Chronic Kidney Disease and the Risks of Death, Cardiovascular Events, and Hospitalization

doi:10.1056/NEJMoa041031

Volume 351:1296-1305		September 23, 2004		Number 13

Chronic Kidney Disease and the Risks of Death, Cardiovascular Events, and Hospitalization

Alan S. Go, M.D., Glenn M. Chertow, M.D., M.P.H., Dongjie Fan, M.S.P.H., Charles E. McCulloch, Ph.D., and Chi-yuan Hsu, M.D.

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ABSTRACT

Background End-stage renal disease substantially increases therisks of death, cardiovascular disease, and use of specializedhealth care, but the effects of less severe kidney dysfunctionon these outcomes are less well defined.

Methods We estimated the longitudinal glomerular filtrationrate (GFR) among 1,120,295 adults within a large, integratedsystem of health care delivery in whom serum creatinine hadbeen measured between 1996 and 2000 and who had not undergonedialysis or kidney transplantation. We examined the multivariableassociation between the estimated GFR and the risks of death,cardiovascular events, and hospitalization.

Results The median follow-up was 2.84 years, the mean age was52 years, and 55 percent of the group were women. After adjustment,the risk of death increased as the GFR decreased below 60 mlper minute per 1.73 m² of body-surface area: the adjusted hazardratio for death was 1.2 with an estimated GFR of 45 to 59 mlper minute per 1.73 m² (95 percent confidence interval, 1.1to 1.2), 1.8 with an estimated GFR of 30 to 44 ml per minuteper 1.73 m² (95 percent confidence interval, 1.7 to 1.9), 3.2with an estimated GFR of 15 to 29 ml per minute per 1.73 m²(95 percent confidence interval, 3.1 to 3.4), and 5.9 with anestimated GFR of less than 15 ml per minute per 1.73 m² (95percent confidence interval, 5.4 to 6.5). The adjusted hazardratio for cardiovascular events also increased inversely withthe estimated GFR: 1.4 (95 percent confidence interval, 1.4to 1.5), 2.0 (95 percent confidence interval, 1.9 to 2.1), 2.8(95 percent confidence interval, 2.6 to 2.9), and 3.4 (95 percentconfidence interval, 3.1 to 3.8), respectively. The adjustedrisk of hospitalization with a reduced estimated GFR followeda similar pattern.

Conclusions An independent, graded association was observedbetween a reduced estimated GFR and the risk of death, cardiovascularevents, and hospitalization in a large, community-based population.These findings highlight the clinical and public health importanceof chronic renal insufficiency.

More than 400,000 Americans have end-stage renal disease, andover 300,000 of these patients require maintenance dialysis.¹Mortality rates remain above 20 percent per year with the useof dialysis, with more than half of the deaths related to cardiovasculardisease. The annual direct medical costs for end-stage renaldisease are nearly $23 billion.¹ Although an estimated 8 millionadults in the United States have chronic kidney disease of atleast stage 3 (as defined by an estimated glomerular filtrationrate [GFR] of less than 60 ml per minute per 1.73 m² of body-surfacearea),² less is known about the rates of death, cardiovasculardisease, and resource use among persons with a reduced estimatedGFR who are not yet receiving maintenance dialysis.

Several, but not all, previous studies suggested that mild-to-moderateelevations in serum creatinine levels are associated with increasedrates of death from any cause³^,⁴^,⁵^,⁶^,⁷^,⁸^,⁹ and from cardiovascularcauses,⁵^,⁷^,¹⁰^,¹¹^,¹²^,¹³ but whether chronic kidney disease independentlyincreases the risk of any type of cardiovascular disease hasnot been established.⁴^,⁵^,⁶^,⁷^,¹⁴ Furthermore, previous studieshave been limited by the inclusion of relatively small numbersof persons with kidney disease,³^,⁴^,⁵^,⁶^,⁷^,⁸^,¹¹^,¹²^,¹³^,¹⁴^,¹⁵^,¹⁶^,¹⁷the use of dichotomous groups of estimated kidney function,³^,⁴^,⁵^,⁶^,⁷^,⁸^,¹⁵the use of the serum creatinine level alone as a proxy for GFRand nonuniform cutoff values to define kidney disease,³^,⁴^,⁵^,⁶^,⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹⁵lack of information on longitudinal changes in GFR and coexistingconditions,³^,⁴^,⁵^,⁶^,⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹⁴^,¹⁵^,¹⁶^,¹⁷ selected populations,⁶^,⁸^,¹¹^,¹⁴^,¹⁶and populations with limited racial or ethnic diversity. Inaddition, few studies have investigated the association betweenchronic kidney disease and the risk of hospitalization,¹⁸ whichhas important economic implications.

