Papers

Predictors of mortality in insulin dependent diabetes: 10 year observational follow up study

^a Steno Diabetes Centre, DK 2820 Gentofte, Denmark, ^b Novo Nordisk, Statistics HRT/CNS/GH, Health Care Development, Bagsvaerd, Denmark, ^c Centre of Preventive Medicine, Medical Department C, Glostrup University Hospital, Glostrup, Denmark

Correspondence to: Dr Rossing.

Abstract

Objective: To evaluate the prognostic significance of microalbuminuria and overt diabetic nephropathy and other putative risk factors for cardiovascular and all cause mortality in insulin dependent diabetes.
Design: Ten year observational follow up study.
Setting: Outpatient diabetic clinic in a tertiary referral centre.
Subjects: All 939 adults with insulin dependent diabetes (duration of diabetes five years or more) attending the clinic in 1984; 593 had normal urinary albumin excretion (</=30 mg/24 h), 181 persistent microalbuminuria (31-299 mg/24 h), and 165 overt nephropathy (>/=300 mg/24 h).
Main outcome measure: All cause and cardiovascular mortality.
Results: Fifteen per cent of patients (90/593) with normoalbuminuria, 25% (45/181) with microalbuminuria, and 44% (72/165) with overt nephropathy at baseline died during follow up. Cox multiple regression analysis identified the following significant predictors of all cause mortality: male sex (relative risk 2.03; 95% confidence interval 1.37 to 3.02), age (1.07; 1.06 to 1.08), height (0.96; 0.94 to 0.98), smoking (1.51; 1.09 to 2.08), social class V versus social class IV (1.70; 1.25 to 2.31), log10 urinary albumin excretion (1.45; 1.18 to 1.77), hypertension (1.63; 1.18 to 2.25), log10 serum creatinine concentration (8.96; 3.34 to 24.08), and haemoglobin A1c concentration (1.11; 1.03 to 1.20). Age, smoking, microalbuminuria, overt nephropathy, and hypertension were significant predictors of cardiovascular mortality. Mortality in patients with microalbuminuria was only slightly increased compared with that in patients with normoalbuminuria. Median survival time after the onset of overt diabetic nephropathy was 13.9 years (95% confidence interval 11.8 to 17.2 years).
Conclusions: Abnormally increased urinary albumin excretion and other potentially modifiable risk factors such as hypertension, smoking, poor glycaemic control, and social class predict increased mortality in insulin dependent diabetes. Microalbuminuria by itself confers only a small increase in mortality. The prognosis of patients with overt diabetic nephropathy has improved, probably owing to effective antihypertensive treatment.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

Relevant Article

Different strategies for screening and prevention of type 2 diabetes in adults: cost effectiveness analysis

Clare L Gillies, Paul C Lambert, Keith R Abrams, Alex J Sutton, Nicola J Cooper, Ron T Hsu, Melanie J Davies, and Kamlesh Khunti
BMJ 2008 336: 1180-1185. [Abstract] [Full Text] [PDF]

This article has been cited by other articles:

• Groop, P.-H., Thomas, M. C., Moran, J. L., Waden, J., Thorn, L. M., Makinen, V.-P., Rosengard-Barlund, M., Saraheimo, M., Hietala, K., Heikkila, O., Forsblom, C., on behalf of the FinnDiane Study Group, (2009). The Presence and Severity of Chronic Kidney Disease Predicts All-Cause Mortality in Type 1 Diabetes. Diabetes 58: 1651-1658 [Abstract] [Full text]  
