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J Thorac Cardiovasc Surg 2007;134:683-689
© 2007 The American Association for Thoracic Surgery

Surgery for Acquired Cardiovascular Disease

Long-term outcomes after coronary artery bypass grafting: Preoperative kidney function is prognostic

^a University of Colorado Health Sciences Center, Division of Renal Diseases and Hypertension, Denver, Colo
^b Department of Thoracic and Cardiovascular Surgery and Angiology, Dupuytren University Hospital, Limoges, France
^c CSC, Inc, Santa Barbara, Calif.

Received for publication November 27, 2006; revisions received March 23, 2007; accepted for publication April 12, 2007.

^_* Address for reprints: Michel B. Chonchol, MD, University of Colorado Health Sciences Center, Division of Renal Diseases and Hypertension; Box C-281, Denver, CO 80262. (Email: Michel.Chonchol{at}uchsc.edu).

	Abstract

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Objective: End-stage renal disease is an independent predictor of mortality after coronary artery bypass grafting. Limited information exists, however, regarding the impact of chronic kidney disease on long-term outcome after bypass grafting. The purpose of this study was to assess the impact of kidney function on long-term outcomes in patients undergoing coronary artery bypass grafting.

Methods: We studied 931 consecutive patients undergoing coronary artery bypass grafting in a single center. Demographic and clinical data were collected preoperatively. Chronic kidney disease was defined preoperatively according to the Modification of Diet in Renal Disease equation as an estimated glomerular filtration rate less than 60 mL · min^–1 · 1.73 m^–2. Multivariate Cox proportional hazard analyses were performed to determine the independent prognostic factors after bypass grafting. The primary outcome was a composite, combining death, acute coronary syndrome, stroke or transient ischemic attack, and coronary or peripheral revascularization during follow-up. Secondary outcomes were overall causes of death and cardiovascular death, acute coronary syndrome, and stroke or transient ischemic attack.

Results: One hundred fourteen (12.2%) patients had preoperative chronic kidney disease (estimated glomerular filtration rate range, 20.5-59.8 mL · min^–1 · 1.73 m^–2). After a mean follow-up of 3.1 ± 1.4 years (median, 3.3 years), chronic kidney disease was found to be an independent predictor of the composite outcome (hazard ratio and 95% confidence interval, 1.46 [1.01-2.11]; P = .0467) and overall death (hazard ratio and 95% confidence interval, 1.89 [1.16-3.07]; P = .0106).

Conclusions: Beyond the perioperative period, preoperative moderate-to-severe chronic kidney disease is an independent long-term predictor of cardiovascular events and total mortality after coronary artery bypass grafting. Chronic kidney disease status should be incorporated into prediction models and clinical risk assessments.

	Introduction

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Dr Chonchol

With the aging of the population in Western countries, as well as the dramatic growth of reported rates of hypertension and diabetes, the prevalence of chronic kidney disease (CKD) and impaired kidney function is also increasing dramatically.^1,2 These two latter conditions are frequently associated with widespread atherosclerotic disease,³ and as a consequence, coronary artery bypass grafting (CABG) is increasingly considered for patients with definite CKD or kidney dysfunction.⁴

Several studies have reported a poor outcome in patients with end-stage renal disease^5,6 and kidney dysfunction after CABG,^7-9 but long-term data for the latter case are scarce. Additionally, most studies that have shown an association between preoperative kidney disease and a higher incidence of morbidity and mortality after CABG have concentrated on patients with elevated serum creatinine.^6,10-13 However, serum creatinine is not a sensitive marker, because its concentration is affected by factors other than glomerular filtration rate (GFR), such as creatinine generation, secretion, and extrarenal excretion.¹⁴ Recent published guidelines advise estimating GFR from prediction equations in patients with cardiovascular disease.^15,16

There is limited information on the influence of moderate-to-severe CKD on the long-term survival of patients undergoing CABG.^17-19 The main objective of this study was to investigate the impact of preoperative CKD, defined as an estimated glomerular filtration rate (eGFR) of less than 60 mL · min^–1 · 1.73 m^–2 measured by the Modification of Diet in Renal Disease (MDRD) study equation on the long-term outcomes of cardiovascular events and total mortality after CABG.

