 |
|
Low Ankle-Brachial Index Associated With Rise in Creatinine Level Over Time
Results From the Atherosclerosis Risk in Communities Study
Ann M. O’Hare, MA, MD;
Rudolph A. Rodriguez, MD;
Peter Bacchetti, PhD
Arch Intern Med. 2005;165:1481-1485.
ABSTRACT
| |
Background A low ankle-brachial index (ABI) predicts risk of cardiovascular death, myocardial infarction, peripheral arterial disease events, and stroke. However, it is unknown whether a low ABI also predicts a decline in renal function.
Methods We examined the association between ABI and change in serum creatinine level over time among 13 655 participants in the Atherosclerosis Risk in Communities (ARIC) study who underwent serum creatinine and ABI measurement at baseline and also underwent serum creatinine measurement 3 years later at the second study visit. The study outcome was a 50% rise in serum creatinine level from baseline to the second study visit.
Results Overall, 0.48% of participants with an ABI of 1 or higher, 0.9% of participants with an ABI between 0.9 and 0.99, and 2.16% of participants with an ABI lower than 0.9 experienced a 50% or greater increase in serum creatinine level. In multivariate analysis, participants with an ABI lower than 0.9 were still more than twice as likely as those in the referent category (ABI  1) to experience an increase in serum creatinine level (odds ratio 2.5; 95% confidence interval, 1.1-5.7) (P = .04), and a linear trend in the incidence of worsening renal function was noted across ABI categories (P = .02). Analyses excluding participants with renal insufficiency, diabetes, and hypertension at baseline all produced similar results.
Conclusion In addition to known associations of the ABI with stroke, myocardial infarction, peripheral arterial disease events, and cardiovascular death, a low ABI also predicts an increase in serum creatinine level over time.
INTRODUCTION
The prevalence and incidence of cardiovascular disease are both high among those with renal insufficiency,1-10 and chronic kidney disease and cardiovascular disease share many of the same risk factors.11-22 However, the contribution of preexisting cardiovascular disease to progression of renal disease has not been examined in detail.
We hypothesized that a low ankle-brachial index (ABI)—a marker for both lower extremity and more generalized atherosclerotic disease23 and a known predictor of cardiovascular death, myocardial infarction, peripheral arterial disease events, and stroke24-28—would also be associated with a decline in renal function over time. We tested this hypothesis using publicly available data from the first and second study visits of the Atherosclerosis Risk in Communities (ARIC) study.29
METHODS
The ARIC study29 was a prospective cohort study of cardiovascular disease among a community sample of middle-aged residents of Jackson, Miss; Forsyth County, North Carolina; Washington County, Maryland; and several suburbs of Minneapolis, Minn. The study consisted of 15 792 men and women aged 45 to 64 years at baseline. Participant recruitment and baseline data collection were completed between 1987 and 1989, and participants subsequently returned for 3 visits, each spaced 3 years apart. The present analysis uses publicly available data from the first and second study visits and was approved by the institutional review board at the University of California, San Francisco.
OUTCOME MEASURE AND PREDICTOR VARIABLES
The primary predictor variable for the present analysis was ABI at the first study visit. The ABI is the ratio of systolic blood pressure at the ankle to systolic blood pressure at the brachial artery. Ankle and brachial systolic blood pressure measurements were ascertained using the Dinamap 1846 SX (Critixon, Tampa, Fla). Ankle blood pressure was measured at the posterior tibial artery in one leg. Two measurements were taken 5 to 8 minutes apart while the participant was in the prone position. Brachial artery systolic blood pressure measurements were taken 5 minutes apart with the participant in the supine position. The ABI was computed by dividing the average of the 2 ankle systolic blood pressure measurements by the average of the first 2 brachial readings. For the purposes of this analysis, we divided ABI measurements into 3 categories at the clinically established cutoffs of 0.9 and 1.0.30
The outcome measure for the present analysis was the occurrence of at least a 50% rise in serum creatinine level between baseline and the first follow-up visit approximately 3 years later. Too few participants experienced a doubling of serum creatinine level (a more conventional measure of renal functional decline) during follow-up for this to be used as an outcome. Regardless of initial creatinine level, a 50% increase in serum creatinine level translates into an approximately 25% decrease in creatinine clearance. This outcome is more easily interpreted than either a fixed increase in serum creatinine level or a fixed decrease in estimated creatinine clearance or glomerular filtration rate. The correlation between fixed increases in serum creatinine level and creatinine clearance is highly variable, depending on the initial creatinine level, and since values can be very inflated in patients with normal renal function, fixed decrements over time in calculated creatinine clearance or glomerular filtration rate may be misleading.