Using longitudinal measures of estimated GFR, a more accuratemethod of assessing kidney function than the measurement ofserum creatinine alone, we examined the effect of the severityof kidney dysfunction on the risks of death, cardiovascularevents, and hospitalization among a large, diverse group ofadults. We hypothesized that there would be a graded, independentassociation between the estimated GFR and the risks of theseoutcomes.

Methods

Study Sample and Measures of Kidney Function

The Kaiser Permanente Renal Registry included all adult members(20 years of age or older) of Kaiser Permanente of NorthernCalifornia, a large integrated health care system insuring morethan 35 percent of the adult population of the San FranciscoBay Area, whose kidney function was known. To be eligible forthe registry, the subjects had to have had one or more outpatientdeterminations of serum creatinine levels recorded in a health-planlaboratory database between January 1, 1996, and December 31,2000. We excluded subjects who had already received a kidneytransplant or who were receiving maintenance dialysis at entry.Given the nature of the study, the institutional review boardof the Kaiser Foundation Research Institute determined thatinformed consent was not required.

We used the abbreviated Modification of Diet in Renal Disease(MDRD) equation to estimate the GFR.¹⁹^,²⁰ We calibrated themeasurement of serum creatinine by the Kaiser regional laboratoryagainst that of the MDRD core laboratory.²¹ The date of thefirst measurement of GFR during the study period was consideredthe subject's index date (baseline). Changes in GFR during follow-upwere estimated from serum creatinine determinations not associatedwith hospitalizations to reflect more accurately stable estimatesof kidney function. We used a modified National Kidney Foundationclassification of chronic kidney disease,²² which classifiesestimated GFR in the following ranges: at least 60 ml per minuteper 1.73 m², 45 to 59 ml per minute per 1.73 m² (stage 3a),30 to 44 ml per minute per 1.73 m² (stage 3b), 15 to 29 ml perminute per 1.73 m² (stage 4), and less than 15 ml per minuteper 1.73 m² (stage 5).

Characteristics of the Subjects

Data on age, sex, and racial or ethnic group were obtained fromhealth-plan databases. All names and identifiers were removedbefore any data were analyzed, according to procedures approvedby the institutional review board at Kaiser.

We identified coexisting illnesses using validated methods²³^,²⁴^,²⁵^,²⁶based on health-plan databases for hospitalization-dischargediagnoses, ambulatory diagnoses, laboratory results, and medicationprescriptions, as well as regional cancer-registry data²⁴ (diagnosticcriteria are listed in the Appendix). These diagnoses includedcoronary disease, stroke or transient ischemic attack, heartfailure, peripheral arterial disease, diabetes mellitus, hypertension,dyslipidemia, lung or liver disease, cancer, and dementia. Wealso evaluated laboratory-database entries for serum albuminto identify subjects with a value of 3.5 g per deciliter orless. The presence of proteinuria was based on laboratory-databaseentries of urine dipstick results of 1+ or greater (approximately30 mg per deciliter or greater) in the absence of a possibleurinary tract infection (i.e., concomitant positive test forurinary nitrite or esterase).

Socioeconomic status was assigned with the use of 2000 U.S.Census-block data, which generally correspond to city blocksor neighborhoods.²⁸ Subjects with a low income were definedas those living in a Census-block group with a median annualhousehold income under $35,000, and those with a low level ofeducation were categorized as those living in a Census-blockgroup in which more than 25 percent of residents older than25 years had less than a 12th-grade education.

