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Original Articles: Adult Cardiac

Long-Term Survival After Cardiac Surgery is Predicted by Estimated Glomerular Filtration Rate

^a Dartmouth Institute for Health Policy and Clinical Practice, Lebanon, New Hampshire
^b Central Maine Medical Center, Lewiston, Maine
^c Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire
^d Providence Health System, Portland, Oregon
^e Catholic Medical Center, Manchester, New Hampshire
^f Fletcher Allen Health Care, Portland
^g Portsmouth Regional Hospital, Portland
^h Maine Medical Center, Portland
ⁱ Eastern Maine Medical Center, Bangor, Maine
^j Concord Hospital, Concord, New Hampshire

Accepted for publication March 3, 2008.

^_* Address correspondence to Dr Brown, Rubin 505, Dartmouth Institute for Health Policy and Clinical Practice, One Medical Center Dr, Lebanon, NH 03756 (Email: jeremiah.r.brown{at}dartmouth.edu).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Background: Estimated glomerular filtration rate (eGFR) before coronary artery bypass graft (CABG) surgery is a key risk factor of in-hospital mortality. However, in patients with normal renal function before CABG, acute kidney injury develops after the procedure, making postoperative renal function assessment necessary for evaluation. Postoperative eGFR and its association with long-term survival have not been well studied.

Methods: We studied 13,593 consecutive CABG patients in northern New England from 2001 to 2006. Patients with preoperative dialysis were excluded. Data were linked to the Social Security Association Death Master File to assess long-term survival. Kaplan-Meier and log-rank techniques were used. Patients were stratified by established categories of postoperative eGFR (90 or greater, 60 to 89, 30 to 59, 15 to 29, and less than 15 mL · min^–1 · 1.73 m^–2).

Results: Median follow-up was 2.8 years (mean, 2.7; range, 0 to 5.5). Patients with moderate to severe acute kidney injury (less than 60) after CABG had significantly worse survival than patients with little or no acute kidney injury (90 or greater).

Conclusions: Patients having moderate to severe acute kidney injury after CABG surgery had worse 5-year survival compared with patients who had normal or near-normal renal function.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Renal consequence after coronary artery bypass graft (CABG) surgery has been of growing concern, with 10% to 15% of patients having acute kidney injury and 1% to 2% failure after the procedure [1, 2]. Clinicians and researchers have begun to assess estimated glomerular filtration rate (eGFR) as a marker of renal insufficiency and disease before and after CABG surgery.

Recent reports have only examined preoperative eGFR and shown an increased risk of short- and long-term mortality with lower preoperative eGFR [3–6]. However, in 3% of patients with normal renal function before CABG, acute kidney injury develops after the procedure, suggesting postoperative renal function as a marker for a more accurate assessment of a patients risk of mortality after the procedure [7]. Others have demonstrated both persistent and temporary worsening renal function after aortic surgery was associated with long-term mortality [8]. Others have demonstrated the clinical usefulness of absolute or relative changes in creatinine from baseline to the postoperative period are associated with worse survival [1, 9]. These results suggest the postoperative renal function plays an integral role in the true assessment of renal damage and its association with long-term mortality. Unfortunately, less is known about the association between postoperative eGFR and long-term survival.

In this study, we examined levels of postoperative eGFR and long-term survival. We hypothesized that postoperative eGFR categories are associated with long-term survival and would provide useful clinical evidence for worsening renal function after isolated CABG surgery.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
The Northern New England Cardiovascular Disease Study Group (NNECDSG) was founded in 1987 as a regional voluntary consortium capturing all of the coronary revascularizations and valve procedures in northern New England at eight medical centers in Vermont, New Hampshire, and Maine. The group consists of clinicians, hospital administrators, and health care research personnel who seek to improve continuously the quality, safety, effectiveness, and cost of medical interventions in cardiovascular disease. The Internal Review Board at each center has approved the use of NNECDSG data for quality improvement and research. Patient consent was obtained if required by the center's Institutional Review Board.