Our analysis was adjusted for the following covariates ascertained at visit 1: demographic characteristics (age, race [black vs nonblack], and sex), baseline Cockcroft-Gault–estimated creatinine clearance,31 comorbid conditions including diabetes (previously diagnosed or fasting glucose level 126 mg/dL [6.99 mmol/L]), smoking behavior (participants were classified as current smokers, former smokers, or nonsmokers), body mass index, fasting lipid levels (low-density lipoprotein [LDL], high-density lipoprotein [HDL], and triglyceride levels), alcohol use, hematocrit values, mean systolic and diastolic blood pressures, and educational level (college vs no college). To account for the slight differences in follow-up time from visit 1 to visit 2 between study participants, exact follow-up time was also included in the multivariable analysis.
STATISTICAL ANALYSIS
All statistical analyses were performed using STATA statistical software (College Station, Tex). We compared baseline characteristics (ascertained at visit 1) across ABI categories. Normally distributed continuous variables were compared using the t test; nonnormally distributed variables (eg, triglyceride levels) were compared using the Mann-Whitney U test; and categorical variables were compared using the  2 test. For all analyses, participants with an ABI of 1 or higher served as the referent category with which the other groups were compared. The association of ABI with worsening renal function was measured using bivariate and multivariate logistic regression analysis. We checked the linearity assumption for numeric predictors by including log-transformed and quadratic terms and breaking the predictor into quartiles. To satisfy the linearity assumption, triglyceride levels, systolic blood pressure, and hematocrit values were log transformed, and estimated creatinine clearance was modeled by quartile. We tested for the presence of a linear trend in the odds of a 50% increase in creatinine level across ABI categories by incorporating the categorical ABI variable into the logistic regression analysis as a numeric variable (scored 0-1-2).
SENSITIVITY ANALYSES
We confirmed the presence of an association between low ABI and the study outcome after excluding, one group at a time, participants with an estimated creatinine clearance lower than 60 mL/min, diabetes, and hypertension (defined as either a mean systolic blood pressure of 140 mm Hg, a mean diastolic blood pressure of 90 mm Hg, or use of antihypertensive medication). To evaluate the impact of possible measurement error for serum creatinine on our results, we performed a companion analysis in which we defined the outcome as a 50% rise in serum creatinine level with an absolute rise in creatinine level of at least 0.4 mg/dL (35.4 µmol/L).14 This analysis was designed to ignore small increases in serum creatinine level occurring among cohort patients with low baseline serum creatinine levels that might be due solely to measurement error.
RESULTS
A total of 13 655 ARIC participants29 underwent creatinine and ABI measurement at visit 1 and creatinine measurement again at visit 2. Among these, 12 179 participants (89%) had an ABI of 1 or higher; 1105 (8%) had an ABI between 0.9 and 0.99; and 371 (3%) had an ABI lower than 0.9. Compared with the referent category of participants with an ABI of 1 or higher, the mean serum creatinine level was similar, but mean creatinine clearance was slightly lower among those with an ABI lower than 0.9 (Table 1). The relationship between baseline creatinine clearance and ABI was nonlinear: a disproportionate number of participants in the lowest and highest quartiles of creatinine clearance had low ABIs (Figure).