• Brantsma, A. H., Bakker, S. J. L., Hillege, H. L., de Zeeuw, D., de Jong, P. E., Gansevoort, R. T., for the PREVEND Study Group, (2008). Cardiovascular and renal outcome in subjects with K/DOQI stage 1-3 chronic kidney disease: the importance of urinary albumin excretion. Nephrol Dial Transplant 23: 3851-3858 [Abstract] [Full text]  
• Saleem, T., Mohammad, K. H., Abdel-Fattah, M. M, Abbasi, A. H. (2008). Association of glycosylated haemoglobin level and diabetes mellitus duration with the severity of coronary artery disease. Diabetes and Vascular Disease Research 5: 184-189 [Abstract]  
• Rademacher, E., Mauer, M., Jacobs, D. R. Jr, Chavers, B., Steinke, J., Sinaiko, A. (2008). Albumin Excretion Rate in Normal Adolescents: Relation to Insulin Resistance and Cardiovascular Risk Factors and Comparisons to Type 1 Diabetes Mellitus Patients. CJASN 3: 998-1005 [Abstract] [Full text]  
• Soedamah-Muthu, S. S., Chaturvedi, N., Witte, D. R., Stevens, L. K., Porta, M., Fuller, J. H., for the EURODIAB Prospective Complications Study G, (2008). Relationship Between Risk Factors and Mortality in Type 1 Diabetic Patients in Europe: The EURODIAB Prospective Complications Study (PCS). Diabetes Care 31: 1360-1366 [Abstract] [Full text]  
• Gillies, C. L, Lambert, P. C, Abrams, K. R, Sutton, A. J, Cooper, N. J, Hsu, R. T, Davies, M. J, Khunti, K. (2008). Different strategies for screening and prevention of type 2 diabetes in adults: cost effectiveness analysis. BMJ 336: 1180-1185 [Abstract] [Full text]  
• Palmas, W., Pickering, T. G., Teresi, J., Schwartz, J. E., Field, L., Weinstock, R. S., Shea, S. (2008). Telemedicine Home Blood Pressure Measurements and Progression of Albuminuria in Elderly People With Diabetes. Hypertension 51: 1282-1288 [Abstract] [Full text]  
• Lajer, M., Tarnow, L., Jorsal, A., Teerlink, T., Parving, H.-H., Rossing, P. (2008). Plasma Concentration of Asymmetric Dimethylarginine (ADMA) Predicts Cardiovascular Morbidity and Mortality in Type 1 Diabetic Patients With Diabetic Nephropathy. Diabetes Care 31: 747-752 [Abstract] [Full text]  
• Raile, K., Galler, A., Hofer, S., Herbst, A., Dunstheimer, D., Busch, P., Holl, R. W. (2007). Diabetic Nephropathy in 27,805 Children, Adolescents, and Adults With Type 1 Diabetes: Effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care 30: 2523-2528 [Abstract] [Full text]  
• Pambianco, G., Costacou, T., Orchard, T. J. (2007). The Prediction of Major Outcomes of Type 1 Diabetes: a 12-Year Prospective Evaluation of Three Separate Definitions of the Metabolic Syndrome and Their Components and Estimated Glucose Disposal Rate: The Pittsburgh Epidemiology of Diabetes Complications Study experience . Diabetes Care 30: 1248-1254 [Abstract] [Full text]  
• Ajjan, R. A, Grant, P. J (2006). Cardiovascular disease prevention in patients with type 2 diabetes: the role of oral anti-diabetic agents. Diabetes and Vascular Disease Research 3: 147-158 [Abstract]  
• Stadler, M., Auinger, M., Anderwald, C., Kastenbauer, T., Kramar, R., Feinbock, C., Irsigler, K., Kronenberg, F., Prager, R. (2006). Long-Term Mortality and Incidence of Renal Dialysis and Transplantation in Type 1 Diabetes Mellitus. J. Clin. Endocrinol. Metab. 91: 3814-3820 [Abstract] [Full text]  