	Materials and Methods

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Study Population and Measures
The study cohort consisted of 931 consecutive patients who underwent CABG at the Dupuytren University Hospital, Limoges, France, between August 1998 and January 2002. All study participants signed an informed consent form before study entry. All preoperative and perioperative data, which included cardiovascular history and cardiovascular risk factors, were collected in a standard form. Patients were considered smokers when they were actively smoking or had stopped within 2 years before the operation. Patients were considered to have diabetes if they had a fasting blood glucose level at entry of more than 7.8 mmol/L or were taking oral hypoglycemic agents or insulin, or both. Those who had a blood pressure of 160/90 mm Hg or higher measured twice before surgery or who were taking antihypertensive drugs for that purpose were considered to have hypertension. Hypercholesterolemia was defined by a fasting blood cholesterol level at entry of more than 240 mg/dL or by the need for lipid-lowering agents for that purpose. Supraventricular arrhythmia was defined by the presence of sustained atrial fibrillation or flutter on the preoperative electrocardiogram. Peripheral vascular disease (PVD) combined any report of clinical peripheral arterial disease (ie, an intermittent claudication and/or a history of vascular surgery for peripheral arterial disease) and any report of stroke or transitory ischemic attack (TIA) and/or any carotid surgery before enrolment. Patients undergoing emergency surgery (coronary angiography to surgery delay < 48 hours) were excluded from the analysis. Patients with acute coronary syndrome (ACS) operated on beyond 48 hours and/or presenting hemodynamic instability were considered in an unstable cardiac status and were included in the study. Preoperative data included the number of bypasses performed, whether the revascularization was complete, the requirement of cardiopulmonary bypass or an off-pump surgery, and the performance of any combined procedure (ie, concomitant valvular or carotid surgery).

Definition of CKD
Preoperative serum creatinine was collected at admission. Serum creatinine was assessed by the Jaffé rate-balked and compensated method, using a kinetic colorimetric assay on the Roche/Hitachi Modular P analyzer (F. Hoffman-LaRoche Inc Ltd, Basel, Switzerland).

We estimated kidney function using a formula derived by the MDRD study group, as suggested by recent published guidelines.^14,16 This equation expresses GFR in milliliters per minute per 1.73 m² body surface area and is calculated as 186 x (serum creatinine^–1.154) x (age^–0.203) x 1.21 (if black) x 0.742 (if female), where serum creatinine is measured in milligrams per deciliter and age is in years. We defined CKD as an eGFR less than 60 mL · min^–1 · 1.73 m^–2.¹⁴

Outcomes
The follow-up period corresponded to the interval from the day of CABG until March 1, 2004. Follow-up was performed by reviewing hospital charts, as well as by telephone contacts with patients’ family physicians. The primary outcome was composite, corresponding to the occurrence of at least one of these events during the follow-up: death, nonfatal ACS corresponding to any type of myocardial infarction or unstable angina after surgery requiring admission to a coronary care unit, secondary coronary revascularization, nonfatal stroke or TIA requiring admission to a neurology department and defined by a neurologist during the hospital stay, and peripheral vascular surgery. Secondary outcomes studied were overall mortality and cardiovascular mortality.

Statistical Analysis
All statistical analyses were performed with SAS software version 8.2 (SAS Institute, Cary, NC). Summary statistics (mean and standard deviation for continuous variables and N and percent for discrete variables) were performed for all covariates, first for the overall sample and then separately by kidney function status. Comparisons were made between the two groups with t tests or ² tests, as appropriate. Univariate Cox regression models were performed for each covariate for each primary or secondary outcome. The CKD status, as well as all other covariates being significant in univariate analyses, was entered into a multivariate model. Cox models were run successively with backward stepping, at each step removing the least significant term. The backward stepping continued until only significant terms remained in the model. Kaplan–Meier survival curves were produced for the composite, overall causes of death, and cardiovascular death outcome showing the survival curves for each CKD group. Nonlinearity between continuously measured eGFR and the outcome measures was explored by fitting restricted cubic splines, as well as by fitting a third-degree polynomial model. Log–rank statistics were calculated comparing the two groups.