|
|
|
|
Table 1. Baseline Characteristics by Ankle-Brachial Index (ABI)*
|
|
|
Compared with participants with an ABI of 1 or higher, those with an ABI lower than 0.9 were older; included a higher percentage of women, blacks, and persons with diabetes; had lower HDL and higher LDL and triglyceride levels; had a slightly lower mean BMI; included a smaller percentage of alcohol users and college graduates and a higher percentage of current smokers; had a higher mean systolic blood pressure and lower mean diastolic blood pressure; and included a higher percentage of participants using antihypertensive medications (Table 1). Overall, serum creatinine level increased in 0.56% of participants (n = 76): 0.48% of those with an ABI of 1 or higher (n = 58), 0.9% of those with an ABI between 0.9 and 0.99 (n = 10), and 2.16% of those with an ABI lower than 0.9 (n = 8). Baseline serum creatinine levels were not significantly different among patients who did and did not experience a 50% rise in serum creatinine level (median creatinine level, 1 mg/dL [88.4 µmol/L] with 25th-75th percentile range, 0.8-1.4 mg/dL [123.8 µmol/L] vs 1.1 mg/dL [97.2 µmol/L] with 25th-75th percentile range, 1.1-1.2 mg/dL [97.2-106.1 µmol/L]) (P = .36). In both bivariate and multivariate analyses, an ABI lower than 0.9 was associated with an increase in serum creatinine level during follow-up, and there was a linear trend across ABI categories (Table 2).
|
|
|
|
Table 2. Association of Baseline Ankle-Brachial Index (ABI) With Worsening Renal Function During Follow-up
|
|
|
Results were similar after exclusion, one group at a time, of those with an estimated clearance lower than 60 mL/min (odds ratio [OR], 2.6; 95% confidence interval [CI], 1.04-6.61) (P = .04), diabetes (OR, 3.5; 95% CI, 1.2-10.5) (P = .03), and hypertension or use of antihypertensive medications (OR, 5.5; 95% CI, 1.4-21.4) (P = .02) at baseline. When we defined the outcome as a 50% rise in serum creatinine level with at least a 0.4 mg/dL (35.4 µmol/L) absolute increase in serum creatinine level (n = 66), the results did not differ substantially from the primary analysis: patients with an ABI lower than 0.9 still had a more than 2-fold adjusted risk of this outcome compared with the referent category (OR, 2.3; 95% CI, 0.92-5.8) (P = .07), and there was a trend across ABI categories (P = .03).
COMMENT
The present study demonstrates that, in addition to its previously demonstrated associations with stroke, myocardial infarction, peripheral arterial disease events, and cardiovascular death,24-28 a low ABI is also associated with an increase in serum creatinine level over time. Participants with an ABI lower than 0.9 had more than 4-fold odds of experiencing a 50% rise in creatinine level compared with those with an ABI of 1 or higher, and the association persisted after adjustment for known predictors of renal functional decline. Because a low ABI is a specific measure of overall atherosclerotic burden,23, 32-34 the existence of an association between baseline ABI and subsequent increase in serum creatinine supports the notion that preexisting atherosclerosis may be a risk factor for deterioration of renal function over time. Furthermore, the strong association of ABI with a rise in serum creatinine level in both unadjusted and adjusted analysis highlights the possible importance of ABI measurement as a means to identify patients at greatest risk for deterioration of renal function over time.
