, Miller M, LeCompte PM.  A clinical and histological study of diabetic nephropathy in the Pima Indians . Diabetes. 1974;;23:61-68.
Rate RG, Knowler WC, Morse HG, et al.  Diabetes mellitus in Hopi and Navajo Indians: prevalence of microvascular complications . Diabetes. 1983;;32:894-899.
Schmitz A, Gundersen HJG, Mogensen CE, et al.  Diabetic glomerulopathy in type II patients—is it different from type I? Acta Endocrinol Suppl (Copenh). 1986;;275:13.
Humphrey LL, Ballard DJ, Frohnert PP, Chu C-P, O'Fallon WM, Palumbo PJ.  Chronic renal failure in non-insulin-dependent diabetes mellitus: a population-based study in Rochester, Minnesota . Ann Intern Med. 1989;;111:788-796.
Kofoed-Enevoldson A, Borch-Johnson K, Kreiner S, Nerup J, Deckert T.  Declining incidence of persistent proteinuria in type I (insulin-dependent) diabetic patients in Denmark . Diabetes. 1987;;36:205-209.
Christensen JS, Gammelgaard J, Tronier B, Svenden PA, Parving H-H.  Kidney function and size in diabetics before and during initial insulin treatment . Kidney Int. 1982;;21:683-688.
Rasch R.  Prevention of diabetic glomerulopathy in streptozotocin diabetic rats by insulin treatment: the mesangial regions . Diabetologia. 1979;;17:243-248.
Mauer SM, Sutherland DER, Steffes MW, et al.  Pancreatic islet transplantation: effect on the glomerular lesions of experimental diabetes in the rat . Diabetes. 1974;;23:748-753.
Bilous RW, Mauer SM, Sutherland DER, Najarian JS, Goetz FC, Steffes MW.  The effects of pancreas transplantation on the glomerular structure of renal allografts in patients with insulindependent diabetes . N Engl J Med. 1989;;321:80-85.
The Kroc Collaborative Study Group.  Blood glucose control and the evolution of diabetic retinopathy and albuminuria: a preliminary multicenter trial . N Engl J Med. 1984;;311:365-372.
Feldt-Rasmussen B, Mathiesen ER, Deckert T.  Effect of two years of strict metabolic control on progression of incipient nephropathy in insulin-dependent diabetes . Lancet. 1986;;2:1300-1304.
Holman RR, Dornan TL, Mayon-White V, et al.  Prevention of deterioration of renal and sensorynerve function by more intensive management of insulin-dependent diabetic patients . Lancet. 1983;;1:204-208.
Dahl-Jorgensen K, Brinchmann-Hansen O, Hanssen KF, et al.  Effect of near normoglycaemia for two years on progression of early diabetic retinopathy, nephropathy, and neuropathy: The Oslo Study . Br Med J. 1986;;293:1195-1199.
The DCCT Research Group.  The Diabetes Control and Complications Trial (DCCT): design and methodologic considerations for the feasibility phase . Diabetes. 1986;;35:530-545.
The DCCT Research Group.  Are continuing studies of metabolic control of microvascular complications in insulin-dependent diabetes mellitus justified? N Engl J Med. 1988;;318:246-250.
Tamborlane WV, Puklin JE, Bergman M, et al.  Long-term improvement of metabolic control with the insulin pump does not reverse diabetic microangiopathy . Diabetes Care. 1982;;5:58-64.
Miller DG, Hampton L, Fredricka V, et al.  The use of an open-loop pump in type I diabetics with renal insufficiency . Diabetic Nephropathy. 1984;; 3:19-21.
Simonson DC.  Etiology and prevalence of hypertension in diabetic patients . Diabetes Care. 1988;;11:821-827.
Christlieb AR, Warram JH, Krolewski AS, et al.  Hypertension: the major risk factor in juvenileonset insulin-dependent diabetics . Diabetes. 1981;; 30( (suppl 2) ):90-96.
Jensen T, Borch-Johnsen K, Deckert T.  Changes in blood pressure and renal function in patients with type I (insulin-dependent) diabetes mellitus prior to clinical diabetes nephropathy . Diabetes Res. 1987;;4:159-162.
Mauer SM, Steffes MW, Azar S, Kupcho-Sandberg S, Brown DM.  The effects of Goldblatt hypertension on development of the glomerular lesions of diabetes mellitus in the rat . Diabetes. 1978;;27:738-744.
Zatz R, Dunn BR, Meyer TW, Anderson S, Rennke HG, Brenner BM.  Prevention of diabetic glomerulopathy by pharmacologic amelioration of glomerular capillary hypertension . J Clin Invest. 1986;;77:1925-1930.