Study Cohort
We prospectively enrolled 19,705 consecutive patients undergoing cardiac surgery. We eliminated 2,978 patients undergoing CABG concurrent with heart valve repair or replacement and 2,979 undergoing valve surgery, leaving 13,748 isolated CABG procedures at participating NNECDSG centers between January 2001 and June 2006; and we obtained the last preoperative and highest postoperative serum creatinine measurements (mg/dL). One hundred fifty-five patients with preoperative renal failure requiring dialysis were excluded from the analysis, leaving 13,593 patients who contributed to the analysis.

Assessment of Renal Function
Stafford-Smith and colleagues [10] have reported postoperative eGFR is superior to percent changes in creatinine when assessing long-term mortality. For this reason, we have chosen to characterize the association of postoperative eGFR and long-term survival. Estimated glomerular filtration rate (eGFR) was calculated using the Modification of Diet in Renal Disease (MDRD) equation (mL · min^–1 · 1.73 m^–2): 186 x (serum creatinine mg/dL)^–1.154 x (age)^–0.203 x (0.742 for women) [11]. Preoperative eGFR was calculated using the last preoperative serum creatinine, and postoperative eGFR was calculated using the highest postoperative serum creatinine. Patients were stratified into postoperative categories of eGFR for the primary analsysis: 90 or greater, 60 to 89, 30 to 59, 15 to 29, and less than 15 (mL · min^–1 · 1.73 m^–2) [12]. We plotted preoperative and postoperative eGFR by 5-year mortality to demonstrate the change in eGFR from baseline to the postoperative period.

Patient Follow-Up
The primary outcome of this analysis was all-cause mortality up to 5 and a half years. Mortality was determined by a match of the NNECDSG registry to the Social Security Death Master File (US Department of Commerce National Technical Information Service) [13]. Patients were matched by name, social security number, and date of birth. For patients with partial matches of these variables, a match score was incorporated to account for keypunch errors in social security numbers, date of births, or variations of first or last name. High matching scores were considered matches. Patients with missing information were matched according to known identifiers or were considered lost to follow-up. The Death Master File includes all deaths reported to the Social Security Administration occurring in or outside of the United States, with 92% sensitivity for all deaths [14]. Time to death for index-admission deaths were recorded from case to discharge. Time to death for post-discharge deaths were calculated from case to date of death recorded by the Social Security Administration. In-hospital death was defined by the NNECDSG registry and validated against each medical center's billing records biannually. Methods for data collection and definitions for these variables have been described previously [1, 15].

Statistical Analysis
Baseline characteristics and clinical outcomes were summarized by percentages and means (± SD). We used ² tests and tests of trend to assess similarities between categories of eGFR. Degrees of freedom for the ² tests depended on the number of groups. In Table 1, sex, hypertension, chronic obstructive pulmonary disease (COPD), peripheral vascular disease (PVD), diabetes mellitus, left main disease, angina, and prior CABG were tested using ² test with 1 degree of freedom; priority using ² test had 2 degrees of freedom. All other continuous variables were tested using Cuzick's nonparametric test for trend across ordered groups of postoperative eGFR, which is an extension of the Wilcoxon rank-sum test in Stata (Stata Corp, College Station, TX). All variables in Table 2 were tested using the ² test with 1 degree of freedom, except for length of stay, where the test of trend was used.

The primary time-to-event analysis was calculated from the time of procedure to death or follow-up time. The secondary analysis examined the survivorship of patients from more than 30 days after the procedure until the time of death or follow-up. These analyses were conducted to demonstrate both the short- and long-term consequences of worsening postoperative eGFR. All analyses were conducted using Stata release 9.0 software (Stata Corp, College Station, Texas) [16]. Adjusted survival plots were generated using R 2.5.0 statistical software (R Foundation for Statistical Computing, Wien, Austria).