• Palmas, W., Moran, A., Pickering, T., Eimicke, J. P., Teresi, J., Schwartz, J. E., Field, L., Weinstock, R. S., Shea, S. (2006). Ambulatory Pulse Pressure and Progression of Urinary Albumin Excretion in Older Patients With Type 2 Diabetes Mellitus. Hypertension 48: 301-308 [Abstract] [Full text]  
• Moran, A., Palmas, W., Pickering, T. G., Schwartz, J. E., Field, L., Weinstock, R. S., Shea, S. (2006). Office and Ambulatory Blood Pressure Are Independently Associated With Albuminuria in Older Subjects With Type 2 Diabetes. Hypertension 47: 955-961 [Abstract] [Full text]  
• Nieuwdorp, M., Mooij, H. L., Kroon, J., Atasever, B., Spaan, J. A.E., Ince, C., Holleman, F., Diamant, M., Heine, R. J., Hoekstra, J. B.L., Kastelein, J. J.P., Stroes, E. S.G., Vink, H. (2006). Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes.. Diabetes 55: 1127-1132 [Abstract] [Full text]  
• Brinkman, J. W., de Zeeuw, D., Duker, J. J., Gansevoort, R. T., Kema, I. P., Hillege, H. L., de Jong, P. E., Bakker, S. J.L. (2005). Falsely Low Urinary Albumin Concentrations after Prolonged Frozen Storage of Urine Samples. Clin. Chem. 51: 2181-2183 [Full text]  
• Weekers, L., Bouhanick, B., Hadjadj, S., Gallois, Y., Roussel, R., Pean, F., Ankotche, A., Chatellier, G., Alhenc-Gelas, F., Lefebvre, P. J., Marre, M. (2005). Modulation of the Renal Response to ACE Inhibition by ACE Insertion/Deletion Polymorphism During Hyperglycemia in Normotensive, Normoalbuminuric Type 1 Diabetic Patients. Diabetes 54: 2961-2967 [Abstract] [Full text]  
• Amin, R, Bahu, T K, Widmer, B, Dalton, R N, Dunger, D B (2005). Longitudinal relation between limited joint mobility, height, insulin-like growth factor 1 levels, and risk of developing microalbuminuria: the Oxford Regional Prospective Study. Arch. Dis. Child. 90: 1039-1044 [Abstract] [Full text]  
• Jensen, J. S., Feldt-Rasmussen, B., Borch-Johnsen, K., Jensen, K. S., Nordestgaard, B. G. (2005). Increased Transvascular Lipoprotein Transport in Diabetes: Association with Albuminuria and Systolic Hypertension. J. Clin. Endocrinol. Metab. 90: 4441-4445 [Abstract] [Full text]  
• Laing, S. P., Jones, M. E., Swerdlow, A. J., Burden, A. C., Gatling, W. (2005). Psychosocial and Socioeconomic Risk Factors for Premature Death in Young People With Type 1 Diabetes. Diabetes Care 28: 1618-1623 [Abstract] [Full text]  
• Jacobsen, P. K. (2005). Review: Preventing End-Stage Renal Disease in Diabetic Patients -- Dual Blockade of the Renin-Angiotensin System (Part II). Journal of Renin-Angiotensin-Aldosterone System 6: 55-68 [Abstract]  
• Vanholder, R., Massy, Z., Argiles, A., Spasovski, G., Verbeke, F., Lameire, N., for the European Uremic Toxin Work Group (EUTox), (2005). Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol Dial Transplant 20: 1048-1056 [Abstract] [Full text]  
• Kistorp, C., Raymond, I., Pedersen, F., Gustafsson, F., Faber, J., Hildebrandt, P. (2005). N-Terminal Pro-Brain Natriuretic Peptide, C-Reactive Protein, and Urinary Albumin Levels as Predictors of Mortality and Cardiovascular Events in Older Adults. JAMA 293: 1609-1616 [Abstract] [Full text]  
