Clinical Manifestations of Kidney Disease Among US Adults With Diabetes, 1988-2014 | Chronic Kidney Disease | JAMA | JAMA Network
[Skip to Navigation]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address Please contact the publisher to request reinstatement.
Tuttle  KR, Bakris  GL, Bilous  RW,  et al.  Diabetic kidney disease: a report from an ADA consensus conference.  Diabetes Care. 2014;37(10):2864-2883.PubMedGoogle ScholarCrossref
de Boer  IH, Rue  TC, Hall  YN, Heagerty  PJ, Weiss  NS, Himmelfarb  J.  Temporal trends in the prevalence of diabetic kidney disease in the United States.  JAMA. 2011;305(24):2532-2539.PubMedGoogle ScholarCrossref
Tuttle  KR, Stein  JH, DeFronzo  RA.  The natural history of diabetic nephropathy.  Semin Nephrol. 1990;10(3):184-193.PubMedGoogle Scholar
Costacou  T, Ellis  D, Fried  L, Orchard  TJ.  Sequence of progression of albuminuria and decreased GFR in persons with type 1 diabetes: a cohort study.  Am J Kidney Dis. 2007;50(5):721-732.PubMedGoogle ScholarCrossref
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(1):57-64.PubMedGoogle ScholarCrossref
Molitch  ME, Steffes  M, Sun  W,  et al; Epidemiology of Diabetes Interventions and Complications Study Group.  Development and progression of renal insufficiency with and without albuminuria in adults with type 1 diabetes in the Diabetes Control and Complications trial and the Epidemiology of Diabetes Interventions and Complications study.  Diabetes Care. 2010;33(7):1536-1543.PubMedGoogle ScholarCrossref
Tsalamandris  C, Allen  TJ, Gilbert  RE,  et al.  Progressive decline in renal function in diabetic patients with and without albuminuria.  Diabetes. 1994;43(5):649-655.PubMedGoogle ScholarCrossref
Kramer  HJ, Nguyen  QD, Curhan  G, Hsu  CY.  Renal insufficiency in the absence of albuminuria and retinopathy among adults with type 2 diabetes mellitus.  JAMA. 2003;289(24):3273-3277.PubMedGoogle ScholarCrossref
Thomas  MC, Macisaac  RJ, Jerums  G,  et al.  Nonalbuminuric renal impairment in type 2 diabetic patients and in the general population (National Evaluation of the Frequency of Renal Impairment Co-existing with NIDDM [NEFRON] 11).  Diabetes Care. 2009;32(8):1497-1502.PubMedGoogle ScholarCrossref
Bojestig  M, Arnqvist  HJ, Karlberg  BE, Ludvigsson  J.  Glycemic control and prognosis in type I diabetic patients with microalbuminuria.  Diabetes Care. 1996;19(4):313-317.PubMedGoogle ScholarCrossref
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.PubMedGoogle ScholarCrossref
Rossing  P, Hougaard  P, Parving  HH.  Progression of microalbuminuria in type 1 diabetes: ten-year prospective observational study.  Kidney Int. 2005;68(4):1446-1450.PubMedGoogle ScholarCrossref
de Boer  IH, Rue  TC, Cleary  PA,  et al; Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Study 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):412-420.PubMedGoogle ScholarCrossref
de Boer  IH, Afkarian  M, Rue  TC,  et al; Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Research Group.  Renal outcomes in patients with type 1 diabetes and macroalbuminuria.  J Am Soc Nephrol. 2014;25(10):2342-2350.PubMedGoogle ScholarCrossref
US Centers for Disease Control and Prevention; National Center for Health Statistics. National Health and Nutrition Examination Survey 1988-1994, 1999-2000, 2001-2002, 2003-2004, 2005-2006, and 2007-2008 documentation files. Accessed December 1, 2010.
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.PubMedGoogle ScholarCrossref
Cowie  CC, Rust  KF, Byrd-Holt  DD,  et al.  Prevalence of diabetes and high risk for diabetes using A1C criteria in the US population in 1988-2006.  Diabetes Care. 2010;33(3):562-568.PubMedGoogle ScholarCrossref
Coresh  J, Astor  BC, McQuillan  G,  et al.  Calibration and random variation of the serum creatinine assay as critical elements of using equations to estimate glomerular filtration rate.  Am J Kidney Dis. 2002;39(5):920-929.PubMedGoogle ScholarCrossref
Selvin  E, Manzi  J, Stevens  LA,  et al.  Calibration of serum creatinine in the National Health and Nutrition Examination Surveys (NHANES) 1988-1994, 1999-2004.  Am J Kidney Dis. 2007;50(6):918-926.PubMedGoogle ScholarCrossref
Coresh  J, Selvin  E, Stevens  LA,  et al.  Prevalence of chronic kidney disease in the United States.  JAMA. 2007;298(17):2038-2047.PubMedGoogle ScholarCrossref
Levey  AS, Stevens  LA, Schmid  CH,  et al; CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration).  A new equation to estimate glomerular filtration rate.  Ann Intern Med. 2009;150(9):604-612.PubMedGoogle ScholarCrossref
R Foundation for Statistical Computing. A language and environment for statistical computing.
Rubin  DB.  Multiple Imputation for Nonresponse in Surveys. New York, NY: J Wiley & Sons; 1987.
Holman  RR, Paul  SK, Bethel  MA, Matthews  DR, Neil  HA.  10-year follow-up of intensive glucose control in type 2 diabetes.  N Engl J Med. 2008;359(15):1577-1589.PubMedGoogle ScholarCrossref
Duckworth  W, Abraira  C, Moritz  T,  et al; VADT Investigators.  Glucose control and vascular complications in veterans with type 2 diabetes.  N Engl J Med. 2009;360(2):129-139.PubMedGoogle ScholarCrossref
DCCT/EDIC Research Group.  Effect of intensive diabetes treatment on albuminuria in type 1 diabetes: long-term follow-up of the Diabetes Control and Complications Trial and Epidemiology of Diabetes Interventions and Complications study.  Lancet Diabetes Endocrinol. 2014;2(10):793-800.PubMedGoogle ScholarCrossref
Klahr  S, Levey  AS, Beck  GJ,  et al; 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(13):877-884.PubMedGoogle ScholarCrossref
Parving  HH, Lehnert  H, Bröchner-Mortensen  J, Gomis  R, Andersen  S, Arner  P; Irbesartan in Patients with Type 2 Diabetes and Microalbuminuria Study Group.  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.PubMedGoogle ScholarCrossref
Stark Casagrande  S, Fradkin  JE, Saydah  SH, Rust  KF, Cowie  CC.  The prevalence of meeting A1C, blood pressure, and LDL goals among people with diabetes, 1988-2010.  Diabetes Care. 2013;36(8):2271-2279.PubMedGoogle ScholarCrossref
Gregg  EW, Li  Y, Wang  J,  et al.  Changes in diabetes-related complications in the United States, 1990-2010.  N Engl J Med. 2014;370(16):1514-1523.PubMedGoogle ScholarCrossref
Molitch  ME, Adler  AI, Flyvbjerg  A,  et al.  Diabetic kidney disease: a clinical update from Kidney Disease: Improving Global Outcomes.  Kidney Int. 2015;87(1):20-30.PubMedGoogle ScholarCrossref
Original Investigation
August 9, 2016