Many studies have reported both cross-sectional and longitudinal associations between baseline renal insufficiency and coronary, cerebral, and peripheral arterial disease.1-9,35 There is also extensive research exploring possible causal mechanisms for an association between renal insufficiency and cardiovascular disease. For example, hyperhomocysteinemia, oxidant stress, elevated levels of lipoprotein(a) and inflammatory markers, and disordered calcium phosphorous metabolism all represent potential pathways for accelerated atherosclerosis in patients with renal insufficiency.36
There has been much less interest in the reverse association: the contribution of atherosclerosis to progression of renal disease. Using baseline data on screenees for the Multiple Risk Factor Intervention Trial (MRFIT), Klag et al12 reported that a history of myocardial infarction was independently associated with an increased risk of end-stage renal disease, though this was not the primary focus of the analysis. Levin et al37 found that among patients with existing chronic kidney disease, the presence of cardiovascular disease predicted time to onset of end-stage renal disease. Bleyer et al22 described a positive independent association between maximum carotid intimal thickness and subsequent rise in serum creatinine level of at least 0.3 mg/dL (26.5 µmol/L) over a 3- to 4-year period among subjects without diabetes enrolled in the Cardiovascular Health Study. Finally, a recent study by McClellan et al38 demonstrated a high rate of progression to end-stage renal disease among Medicare beneficiaries hospitalized for congestive heart failure and for acute myocardial infarction.
Data from several autopsy series also lend some support to the notion that systemic atherosclerosis may predispose to renal insufficiency. Among persons free of clinical renal disease and renal artery stenosis, the prevalence of glomerulosclerosis was noted to be higher among those with moderate to severe intrarenal atherosclerosis than among those with mild atherosclerosis.39 In a second autopsy series of persons aged 25 to 54 years, renal arteriolar hyalinization was correlated with raised lesions in the coronary arteries and aorta.40
While the association reported herein between low ABI and rising creatinine level may reflect a shared risk factor profile between renal disease and atherosclerosis,41 we were not able to explain away this association by controlling for many of the known risk factors for renal disease. Because the kidney is a highly vascular organ whose function is dependent on an intact circulatory system, it makes intuitive sense that systemic atherosclerotic disease could be causally associated with declining renal function. Based on our findings and the aforementioned studies, we would argue that systemic atherosclerosis may be a risk factor for renal insufficiency as it is for myocardial infarction, stroke, and peripheral arterial disease events.
A limitation of the present study is that our definition of worsening renal function may be inaccurate owing to changes in patient age and muscle mass over time. While measured changes in creatinine clearance would probably be the best way to identify those with declining renal function, these data were not collected in ARIC.29 Alternate measures of declining renal function such as fixed changes in serum creatinine level, calculated clearance, or glomerular filtration rate are less clearly interpretable than a percentage change in serum creatinine level. Finally, we were unable to use incidence of new onset of renal insufficiency (defined as incidence of a calculated creatinine clearance of <60 mL/min) among patients experiencing a 50% increase in serum creatinine level because of the rarity of this outcome (n = 41) over the short follow-up period. Thus, in the absence of measured creatinine clearance, we believe that our definition of worsening renal function as a percentage rise in serum creatinine level represents the most appropriate choice.
A second limitation is that our analysis did not include detailed information on the severity of important confounding comorbid conditions such as diabetes and hypertension. However, it is somewhat reassuring that even after excluding participants with diabetes or hypertension at baseline, a low ABI was still strongly associated with the study outcome.
Finally, declining renal function was a relatively uncommon outcome in this sample of middle-aged community-dwelling adults. Therefore, the clinical importance of ABI measurement as a predictor of declining renal function would be best assessed in populations where worsening renal function is a more common outcome.
In conclusion, a low ABI is predictive not just of recognized atherosclerotic events such as stroke, myocardial infarction, peripheral arterial disease events, and cardiovascular death, but also of rising creatinine level over time. These findings support the notion of systemic atherosclerosis as a risk factor for decline in renal function and also highlight the possible importance of ABI measurement as a means to identify patients at greatest risk for deterioration of renal function over time.
AUTHOR INFORMATION
Correspondence: Ann M. O'Hare, MA, MD, Veterans Affairs Medical Center, Box 111J (Nephrology), 4150 Clement St, San Francisco, CA 94121 (Ann.O'Hare{at}med.va.gov).
Accepted for Publication: November 3, 2004.
Funding/Support: Dr O'Hare is supported by a Career Development Award from the Department of Veterans Affairs Health Services Research and Development Service, Washington, DC.
Financial Disclosure: None.