• Jacobsen, P. K. (2005). Preventing end stage renal disease in diabetic patients -- genetic aspect (part I). Journal of Renin-Angiotensin-Aldosterone System 6: 1-14 [Abstract]  
• Maahs, D. M., Kinney, G. L., Wadwa, P., Snell-Bergeon, J. K., Dabelea, D., Hokanson, J., Ehrlich, J., Garg, S., Eckel, R. H., Rewers, M. J. (2005). Hypertension Prevalence, Awareness, Treatment, and Control in an Adult Type 1 Diabetes Population and a Comparable General Population. Diabetes Care 28: 301-306 [Abstract] [Full text]  
• Hadjadj, S., Pean, F., Gallois, Y., Passa, P., Aubert, R., Weekers, L., Rigalleau, V., Bauduceau, B., Bekherraz, A., Roussel, R., Dussol, B., Rodier, M., Marechaud, R., Lefebvre, P. J., Marre, M., for the Genesis France-Belgium Study, (2004). Different Patterns of Insulin Resistance in Relatives of Type 1 Diabetic Patients With Retinopathy or Nephropathy: The Genesis France-Belgium Study. Diabetes Care 27: 2661-2668 [Abstract] [Full text]  
• Marshall, S M (2004). Recent advances in diabetic nephropathy. Postgrad. Med. J. 80: 624-633 [Abstract] [Full text]  
• de Zeeuw, D., Remuzzi, G., Parving, H.-H., Keane, W. F., Zhang, Z., Shahinfar, S., Snapinn, S., Cooper, M. E., Mitch, W. E., Brenner, B. M. (2004). Albuminuria, a Therapeutic Target for Cardiovascular Protection in Type 2 Diabetic Patients With Nephropathy. Circulation 110: 921-927 [Abstract] [Full text]  
• Menne, J., Park, J.-K., Boehne, M., Elger, M., Lindschau, C., Kirsch, T., Meier, M., Gueler, F., Fiebeler, A., Bahlmann, F. H., Leitges, M., Haller, H. (2004). Diminished Loss of Proteoglycans and Lack of Albuminuria in Protein Kinase C-{alpha}--Deficient Diabetic Mice. Diabetes 53: 2101-2109 [Abstract] [Full text]  
• Klausen, K., Borch-Johnsen, K., Feldt-Rasmussen, B., Jensen, G., Clausen, P., Scharling, H., Appleyard, M., Jensen, J. S. (2004). Very Low Levels of Microalbuminuria Are Associated With Increased Risk of Coronary Heart Disease and Death Independently of Renal Function, Hypertension, and Diabetes. Circulation 110: 32-35 [Abstract] [Full text]  
• Kuo, Y.-F., Raji, M. A., Peek, M. K., Goodwin, J. S. (2004). Health-Related Social Disengagement in Elderly Diabetic Patients: Association with subsequent disability and survival. Diabetes Care 27: 1630-1637 [Abstract] [Full text]  
• Young, B. A., Pugh, J. A., Maynard, C., Reiber, G. (2004). Diabetes and Renal Disease in Veterans. Diabetes Care 27: B45-B49 [Abstract] [Full text]  
• Soedamah-Muthu, S. S., Chaturvedi, N., Toeller, M., Ferriss, B., Reboldi, P., Michel, G., Manes, C., Fuller, J. H. (2004). Risk Factors for Coronary Heart Disease in Type 1 Diabetic Patients in Europe: The EURODIAB Prospective Complications Study. Diabetes Care 27: 530-537 [Abstract] [Full text]  
• Sarnak, M. J., Levey, A. S., Schoolwerth, A. C., Coresh, J., Culleton, B., Hamm, L. L., McCullough, P. A., Kasiske, B. L., Kelepouris, E., Klag, M. J., Parfrey, P., Pfeffer, M., Raij, L., Spinosa, D. J., Wilson, P. W. (2003). Kidney Disease as a Risk Factor for Development of Cardiovascular Disease: A Statement From the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Hypertension 42: 1050-1065 [Full text]  