Outcomes

Data on subjects were censored if they underwent kidney transplantationor disenrolled from the health plan, which was defined as acontinuous gap in membership of more than 90 days without theinterim use of services. Incident end-stage renal disease, definedby the receipt of maintenance dialysis or a kidney transplant,was identified from a comprehensive health-plan registry.²⁹The primary outcomes of interest included death from any cause,cardiovascular events, and hospitalizations through December31, 2000. Death was identified from a search of health-plandatabases and the California death registry.³⁰ A cardiovascularevent was defined as hospitalization for coronary disease, heartfailure, stroke, or peripheral arterial disease (see the Appendix).

Statistical Analysis

Event rates were directly adjusted for age with the use of theage distribution of the adult source population and are presentedas the number of events per 100 person-years, with 95 percentconfidence intervals. To evaluate the independent effect ofthe estimated GFR on outcomes, we used Cox proportional-hazardsmodels with time-dependent covariates for changing GFR and coexistingillnesses. All variables known to be associated with eitherthe estimated GFR or the outcomes were included in the finalmodels, along with any variables associated with a reduced estimatedGFR (i.e., less than 60 ml per minute per 1.73 m²) in univariateanalyses with a P value of less than 0.01. Age was entered asa categorical variable (20 to 49, 50 to 59, 60 to 69, 70 to79, and 80 years or older), with other covariates included asdichotomous variables. For recurrent outcomes of cardiovascularevents and hospitalizations, we used a "sandwich" estimate ofthe variance–covariance matrix to obtain standard errorsaccommodating the clustering of observations on subjects.³¹In the model for death, we did not include cardiovascular eventsor hospitalizations that occurred after the index date, sincethey were hypothesized to be part of the pathway by which reducedGFR may increase the risk of death.

Each subject and time was assigned an estimated GFR with theuse of the last-value-carried-forward method. Given the varyingnumbers and spacing of measurements of GFR for each subject,this approach may preferentially attribute outcome events tohigher levels of GFR. To address this possibility we analyzeda subgroup of subjects who had had regular serum creatininedeterminations spaced between 1 and 14 months apart throughoutfollow-up. Also, although age and sex are important predictorsof adverse events and are incorporated into the MDRD equation,we found no interactions among age, sex, and GFR and thus presentonly the main-model results.

All analyses were conducted with the use of SAS software (version8.2). The institutional review board of each collaborating institutionapproved the study.

Results

Baseline Characteristics

We identified 1,120,295 adults who had had one or more outpatientmeasurements of serum creatinine, had not previously receiveddialysis or a kidney transplant, and were alive on the indexdate. The median number of outpatient measurements of serumcreatinine per subject during follow-up was three (interquartilerange, one to four).

Subjects with a low estimated GFR at baseline were older thanthose with an estimated GFR of at least 60 ml per minute per1.73 m², and there was greater minority-group representationamong subjects with a low estimated GFR (Table 1). As comparedwith the group with an estimated GFR of at least 60 ml per minuteper 1.73 m², the groups with a reduced estimated GFR also hada higher prevalence of prior cardiovascular disease, proteinuria,diabetes, hypertension, a serum albumin level of 3.5 g per deciliteror less, prior hospitalizations, and other coexisting illnesses(Table 1). Among the 60.7 percent of subjects who had one ormore urine dipstick determinations at any time during follow-up,17.6 percent were found to have proteinuria. Among the 21.2percent of subjects who had one or more serum albumin determinationsat any time during follow-up, 27.8 percent were found to havereduced levels.

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Table 1. Baseline Characteristics of 1,120,295 Ambulatory Adults, According to the Estimated GFR at Baseline.

Outcomes According to the Estimated GFR

The median follow-up among the 1,120,295 subjects was 2.84 years(interquartile range, 1.65 to 4.01), which amounts to 3,132,192person-years. Overall, 21.8 percent of subjects disenrolledduring follow-up, but those who disenrolled were substantiallyyounger, were relatively unlikely to have a reduced estimatedGFR, and had fewer coexisting illnesses than those who remainedenrolled (data not shown). The vital status was complete forall subjects.

During follow-up, 3171 (0.28 percent) subjects began maintenancedialysis and 329 (0.03 percent) underwent kidney transplantation.There were 51,424 deaths, 138,291 cardiovascular events, and554,651 hospitalizations. Age-standardized rates of death, cardiovascularevents, and hospitalization increased substantially with progressivelylower estimated GFRs (Figure 1).