Author Affiliations: Departments of Medicine (Drs O’Hare and Rodriguez) and Epidemiology and Biostatistics (Dr Bacchetti), University of California, and Departments of Medicine, Veterans Affairs Medical Center (Dr O’Hare) and San Francisco General Hospital (Dr Rodriguez), San Francisco, Calif.
REFERENCES
| |
1. Fried LF, Shlipak MG, Crump C, et al. Renal insufficiency as a predictor of cardiovascular outcomes and mortality in elderly individuals. J Am Coll Cardiol. 2003;41:1364-1372.
FREE FULL TEXT
2. Garg AX, Clark WF, Haynes RB, House AA. Moderate renal insufficiency and the risk of cardiovascular mortality: results from the NHANES I. Kidney Int. 2002;61:1486-1494.
FULL TEXT
|
ISI
| PUBMED
3. Manjunath G, Tighiouart H, Coresh J, et al. Level of kidney function as a risk factor for cardiovascular outcomes in the elderly. Kidney Int. 2003;63:1121-1129.
FULL TEXT
|
ISI
| PUBMED
4. Muntner P, He J, Hamm L, Loria C, Whelton PK. Renal insufficiency and subsequent death resulting from cardiovascular disease in the United States. J Am Soc Nephrol. 2002;13:745-753.
FREE FULL TEXT
5. Shlipak MG, Simon JA, Grady D, Lin F, Wenger NK, Furberg CD. Renal insufficiency and cardiovascular events in postmenopausal women with coronary heart disease. J Am Coll Cardiol. 2001;38:705-711.
FREE FULL TEXT
6. O'Hare AM, Vittinghoff E, Hsia J, Shlipak MG. Renal insufficiency and the risk of lower extremity peripheral arterial disease: results from the Heart and Estrogen/Progestin Replacement Study (HERS). J Am Soc Nephrol. 2004;15:1046-1051.
FREE FULL TEXT
7. Weiner DE, Tighiouart H, Amin MG, et al. Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: a pooled analysis of community-based studies. J Am Soc Nephrol. 2004;15:1307-1315.
FREE FULL TEXT
8. O'Hare AM, Glidden DV, Fox CS, Hsu CY. High prevalence of peripheral arterial disease in persons with renal insufficiency: results from the National Health and Nutrition Examination Survey 1999-2000. Circulation. 2004;109:320-323.
FREE FULL TEXT
9. Mann JF, Gerstein HC, Pogue J, Bosch J, Yusuf S. Renal insufficiency as a predictor of cardiovascular outcomes and the impact of ramipril: the HOPE randomized trial. Ann Intern Med. 2001;134:629-636.
FREE FULL TEXT
10. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351:1296-1305.
FREE FULL TEXT
11. Brancati FL, Whelton PK, Randall BL, Neaton JD, Stamler J, Klag MJ. 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;278:2069-2074.
FREE FULL TEXT
12. Klag MJ, Whelton PK, Randall BL, et al. Blood pressure and end-stage renal disease in men. N Engl J Med. 1996;334:13-18.
FREE FULL TEXT
13. Klag MJ, Whelton PK, Randall BL, Neaton JD, Brancati FL, Stamler J. End-stage renal disease in African-American and white men: 16-year MRFIT findings. JAMA. 1997;277:1293-1298.
FREE FULL TEXT
14. Muntner P, Coresh J, Smith JC, Eckfeldt J, Klag MJ. Plasma lipids and risk of developing renal dysfunction: the atherosclerosis risk in communities study. Kidney Int. 2000;58:293-301.
FULL TEXT
|
ISI
| PUBMED
15. Young JH, Klag MJ, Muntner P, Whyte JL, Pahor M, Coresh J. Blood pressure and decline in kidney function: findings from the Systolic Hypertension in the Elderly Program (SHEP). J Am Soc Nephrol. 2002;13:2776-2782.