Mathiesen ER, Ronn B, Jensen T, Storm B, Deckert T.  Relationship between blood pressure and urinary albumin excretion in development of micoralbuminuria . Diabetes. 1990;;39:345-349.
Viberti GC, Keen H. Wiseman MJ.  Raised arterial pressure in parents of proteinuric insulindependent diabetics . Br Med J. 1987;;295:515-517.
Krolewski AS, Canessa M, Warram JH, et al.  Predispostion to hypertension and susceptibility to renal disease in insulin-dependent diabetes mellitus . N Engl J Med. 1988;;318:140-145.
Krolewski AS.  The natural history of diabetic nephropathy in type I diabetes and the role of hypertension . Ann Intern Med. 1989;;110:795-798.
Knowler WC, Bennett PH, Nelson RG.  Prediabetic blood pressure predicts albuminuria after development of NIDDM . Diabetes. 1988;;37( (suppl 1) ):120a. Abstract.
Wiseman M, Viberti GC, Mackintosh D, Jarrett RF, Keen H.  Glycemia, arterial pressure and microalbuminuria in type 1 (insulin-dependent) diabetes mellitus . Diabetologia. 1984;;26:401-405.
Keen H, Chlouverakis C, Fuller JH, Jarrett RJ.  The concomitants of raised blood sugar: studies in newly detected hyperglycemics, II: urinary albumin excretion, blood pressure and their relation to blood sugar levels . Guy's Hosp Rep. 1969;;118:247-252.
Viberti GC, Bending JJ.  Early diabetic nephropathy . Adv Nephrol. 1988;;17:101-112.
Mimran A, Insua A, Ribstein J, Bringer J, Monnier L.  Comparative effect of captopril and nifedipine in normotensive patients with incipient diabetic nephropathy . Diabetes Care. 1988;;11:850-853.
Parving H-H, Smidt UM, Andersen AR, Svendsen PA.  Early aggressive antihypertensive treatment reduces rate of decline in kidney function in diabetic nephropathy . Lancet. 1983;;1:1175-1178.
Bjorck S, Nyberg G, Mulec H, Granerus G, Herlitz H, Aurell M.  Beneficial effects of angiotensin-converting enzyme inhibition on renal function in patients with diabetic nephropathy . Br Med J. 1986;;293:471-474.
Taguma AC, Kitamoto UY, Futaki G, et al.  Effect of captopril on heavy proteinuria in azotemic diabetes . N Engl J Med. 1985;;313:1617-1620.
The Working Group on Hypertension in Diabetes.  Statement on hypertension in diabetes mellitus . Arch Intern Med. 1987;;147:830-842.
The Working Group on Hypertension in Diabetes.  Statement on hypertension in diabetes mellitus . Arch Intern Med. 1987;;147:1165-1166.
Rosenstock J, Raskin P.  Early diabetic nephropathy: assessment and potential therapeutic interventions . Diabetes Care. 1986;;9:529-545.
Hawthorne V, Herman WH, eds.  International Symposium on Preventing the Kidney Disease of Diabetes Mellitus: public health perspectives . Am J Kidney Dis. 1989;;13:2-6.
Kaplan NM, Rosenstock J, Raskin P.  A differing view of treatment of hypertension in patients with diabetes mellitus . Arch Intern Med. 1987;;147: 1160-1162.
Keane WF, Anderson S, [ill]urell M, de Zeeuw D, Narins RG, Povar G.  Angiotension-converting enzyme inhibitors and progressive renal insufficiency . Ann Intern Med. 1989;;111:503-516.
Feig PU, Rutan GH.  Angiotension-converting enzyme inhibitors: the end of end-stage renal disease? Ann Intern Med. 1989;;111:451-452.
Hostetter TH, Meyer TW, Rennke HG, Brenner BM.  Chronic effects of dietary protein on renal structure and function in the rat with intact and reduced renal mass . Kidney Int. 1986;;30:509-517.
Don BR, Schambelan M.  Diabetes, dietary protein and glomerular hyperfiltration . West J Med. 1987;;147:449-455.
Wiseman MJ, Bogneth E, Dodds R, Keen H, Viberti GC.  Changes in renal function in response to protein restricted diet in type I diabetes . Diabetologia. 1987;;30:154-159.
Cohen DL, Dodds R, Viberti GC.  Reduction of microalbuminuria and glomerular filtration rate by dietary protein restriction in type I (insulin-dependent) diabetic patients: an effect independent of blood glucose control and arterial pressure changes . Diabetologia. 1986;;29:528a. Abstract.