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Figure 1. Age-Standardized Rates of Death from Any Cause (Panel A), Cardiovascular Events (Panel B), and Hospitalization (Panel C), According to the Estimated GFR among 1,120,295 Ambulatory Adults.
A cardiovascular event was defined as hospitalization for coronary heart disease, heart failure, ischemic stroke, and peripheral arterial disease. Error bars represent 95 percent confidence intervals. The rate of events is listed above each bar.

The group of subjects with an estimated GFR of at least 60 mlper minute per 1.73 m² was used as the reference group in theanalysis of the association between the level of the estimatedGFR and each outcome. After adjustment for differences in sociodemographiccharacteristics and the presence or absence of prior cardiovasculardisease, prior hospitalizations, diabetes, hypertension, dyslipidemia,lung or liver disease, cancer, a serum albumin level of 3.5g per deciliter or less, dementia, proteinuria, and the initiationof dialysis during follow-up, the risk of death from any causeincreased sharply as the estimated GFR declined, ranging froma 17 percent increase in risk with an estimated GFR of 45 to59 ml per minute per 1.73 m² to a nearly 600 percent increasewith an estimated GFR of less than 15 ml per minute per 1.73m² (Table 2). The adjusted risk of any cardiovascular eventalso increased as the estimated GFR decreased, ranging froma 43 percent increase in risk with an estimated GFR of 45 to59 ml per minute per 1.73 m² to a 343 percent increase withan estimated GFR of less than 15 ml per minute per 1.73 m² (Table 2).Finally, the adjusted risk of hospitalization increasedas the estimated GFR decreased, ranging from an increase of14 percent with an estimated GFR of 45 to 59 ml per minute per1.73 m² to an increase of 315 percent with an estimated GFRof less than 15 ml per minute per 1.73 m² (Table 2). The presenceof documented proteinuria was also an independent predictorof death (adjusted hazard ratio, 1.3; 95 percent confidenceinterval, 1.3 to 1.4), cardiovascular events (adjusted hazardratio, 1.3; 95 percent confidence interval, 1.2 to 1.3), andhospitalization (adjusted hazard ratio, 1.4; 95 percent confidenceinterval, 1.4 to 1.4).

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Table 2. Adjusted Hazard Ratio for Death from Any Cause, Cardiovascular Events, and Hospitalization among 1,120,295 Ambulatory Adults, According to the Estimated GFR.

In a subgroup of 172,144 subjects who had regular measurementsof serum creatinine during follow-up (mean [±SD] numberof measurements, 3.3±2.1; mean interval between measurements,7.5±3.4 months), the adjusted risks of adverse outcomesdiffered materially from those for the entire cohort only amongthe subjects with an estimated GFR of 45 to 59 ml per minuteper 1.73 m². In the analysis of the subgroup itself, as comparedwith the subjects with an estimated GFR of at least 60 ml perminute per 1.73 m², the subjects with an estimated GFR of 45to 59 ml per minute per 1.73 m² had a similar adjusted hazardratio for death (1.0; 95 percent confidence interval, 1.0 to1.1) and hospitalization (1.0; 95 percent confidence interval,1.0 to 1.0). The adjusted risk of cardiovascular events wasalso attenuated (1.2; 95 percent confidence interval, 1.1 to1.3).

Discussion

Among a large, diverse population of adults, a reduced estimatedGFR was associated with increased risks of death, cardiovascularevents, and hospitalization that were independent of known riskfactors, a history of cardiovascular disease, and the presenceof documented proteinuria. Our study demonstrates that thesegraded risks of adverse events rose sharply for subjects withan estimated GFR of less than 45 ml per minute per 1.73 m² foreach outcome examined both in the overall cohort and in subgroupanalyses. Furthermore, in the cohort as a whole, the absoluterates of these outcomes were considerably higher than the riskof end-stage renal disease.