	Results

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Baseline Characteristics
In this study population of 931 patients, 114 (12.2%) had moderate-to-severe CKD as defined above (mean eGFR 46.6 ± 10.7 mL · min^–1 · 1.73 m^–2, range: 20.5-59.8 mL · min^–1 · 1.73 m^–2). These subjects were older, were more likely to be female, and were more likely to have a history of hypertension, diabetes, PVD, and New York Heart Association class III or IV than participants without CKD. A higher proportion of concomitant valvular surgery was noted in those with CKD (Table 1).

During this period, 192 (20.6%) patient results met the primary outcome. Ninety-four patients died, including 60 cases of cardiovascular death. Forty-two patients had ACS during follow-up, and 28 underwent secondary coronary revascularization. Thirty-three had a stroke or TIA, and 40 had peripheral vascular surgery.

Primary outcome
During the entire follow-up period, 37 (32.5%) patients in the CKD group and 155 (19%) in the group without CKD met the primary outcome (P = .0009). Figures 1, 2, and 3 show the composite, overall, and cardiovascular freedom from events curves according to the absence or presence of CKD, respectively. In univariate and multivariate analyses (Table 2), moderate-to-severe CKD was independently associated with the occurrence of the primary composite outcome during follow-up. The model was repeated, replacing the binary CKD variable by eGFR as a continuous variable. After multivariate adjustment, eGFR remained significantly associated with the primary outcome, with a hazard ratio (HR) at 1.11 (95% confidence interval [CI] 1.01, 1.22; P = .0396) per 10 mL · min^–1 · 1.73 m^–2 decrease of eGFR (full model not shown). Other independent predictors of the primary outcome included increased age, preoperative supraventricular arrhythmia, New York Heart Association class III or IV, concomitant valvular surgery, presence of PVD, and unstable cardiac status. Furthermore, the relationship between eGFR and outcome appeared linear, since no additional information was provided with nonlinear models.

View larger version (11K): [in this window] [in a new window]   Figure 1. Kaplan–Meier estimates of probability of the composite end point after CABG by eGFR category. GFR is expressed in milliliters per minute per 1.73 m2. CKD, Chronic kidney disease; CABG, coronary artery bypass grafting; eGFR, estimated glomerular filtration rate; GFR, glomerular filtration rate.

View larger version (10K): [in this window] [in a new window]   Figure 2. Kaplan–Meier estimates of probability of overall survival after CABG by eGFR category. GFR is expressed in milliliters per minute per 1.73 m2. Definitions of acronyms as in Figure 1.

View larger version (9K): [in this window] [in a new window]   Figure 3. Kaplan–Meier estimates of probability of cardiovascular survival after CABG by eGFR category. GFR is expressed in milliliters per minute per 1.73 m2. Definitions of acronyms as in Figure 1.

View larger version (13K): [in this window] [in a new window]   Figure 4. Cubic spline analysis for risk of outcome (composite, death, and cardiovascular [CV] death) with decreasing eGFR. GFR is expressed in milliliters per minute per 1.73 m2. eGFR, Estimated glomerular filtration rate; GFR, glomerular filtration rate.

	Discussion

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In this longitudinal study, moderate-to-severe preoperative CKD was found to be a significant predictive marker of subsequent events in patients after CABG. This prognostic value is independent of many usual prognostic comorbidities, which can be shared between coronary artery disease and CKD, including diabetes, hypertension, heart failure, or the presence of PVD. In this cohort, the 12% prevalence of CKD in patients undergoing CABG is relatively low, compared with 21% to 37% reported elsewhere.^9,13,18,19 Nevertheless, CKD was shown to increase the risk for the primary composite outcome of death, nonfatal ACS, coronary revascularization, stroke and peripheral vascular surgery, as well as overall mortality alone, by 46% and 89%, respectively.