Clinical Manifestations of Kidney Disease Among US Adults With Diabetes, 1988-2014

Author Affiliations
  • 1Kidney Research Institute and Division of Nephrology, Department of Medicine, University of Washington, Seattle
  • 2Department of Biostatistics, University of Washington, Seattle
  • 3Providence Health Care, Spokane, Washington
  • 4Institute of Translational Health Sciences, University of Washington School of Medicine, Seattle
  • 5Department of Epidemiology, University of Washington, Seattle
JAMA. 2016;316(6):602-610. doi:10.1001/jama.2016.10924

Importance  Diabetic kidney disease is the leading cause of chronic and end-stage kidney disease in the United States and worldwide. Changes in demographics and treatments may affect the prevalence and clinical manifestations of diabetic kidney disease.

Objective  To characterize the clinical manifestations of kidney disease among US adults with diabetes over time.

Design, Setting, and Participants  Serial cross-sectional studies of adults aged 20 years or older with diabetes mellitus participating in National Health and Nutrition Examination Surveys from 1988 through 2014.

Exposures  Diabetes was defined as hemoglobin A1c greater than 6.5% or use of glucose-lowering medications.

Main Outcomes and Measures  Albuminuria (urine albumin-to-creatinine ratio ≥30 mg/g), macroalbuminuria (urine albumin-to-creatinine ratio ≥300 mg/g), reduced estimated glomerular filtration rate (eGFR <60 mL/min/1.73 m2), and severely reduced eGFR (<30 mL/min/1.73 m2), incorporating data on biological variability to estimate the prevalence of persistent abnormalities.

Results  There were 6251 adults with diabetes included (1431 from 1988-1994, 1443 from 1999-2004, 1280 from 2005-2008, and 2097 from 2009-2014). The prevalence of any diabetic kidney disease, defined as persistent albuminuria, persistent reduced eGFR, or both, did not significantly change over time from 28.4% (95% CI, 23.8%-32.9%) in 1988-1994 to 26.2% (95% CI, 22.6%-29.9%) in 2009-2014 (prevalence ratio, 0.95 [95% CI, 0.86-1.06] adjusting for age, sex, and race/ethnicity; P = .39 for trend). However, the prevalence of albuminuria decreased progressively over time from 20.8% (95% CI, 16.3%-25.3%) in 1988-1994 to 15.9% (95% CI, 12.7%-19.0%) in 2009-2014 (adjusted prevalence ratio, 0.76 [95% CI, 0.65-0.89]; P < .001 for trend). In contrast, the prevalence of reduced eGFR increased from 9.2% (95% CI, 6.2%-12.2%) in 1988-1994 to 14.1% (95% CI, 11.3%-17.0%) in 2009-2014 (adjusted prevalence ratio, 1.61 [95% CI, 1.33-1.95] comparing 2009-2014 with 1988-1994; P < .001 for trend), with a similar pattern for severely reduced eGFR (adjusted prevalence ratio, 2.86 [95% CI, 1.38-5.91]; P = .004 for trend). Significant heterogeneity in the temporal trend for albuminuria was noted by age (P = .049 for interaction) and race/ethnicity (P = .007 for interaction), with a decreasing prevalence of albuminuria observed only among adults younger than 65 years and non-Hispanic whites, whereas the prevalence of reduced GFR increased without significant differences by age or race/ethnicity. In 2009-2014, approximately 8.2 million adults with diabetes (95% CI, 6.5-9.9 million adults) had albuminuria, reduced eGFR, or both.

Conclusions and Relevance  Among US adults with diabetes from 1988 to 2014, the overall prevalence of diabetic kidney disease did not change significantly, whereas the prevalence of albuminuria declined and the prevalence of reduced eGFR increased.