• Sarnak, M. J., Levey, A. S., Schoolwerth, A. C., Coresh, J., Culleton, B., Hamm, L. L., McCullough, P. A., Kasiske, B. L., Kelepouris, E., Klag, M. J., Parfrey, P., Pfeffer, M., Raij, L., Spinosa, D. J., Wilson, P. W. (2003). Kidney Disease as a Risk Factor for Development of Cardiovascular Disease: A Statement From the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108: 2154-2169 [Full text]  
• Shearer, A., Scuffham, P., Gordois, A., Oglesby, A. (2003). Predicted Costs and Outcomes From Reduced Vibration Detection in People With Diabetes in the U.S.. Diabetes Care 26: 2305-2310 [Abstract] [Full text]  
• Allen, K. V., Walker, J. D. (2003). Microalbuminuria and Mortality in Long-Duration Type 1 Diabetes. Diabetes Care 26: 2389-2391 [Abstract] [Full text]  
• Asao, K., Sarti, C., Forsen, T., Hyttinen, V., Nishimura, R., Matsushima, M., Reunanen, A., Tuomilehto, J., Tajima, N. (2003). Long-Term Mortality in Nationwide Cohorts of Childhood-Onset Type 1 Diabetes in Japan and Finland. Diabetes Care 26: 2037-2042 [Abstract] [Full text]  
• Arun, C. S., Stoddart, J., Mackin, P., MacLeod, J. M., New, J. P., Marshall, S. M. (2003). Significance of Microalbuminuria in Long-Duration Type 1 Diabetes. Diabetes Care 26: 2144-2149 [Abstract] [Full text]  
• Poulsen, L. (2003). Review: Early renal involvement in Type 1 diabetes mellitus -- Part 2: ACE inhibitor intervention in Type 1 diabetes with low grade microalbuminuria. Journal of Renin-Angiotensin-Aldosterone System 4: 17-26 [Abstract]  
• Poulsen, L. (2002). Blood pressure and cardiac autonomic function in relation to risk factors and treatment perspectives in Type 1 diabetes. Journal of Renin-Angiotensin-Aldosterone System 3: 222-242 [Abstract]  
• Hillege, H. L., Fidler, V., Diercks, G. F.H., van Gilst, W. H., de Zeeuw, D., van Veldhuisen, D. J., Gans, R. O.B., Janssen, W. M.T., Grobbee, D. E., de Jong, P. E., for the Prevention of Renal and Vascular End Stage, (2002). Urinary Albumin Excretion Predicts Cardiovascular and Noncardiovascular Mortality in General Population. Circulation 106: 1777-1782 [Abstract] [Full text]  
• Kornerup, K., Nordestgaard, B. G., Feldt-Rasmussen, B., Borch-Johnsen, K., Jensen, K. S., Jensen, J. S. (2002). Transvascular Low-Density Lipoprotein Transport in Patients With Diabetes Mellitus (Type 2): A Noninvasive In Vivo Isotope Technique. Arterioscler. Thromb. Vasc. Bio. 22: 1168-1174 [Abstract] [Full text]  
• Singh, N. (2002). Diabetes, Heart Rate, and Mortality. J CARDIOVASC PHARMACOL THER 7: 117-129 [Abstract]  
• Rossing, P., Hougaard, P., Parving, H.-H. (2002). Risk Factors for Development of Incipient and Overt Diabetic Nephropathy in Type 1 Diabetic Patients: A 10-year prospective observational study. Diabetes Care 25: 859-864 [Abstract] [Full text]  
• Canani, L. H., Ng, D. P.K., Smiles, A., Rogus, J. J., Warram, J. H., Krolewski, A. S. (2002). Polymorphism in Ecto-Nucleotide Pyrophosphatase/Phosphodiesterase 1 Gene (ENPP1/PC-1) and Early Development of Advanced Diabetic Nephropathy in Type 1 Diabetes. Diabetes 51: 1188-1193 [Abstract] [Full text]  
• Mattix, H. J., Hsu, C.-y., Shaykevich, S., Curhan, G. (2002). Use of the Albumin/Creatinine Ratio to Detect Microalbuminuria: Implications of Sex and Race. J. Am. Soc. Nephrol. 13: 1034-1039 [Abstract] [Full text]  