Data on moderate-to-severe CKD defined by a more reliable estimate of kidney function (eGFR) and its prognostic value on a variety of long-term cardiovascular outcomes are scarce.^9,18 In an analysis from The Society of Thoracic Surgeons National Cardiac Database, Cooper and associates⁹ reviewed the case histories of 483,914 patients receiving isolated CABG. The authors showed an association between eGFR and operative mortality and morbidities, but specific long-term cardiovascular end points were not evaluated. In a British study,¹⁸ 37% of patients undergoing CABG presented with an eGFR less than 60 mL · min^–1 · 1.73 m^–2, and eGFR was an independent predictor of short- and long-term mortality. The only outcome evaluated was overall mortality, and the median length of follow-up was 2.3 years. With a longer follow-up period of 3.3 years, our study is the first providing evidence of the additive predictive power of eGFR on a series of combined cardiovascular end point and overall mortality.¹⁹

Although we did not observe CKD to be an independent predictor of the short-term (30 days) postoperative outcome, most likely because of very few events that had accrued during this period, the interpretation of the survival curves after CABG in our cohort suggest that the highest risk of achieving the composite outcome and overall death in the group with CKD can be observed in the initial 12 months after surgery. After this period, the survival curves appeared to be parallel in CKD and no-CKD patients.

The National Kidney Foundation has recommended that GFR should be estimated from prediction equations that include serum creatinine concentration and some or all of the following variables: age, sex, race, and body size. The MDRD study and Cockcroft–Gault equations provide useful estimates of GFR in adults.¹⁴ We have chosen for our analysis to primarily define CKD on the basis of the MDRD study equation because it has been established to be more accurate in patients with moderate-to-severe kidney disease.¹⁶ Furthermore, an independent association has been established between reduced eGFR measure by the MDRD equation and the risk of death, cardiovascular events, and hospitalization in large, community-based populations.²⁰ In addition, the science advisory from the American Heart Association Kidney and Cardiovascular Disease Council recently recommended that all patients with cardiovascular disease should be screened for evidence of kidney disease with the combined use of the MDRD equation to estimate GFR and a sensitive test to detect microalbuminuria.¹⁵

Studies in patients with cardiovascular disease have consistently shown that the level of kidney function is an independent risk factor for cardiovascular mortality.^20-23 This association has multiple explanations: (1) Excess comorbidities have been reported in patients with CKD, including volume expansion resulting from sodium retention, hypertension, and insulin resistance with impaired glucose tolerance.²⁴ (2) Abnormal vascular biology in CKD has been widely established; as renal function declines, a host of abnormalities develops, including increased oxidative stress, inflammation (eg, increased c-reactive protein),^25,26 phosphate retention with medial vascular calcification,²⁷ increased parathyroid hormone concentrations with myocardial calcification and dysfunction,²⁸ and anemia and left ventricular hypertrophy,²⁹ all of which could increase cardiovascular disease.²³ Increased plasma homocysteine, fibrinogen, and uric acid are other cardiovascular risk factors that occur with CKD.^23,24 (3) Numerous studies^23,30 have linked the presence of CKD with underuse of key cardiovascular medications after CABG. (4) Finally, therapeutic nihilism has been associated with these chronically ill patients.²³

Despite the comprehensive nature of the dataset, there are several limitations to consider in this analysis. First, we were unable to determine the cause and duration of kidney dysfunction and we did not have information regarding microalbuminuria or overt proteinuria. Second, we defined CKD on the basis of eGFR rather than on definite measurements of kidney function; however, direct measurements of GFR are rarely used in clinical practice. Third, hemodynamic changes that could occur from underlying cardiovascular disease or use of angiotensin antagonists that could potentially affect kidney function were not measured. Finally, measurements of eGFR were based on a single serum creatinine determination, which could have been influenced by unstable cardiac status. The strengths of this study are the large number of patients, the inclusion of several demographic, clinical, and operative factors for the patient, and a longer follow-up period than that of previous studies with a similar eGFR threshold.^18,19

In conclusion, the preoperative measurement of kidney function, particularly eGFR, is a powerful and independent predictor of overall mortality and cardiovascular events in patients undergoing CABG. These results lead us to recommend the incorporation of preoperative eGFR into the risk assessments of perioperative and long-term outcomes after CABG.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Marc Laskar Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Chonchol, M. B. Articles by Laskar, M. Search for Related Content PubMed Articles by Chonchol, M. B. Articles by Laskar, M. Related Collections Chest wall