Arteriosclerosis, Thrombosis, and Vascular Biology. 1999;19:1992-1997
© 1999 American Heart Association, Inc.
Atherosclerosis and Lipoproteins |
Urinary Albumin Excretion
An Independent Predictor of Ischemic Heart Disease
From the Centre of Preventive Medicine, Glostrup University Hospital, Glostrup (K.B.-J., M.S., J.S.J.); the Department of Nephrology, Rigshospitalet, University Hospital (B.F.-R.); and the Department of Nephrology, Herlev University Hospital, Herlev (S.S.), Denmark.
Correspondence to Chief Physician Knut Borch-Johnsen, MD, MSc, Steno Diabetes Centre, Niels Steensensvej 2, DK-2820 Gentofte, Denmark. E-mail kbjo{at}novo.dk
Abstract—Cross-sectional studies suggest that an increased urinary albumin excretion rate is associated with cardiovascular disease, dyslipidemia, and hypertension. The purpose of this study was to analyze prospectively whether the urinary albumin-to -creatinine (A/C) ratio can independently predict ischemic heart disease (IHD) in a population-based cohort. In 1983, urinary albumin and creatinine levels were measured, along with the conventional atherosclerotic risk factors, in 2085 consecutive participants without IHD, renal disease, urinary tract infection, or diabetes mellitus. The participants were followed up until death, emigration, or December 31, 1993. IHD was defined as a hospital discharge diagnosis or cause of death including the diagnoses ICD-8 and 410 to 414. Seventy-nine individuals developed IHD during the 21 130 person-years of follow-up. They were characterized by a preponderance of males and higher age, body mass index, blood pressure, lipoproteins, and proportion of current smokers. Microalbuminuria was defined as an A/C ratio) >90 percentile (>0.65 mg/mmol). When adjusted for other risk factors, the relative risk of IHD associated with microalbuminuria was 2.3 (95% CI, 1.3 to 3.9, P=0.002), and the 10-year disease-free survival decreased from 97% to 91% (P<0.0001) when microalbuminuria was present. An interaction between microalbuminuria and smoking was observed, and the presence of microalbuminuria more than doubled the predictive effect of the conventional atherosclerotic risk factors for development of IHD. It is concluded that microalbuminuria is not only an independent predictor of IHD but also substantially increases the risk associated with other established risk factors.
Key Words: urinary albumin excretion • microalbuminuria • ischemic heart disease • atherosclerosis
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|
|
|
|
|
|
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|
|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 M. F Yuyun, K.-T. Khaw, R. Luben, A. Welch, S. Bingham, N. E Day, and N. J Wareham Microalbuminuria independently predicts all-cause and cardiovascular mortality in a British population: The European Prospective Investigation into Cancer in Norfolk (EPIC-Norfolk) population study Int. J. Epidemiol., February 1, 2004; 33(1): 189 - 198. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
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|
|
|
|
|
|
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|
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|
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|
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