FREE FULL TEXT
16. Haroun MK, Jaar BG, Hoffman SC, Comstock GW, Klag MJ, Coresh J. Risk factors for chronic kidney disease: a prospective study of 23,534 men and women in Washington County, Maryland. J Am Soc Nephrol. 2003;14:2934-2941.
FREE FULL TEXT
17. Perneger TV, Brancati FL, Whelton PK, Klag MJ. End-stage renal disease attributable to diabetes mellitus. Ann Intern Med. 1994;121:912-918.
FREE FULL TEXT
18. Perneger TV, Whelton PK, Klag MJ. Race and end-stage renal disease: socioeconomic status and access to health care as mediating factors. Arch Intern Med. 1995;155:1201-1208.
FREE FULL TEXT
19. Perneger TV, Whelton PK, Puddey IB, Klag MJ. Risk of end-stage renal disease associated with alcohol consumption. Am J Epidemiol. 1999;150:1275-1281.
FREE FULL TEXT
20. Goetz FC, Jacobs DR Jr, Chavers B, Roel J, Yelle M, Sprafka JM. Risk factors for kidney damage in the adult population of Wadena, Minnesota: a prospective study. Am J Epidemiol. 1997;145:91-102.
FREE FULL TEXT
21. Fox CS, Larson MG, Leip EP, Culleton B, Wilson PW, Levy D. Predictors of new-onset kidney disease in a community-based population. JAMA. 2004;291:844-850.
FREE FULL TEXT
22. Bleyer AJ, Shemanski LR, Burke GL, Hansen KJ, Appel RG. Tobacco, hypertension, and vascular disease: risk factors for renal functional decline in an older population. Kidney Int. 2000;57:2072-2079.
FULL TEXT
|
ISI
| PUBMED
23. Zheng ZJ, Sharrett AR, Chambless LE, et al. Associations of ankle-brachial index with clinical coronary heart disease, stroke and preclinical carotid and popliteal atherosclerosis: the Atherosclerosis Risk in Communities (ARIC) Study. Atherosclerosis. 1997;131:115-125.
FULL TEXT
|
ISI
| PUBMED
24. Leng GC, Fowkes FG, Lee AJ, Dunbar J, Housley E, Ruckley CV. Use of ankle brachial pressure index to predict cardiovascular events and death: a cohort study. BMJ. 1996;313:1440-1444.
25. Newman AB, Shemanski L, Manolio TA, et al. Ankle-arm index as a predictor of cardiovascular disease and mortality in the Cardiovascular Health Study. Arterioscler Thromb Vasc Biol. 1999;19:538-545.
FREE FULL TEXT
26. Abbott RD, Rodriguez BL, Petrovitch H, et al. Ankle-brachial blood pressure in elderly men and the risk of stroke: the Honolulu Heart Program. J Clin Epidemiol. 2001;54:973-978.
FULL TEXT
|
ISI
| PUBMED
27. Murabito JM, Evans JC, Larson MG, Nieto K, Levy D, Wilson PW. The ankle-brachial index in the elderly and risk of stroke, coronary disease, and death: the Framingham Study. Arch Intern Med. 2003;163:1939-1942.
FREE FULL TEXT
28. Tsai AW, Folsom AR, Rosamond WD, Jones DW. Ankle-brachial index and 7-year ischemic stroke incidence: the ARIC study. Stroke. 2001;32:1721-1724.
FREE FULL TEXT
29. The ARIC Investigators. The Atherosclerosis Risk in Communities (ARIC) Study: design and objectives. Am J Epidemiol. 1989;129:687-702.
FREE FULL TEXT
30. Sacks D, Bakal CW, Beatty PT, et al. Position statement on the use of the ankle-brachial index in the evaluation of patients with peripheral vascular disease: a consensus statement developed by the standards division of the society of cardiovascular & interventional radiology. J Vasc Interv Radiol. 2002;13:353.
ISI
| PUBMED
31. Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron. 1976;16:31-41.
ISI
| PUBMED
32. Newman AB, Siscovick DS, Manolio TA, et al. Ankle-arm index as a marker of atherosclerosis in the Cardiovascular Health Study. Circulation. 1993;88:837-845.