There has been rapidly growing interest in the relation betweenkidney disease and the risk of death and cardiovascular disease.With recognition that the presence of chronic kidney diseasethat does not necessitate dialysis is of considerable importance,several studies have examined the association of different cutoffvalues of serum creatinine with the risks of death from anycause, death from cardiovascular causes, and cardiovascularevents, and most,³^,⁴^,⁶^,⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹²^,¹⁵ but not all,⁵^,¹³ ofthese studies have found increased risks with higher serum creatininelevels. Others have noted high rates of hospitalization amongpersons with elevated serum creatinine levels.¹⁸ However, sinceserum creatinine levels are not linearly associated with GFR,³²the use of predictive equations (the Cockcroft–Gault equationfor creatinine clearance³³ and the MDRD equation for estimatedGFR¹⁹) has been proposed as a more accurate means of estimatingthe GFR, with the MDRD equation having better predictive abilityin certain populations.²⁰

Relatively few studies have evaluated the estimated GFR andthe risk of outcomes in the general population. In the SecondNational Health and Nutrition Examination Survey (NHANES II),¹²an estimated GFR of less than 70 ml per minute per 1.73 m² wasassociated with a 68 percent increase in the risk of death fromany cause and a 51 percent increase in the risk of death fromcardiovascular causes, as compared with an estimated GFR ofat least 90 ml per minute per 1.73 m². In the AtherosclerosisRisk in Communities Study,¹⁷ an estimated GFR of 15 to 59 mlper minute per 1.73 m² at baseline was associated with a 38percent increase in the risk of cardiovascular disease, as comparedwith an estimated GFR of 90 to 150 ml per minute per 1.73 m².Similar results were obtained in a cohort of older adults (atleast 65 years of age)¹⁶ for an estimated GFR of 15 to 59 mlper minute per 1.73 m², as compared with an estimated GFR of90 to 130 ml per minute per 1.73 m². However, the NHANES I EpidemiologicFollow-up Study did not find a significant association betweenan estimated GFR of approximately 30 to 60 ml per minute per1.73 m² and the risk of death from any cause or death from cardiovascularcauses.¹³ In addition, in the Framingham Heart Study, an elevatedserum creatinine level — 1.5 to 3.0 mg per deciliter (133to 265 µmol per liter) in men and 1.4 to 3.0 mg per deciliter(124 to 265 µmol per liter) in women — was associatedwith a significant risk of death among men but not women andwas not associated with the risk of cardiovascular events ineither sex.⁵

These studies were limited by the use of a single measurementof kidney function, the use of a broad range of definitionsof diminished kidney function, and the inclusion of relativelysmall numbers of persons with kidney disease, thus limitingtheir statistical power to examine different levels of reducedGFR. Furthermore, although several studies used the MDRD equationto estimate GFR, serum creatinine measurements were not directlycalibrated to the values of the MDRD laboratory, so the absolutethreshold level of GFR associated with adverse outcomes cannotbe known with confidence.

Our study further delineates the relation between the GFR andthe risk of adverse events. We found nonlinear relations betweenthe GFR and the risks of death, cardiovascular events, and hospitalization,with an increased risk associated with an estimated GFR of lessthan 60 ml per minute per 1.73 m², which further rose sharplywhen values dropped below 45 ml per minute per 1.73 m². We foundthat an estimated GFR of 15 to 29 ml per minute per 1.73 m²and an estimated GFR of less than 15 ml per minute per 1.73m² in the absence of dialysis were associated with strikinglyhigh age-adjusted mortality rates (11.4 and 14.1 per 100 person-years,respectively). These rates approach the rates among patientswith treated end-stage renal disease.¹ Although the preventionof end-stage renal disease remains a very important goal inpatients with kidney disease, more effective interventions areclearly needed to reduce the disproportionate cardiovascularand economic burden in this population.