Evanoff GV, Thompson CS, Brown J, Weinman EJ.  The effect of dietary protein restriction on the progression of diabetic nephropathy: a 12-month follow-up . Arch Intern Med. 1987;;147:492-495.
Bending JJ, Dodds RA, Keen H, Viberti GC.  Renal responses to restricted protein intake in diabetic nephropathy . Diabetes. 1988;;37:1641-1646.
American Diabetes Association.  Nutritional recommendations and principles for individuals with diabetes mellitus: 1986 . Diabetes Care . 1987;; 10:126-132.
Keane WF, Kasiske BL, O'Donnell MP.  Hyperlipidemia and the progression of renal disease . Am J Clin Nutr. 1988;;47:157-160.
Pettitt DJ, Saad MF.  Inheritance of predisposition to renal insufficiency in diabetic men . Diabetes. 1988;;37( (suppl 1) ):51A. Abstract.
Seaquist ER, Goetz FC, Rich S, Barbosa J.  Familial clustering of diabetic kidney disease . N Engl J Med. 1989;;320:1161-1165.
Barnett AH, Pyke DA.  The genetics of diabetic complications . Clin Endocrinol Metab. 1986;;15: 715-726.
Rettig BS, Teutsch SM.  The incidence of endstage renal disease in type I and type II diabetes mellitus . Diabetic Nephropathy. 1984;;3:26-27.
Kappel DF, Van Tuinen M.  Trends in the incidence of treated end-stage renal disease secondary to diabetic nephropathy: 1975-84 . Am J Kidney Dis. 1986;;8:234-238.
Cowie CC, Port FK, Wolfe RA, Savage PJ, Moll PP, Hawthorne VM.  Disparities in incidence of diabetic end-stage renal disease according to race and type of diabetes . N Engl J Med. 1989;;321:1074-1079.
Nelson RG, Pettitt DJ, Carraher MJ, Baird HR, Knowler WC.  Effect of proteinuria on mortality in NIDDM . Diabetes. 1988;;37:1499-1504.
Nelson RG, Newman JM, Knowler WC, et al.  Incidence of end-stage renal disease in type 2 diabetes mellitus in Pima Indians . Diabetologia. 1988;; 31:730-736.
Pugh JA, Stern MP, Zapata M.  Excess incidence of treatment of end-stage renal disease in Mexican-Americans . Am J Epidemiol . 1988;;127: 135-144.
Newman JM, Marfin AA, Eggers PW, Helgerson SD.  End-stage renal disease among Native Americans . Am J Public Health. 1990;;80:318-319.
Haffner SM, Mitchell BD, Pugh JA, et al.  Proteinuria in Mexican-Americans and non-Hispanic whites with NIDDM . Diabetes Care. 1989;;12:530-536.
Eggers PW, Connerton R, McMullan M.  The Medicare experience with end-stage renal disease . Health Care Financ Rev. 1984;;5:69-88.
Raskin P, Rosenstock J.  Aldose-reductase inhibitors and diabetic complications . Am J Med. 1987;;83:298-306.
Nath KA.  Platelets, antiplatelet therapy, and diabetic nephropathy . Mayo Clin Proc. 1988;;63:80-85.
Watts GF, Hodgson B, Morris RW, Shaw KM, Polak A.  Side-room tests to screen for microalbuminuria in diabetes mellitus . Diabetes Med. 1988;;5:298-303.
Linton AS, Rowe DJF.  Ames' 'Microbumintest' evaluated, and its correlation with total protein and albumin concentration in urine . Clin Chem. 1988;;34:1927-1928.
Coonrod BA, Ellis D, Becker DJ, et al.  Assessment of Albusure and its usefulness in identifying IDDM subjects at increased risk for developing clinical diabetic nephropathy . Diabetes Care. 1989;; 12:389-393.
Drury TF, Montgomery LE, Cohen BB.  Health insurance and health care coverage of adult diabetics . In: Harris MI, Hamman RF, eds. Diabetes in America . Bethesda, Md: US Dept of Health and Human Services; 1985;:XXXI-1-XXXI-14. Publication NIH 85-1468.
 Poor's access to care has declined markedly, new Robert Wood Johnson study reveals . Am Hosp Assoc News . (May) 1987;.
Pugh JA.  End-stage renal disease in Mexican-Americans . Presented at the Annual Meeting, American Public Health Association; November 15,1988 ; Boston, Mass.
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To understand the clinical management of acute heart failure syndromes.
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