FREE FULL TEXT
33. Otah KE, Madan A, Otah E, Badero O, Clark LT, Salifu MO. Usefulness of an abnormal ankle-brachial index to predict presence of coronary artery disease in African-Americans. Am J Cardiol. 2004;93:481-483.
FULL TEXT
|
ISI
| PUBMED
34. Aronow WS, Ahn C. Prevalence of coexistence of coronary artery disease, peripheral arterial disease, and atherothrombotic brain infarction in men and women 62 years of age. Am J Cardiol. 1994;74:64-65.
FULL TEXT
|
ISI
| PUBMED
35. Shlipak MG, Fried LF, Crump C, et al. Cardiovascular disease risk status in elderly persons with renal insufficiency. Kidney Int. 2002;62:997-1004.
FULL TEXT
|
ISI
| PUBMED
36. Zoccali C, Mallamaci F, Tripepi G. Traditional and emerging cardiovascular risk factors in end-stage renal disease. Kidney Int Suppl. 2003;Jun:S105-S110.
37. Levin A, Djurdjev O, Barrett B, et al. Cardiovascular disease in patients with chronic kidney disease: getting to the heart of the matter. Am J Kidney Dis. 2001;38:1398-1407.
ISI
| PUBMED
38. McClellan WM, Langston RD, Presley R. Medicare patients with cardiovascular disease have a high prevalence of chronic kidney disease and a high rate of progression to end-stage renal disease. J Am Soc Nephrol. 2004;15:1912-1919.
FREE FULL TEXT
39. Kasiske BL. Relationship between vascular disease and age-associated changes in the human kidney. Kidney Int. 1987;31:1153-1159.
ISI
| PUBMED
40. Tracy RE, Strong JP, Newman WP III, Malcom GT, Oalmann MC, Guzman MA. Renovasculopathies of nephrosclerosis in relation to atherosclerosis at ages 25 to 54 years. Kidney Int. 1996;49:564-570.
ISI
| PUBMED
41. Sarnak MJ, Levey AS, Schoolwerth AC, et al. 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. 2003;108:2154-2169.
FREE FULL TEXT
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati
What's this?
RELATED LETTERS
Systemic Atherosclerosis and Kidney Disease
Abhijit V. Kshirsagar and Romulo E. Colindres
Arch Intern Med. 2006;166(2):250.
EXTRACT
| FULL TEXT
Systemic Atherosclerosis and Kidney Disease—Reply
Ann M. O’Hare, Rudolph A. Rodriguez, and Peter Bacchetti
Arch Intern Med. 2006;166(2):250.
EXTRACT
| FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
|
A Simple Algorithm to Predict Incident Kidney Disease
Kshirsagar et al.
Arch Intern Med 2008;168:2466-2473.
ABSTRACT
| FULL TEXT
Combined Effect of Chronic Kidney Disease and Peripheral Arterial Disease on All-Cause Mortality in a High-Risk Population
Liew et al.
CJASN 2008;3:1084-1089.
ABSTRACT
| FULL TEXT
Cardiovascular Disease and Subsequent Kidney Disease
Elsayed et al.
Arch Intern Med 2007;167:1130-1136.
ABSTRACT
| FULL TEXT
Lower Progression Rate of End-Stage Renal Disease in Patients with Peripheral Arterial Disease Using Statins or Angiotensin-Converting Enzyme Inhibitors
Feringa et al.
J. Am. Soc. Nephrol. 2007;18:1872-1879.
ABSTRACT
| FULL TEXT
Systemic Atherosclerosis and Kidney Disease
Kshirsagar and Colindres
Arch Intern Med 2006;166:250-250.
FULL TEXT
Systemic Atherosclerosis and Kidney Disease--Reply
O'Hare et al.
Arch Intern Med 2006;166:250-250.
FULL TEXT
|
64; second quartile, 65 to 75; third quartile, 76 to 89; fourth quartile,