Multiple possible explanations exist for the association betweenchronic kidney disease and increased risks of death and cardiovasculardisease. We observed an increased prevalence of prior cardiovasculardisease, known risk factors for cardiovascular events and death,and coexisting conditions with lower levels of the estimatedGFR. However, a reduced estimated GFR was an independent andstrong risk factor for adverse outcomes. Reduced kidney functionis also associated with increased levels of inflammatory factors,³⁴^,³⁵abnormal apolipoprotein levels,³⁴ elevated plasma homocysteine,³⁴enhanced coagulability,³⁵ anemia,³⁶ left ventricular hypertrophy,³⁷increased arterial calcification,³⁸ endothelial dysfunction,³⁹and arterial stiffness.⁴⁰ Whether and how these and other factorsinteract to increase the risk of adverse outcomes remains unclearbut are the focus of ongoing investigations.⁴¹ Our large, ethnicallydiverse population is typical of patients receiving usual clinicalcare rather than referral populations, recruited cohorts, orclinical-trial participants, and thus, our results are probablymore generalizable. The inclusion of large numbers of subjectswith a spectrum of kidney disease also enabled us to make amore detailed evaluation of the effect of the level of the GFRon outcomes. Use of outpatient serum creatinine values thatwere directly calibrated to those of the MDRD core laboratoryincreased our confidence in the validity of the observed associationsof absolute, not just relative, levels of the estimated GFR.Most subjects had serial estimates of the GFR in order to characterizekidney function over time as accurately as possible. We hadcomplete records of deaths and hospitalizations among thesesubjects that occurred at health-plan and other facilities.Our study also shows that the use of a baseline estimate ofthe GFR alone may lead to the misattribution of events to acertain level of GFR measured in the distant past and to thesubsequent attenuation of the true strength of the associationbetween a reduced GFR and outcomes.

Our study had several limitations. As a study of subjects whoreceived usual clinical care, estimates of the GFR were notavailable for the entire source population. For example, patientswith a reduced GFR who did not use medical services would nothave been included. However, over half of adult members of thehealth plan had serum creatinine measurements, which allowedfor a robust assessment of the estimated GFR and outcomes amongmore than 1.1 million subjects. We did not have informationon tobacco or alcohol use, diet, physical activity, other possibleunmeasured confounders (e.g., body-mass index), or the severityof certain conditions (e.g., level of blood pressure or severityof diabetes). Nevertheless, residual confounding is unlikelyto explain the large effect estimates observed for most categoriesof a reduced estimated GFR. Finally, since our study was conductedamong insured adults in northern California, our results maynot be completely generalizable to uninsured persons or personsin other geographic regions.

In conclusion, we found an independent, graded association betweenlower levels of the estimated GFR and the risks of death, cardiovascularevents, and hospitalization. These risks were evident at anestimated GFR of less than 60 ml per minute per 1.73 m² andsubstantially increased with an estimated GFR of less than 45ml per minute per 1.73 m². Our findings support the validityof the National Kidney Foundation staging system for chronickidney disease²² but suggest that the system could be furtherrefined, since all persons with stage 3 chronic kidney disease(GFR, 30 to 59 ml per minute per 1.73 m²) may not be at equalrisk for each outcome. Our findings highlight the clinical andpublic health importance of chronic kidney disease that doesnot necessitate dialysis.

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Supported by a grant (R01 DK58411) from the National Institutefor Diabetes, Digestive, and Kidney Diseases.

Presented in part at the 36th Annual Meeting of the AmericanSociety of Nephrology, San Diego, Calif., November 14 to 17,2003.

Dr. Go reports having received research support from Amgen.Dr. Chertow reports having received research support from Genzyme,Amgen, and Kureha Chemical and having served on advisory boardsfor Genzyme and Amgen.

Source Information

From the Division of Research, Kaiser Permanente of Northern California, Oakland (A.S.G., D.F.); and the Departments of Epidemiology and Biostatistics (A.S.G., G.M.C., C.E.M.) and Medicine (A.S.G., G.M.C., C.-y.H.), University of California, San Francisco, San Francisco.

Address reprint requests to Dr. Go at the Division of Research, Kaiser Permanente of Northern California, 2000 Broadway, 3rd Fl., Oakland, CA 94612-2304, or at alan.s.go{at}kp.org.

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Appendix

The following criteria and International Classification of Diseases,9th Revision, Clinical Modification (ICD-9-CM), and CurrentProcedural Terminology (CPT) codes, if relevant, were used todefine coexisting illnesses (Table 3).

Related Letters:

Chronic Renal Disease and Cardiovascular Risk
Risch L., Sagmeister M., Huber A., Cheng H., Go A. S., Chertow G. M., Hsu C.-y., Anavekar N. S., McMurray J. J.V., Pfeffer M. A.
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N Engl J Med 2005; 352:199-200, Jan 13, 2005. Correspondence

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