• Joss, N., Paterson, K. R, Deighan, C. J, Simpson, K., Boulton-Jones, J M. (2002). Vascular disease and survival in patients with type 2 diabetes and nephropathy. British Journal of Diabetes & Vascular Disease 2: 137-142 [Abstract]  
• Pedrinelli, R., Dell'Omo, G., Penno, G., Mariani, M. (2001). Non-diabetic microalbuminuria, endothelial dysfunction and cardiovascular disease. Vasc Med 6: 257-264 [Abstract]  
• Weis, U., Turner, B., Gibney, J., Watts, G.F., Burke, V., Shaw, K.M., Cummings, M.H. (2001). Long-term predictors of coronary artery disease and mortality in type 1 diabetes. QJM 94: 623-630 [Abstract] [Full text]  
• Hovind, P., Rossing, P., Tarnow, L., Toft, H., Parving, J., Parving, H.-H. (2001). Remission of Nephrotic-Range Albuminuria in Type 1 Diabetic Patients. Diabetes Care 24: 1972-1977 [Abstract] [Full text]  
• Wang, J.-G., Staessen, J. A., Fagard, R. H., Birkenhager, W. H., Gong, L., Liu, L. (2001). Prognostic Significance of Serum Creatinine and Uric Acid in Older Chinese Patients With Isolated Systolic Hypertension. Hypertension 37: 1069-1074 [Abstract] [Full text]  
• HADJADJ, S., BELLOUM, R., BOUHANICK, B., GALLOIS, Y., GUILLOTEAU, G., CHATELLIER, G., ALHENC-GELAS, F., MARRE, M. (2001). Prognostic Value of Angiotensin-I Converting Enzyme I/D Polymorphism for Nephropathy in Type 1 Diabetes Mellitus: A Prospective Study. J. Am. Soc. Nephrol. 12: 541-549 [Abstract] [Full text]  
• Iso, H., Stampfer, M. J., Manson, J. E., Rexrode, K., Hu, F. B., Hennekens, C. H., Colditz, G. A., Speizer, F. E., Willett, W. C. (2001). Prospective Study of Fat and Protein Intake and Risk of Intraparenchymal Hemorrhage in Women. Circulation 103: 856-863 [Abstract] [Full text]  
• Jensen, J. S., Feldt-Rasmussen, B., Strandgaard, S., Schroll, M., Borch-Johnsen, K. (2000). Arterial Hypertension, Microalbuminuria, and Risk of Ischemic Heart Disease. Hypertension 35: 898-903 [Abstract] [Full text]  
• GAMBARO, G., VAN DER WOUDE, F. J. (2000). Glycosaminoglycans: Use in Treatment of DiabeticNephropathy. J. Am. Soc. Nephrol. 11: 359-368 [Full text]  
• Borch-Johnsen, K., Feldt-Rasmussen, B., Strandgaard, S., Schroll, M., Jensen, J. S. (1999). Urinary Albumin Excretion : An Independent Predictor of Ischemic Heart Disease. Arterioscler. Thromb. Vasc. Bio. 19: 1992-1997 [Abstract] [Full text]  
• Benzie, I. F.F., Chung, W.-y., Tomlinson, B. (1999). Simultaneous Measurement of Allantoin and Urate in Plasma: Analytical Evaluation and Potential Clinical Application in Oxidant:Antioxidant Balance Studies. Clin. Chem. 45: 901-904 [Full text]  
• Kanters, S. D., Banga, J.-D., Stolk, R. P, Algra, A. (1999). Incidence and determinants of mortality and cardiovascular events in diabetes mellitus: a meta-analysis. Vasc Med 4: 67-75 [Abstract]  
• WALSER, M., HILL, S. (1999). Can Renal Replacement Be Deferred by a Supplemented Very Low Protein Diet?. J. Am. Soc. Nephrol. 10: 110-116 [Abstract] [Full text]  
• Clausen, P., Jensen, J. S., Borch-Johnsen, K., Jensen, G., Feldt-Rasmussen, B. (1998). Ambulatory Blood Pressure and Urinary Albumin Excretion in Clinically Healthy Subjects. Hypertension 32: 71-77 [Abstract] [Full text]