	Results

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Patients were divided into five categories of postoperative eGFR (number): 90 or greater (1,989), 60 to 89 (5,887), 30 to 59 (4,463), 15 to 29 (1,000), and less than 15 (254) mL · min^–1 · 1.73 m^–2. Baseline characteristics are shown in Table 1. All patient demographics, preoperative disease characteristics were significantly different. Patients in the lowest categories of postoperative eGFR had a worse cardiac profile (higher percentage of patients with 50% or more left main disease, more diseased vessels, lower ejection fraction, higher left ventricular end diastolic pressure) and more likely to have prior CABG surgeries.

Clinical Outcomes
We summarize the clinical outcomes by postoperative eGFR in Table 2. Overall, patients with moderate to severe eGFR (30 to 59, 15 to 29, less than 15) were more likely to have worse outcomes, including a longer length of stay, developed dialysis-dependent renal failure, atrial fibrillation, low output failure, mediastinitis, pneumonia, return to the operating room for bleeding, and higher in-hospital and 5-year mortality. Patients with acute kidney injury were more likely to have low cardiac output, hypotension, and infection (mediastinitis or pneumonia).

Survival Analysis
The adjusted Kaplan-Meier survival plot demonstrates an increased 5-year mortality for patients with a 30 to 59, 15 to 29 and less than 15 eGFR postoperatively (Fig 1). Median follow-up was 2.8 years (mean, 2.7; range, 0 to 5.5). The survival curves were significantly different at p less than 0.001, as calculated by a log-rank test with 4 degrees of freedom. The 5-year incidence of death (per 10 person-years of follow-up) for postoperative eGFR categories: 90 or greater (1.4), 60 to 89 (1.8), 30 to 59 (3.9), 15 to 29 (12.4) and less than 15 (21.2). Each decrease in eGFR category (e.g., mild to moderate, or moderate to severe) had a higher incidence rate of death (Table 3).

View larger version (19K): [in this window] [in a new window]   Fig 1. Adjusted survival plot by categories of postoperative estimated glomerular filtration rate (eGFR). Adjusted Kaplan-Meier survival plot stratified by postoperative eGFR (in order, from top to bottom): 90 or greater, 60 to 89, 30 to 59, 15 to 29, less than 15 mL · min–1 · 1.73 m–2. Curves were adjusted for age, sex, prior coronary artery bypass graft surgery, body mass index, diabetes, chronic obstructive pulmonary disease, priority, ejection fraction, number of diseased vessels, baseline hematocrit, and baseline eGFR. Ordinate graphs the proportion survived. Abscissa graphs person-years of follow-up.

View larger version (26K): [in this window] [in a new window]   Fig 2. Adjusted survival plot by categories of postoperative estimated glomerular filtration rate (eGFR) after 30 days. Adjusted Kaplan-Meier survival plot stratified by postoperative eGFR (in order, from top to bottom): 90 or greater, 60 to 89, 30 to 59, 15 to 29, less than 15 mL · min–1 · 1.73 m–2. Curves were adjusted for age, sex, prior coronary artery bypass graft surgery, body mass index, diabetes mellitus, chronic obstructive pulmonary disease, priority, ejection fraction, number of diseased vessels, baseline hematocrit, and baseline eGFR. Ordinate graphs the proportion survived. Abscissa graphs person-years of follow-up.

View larger version (49K): [in this window] [in a new window]   Fig 3. Five-year mortality plot by categories of preoperative and postoperative estimated glomerular filtration rate (eGFR). Five-year mortality is plotted by preoperative eGFR and postoperative eGFR in predefined categories of renal function. Regardless of preoperative eGFR category, eGFR on average worsens and has an exponential increase in 5-year mortality.

	Comment

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

Our findings are consistent with other reports in the literature. Stafford-Smith and colleagues [10] reported postoperative creatine clearance (using the Cockcroft-Gault equation) [17] was the best indicator for long-term survival. We extended our analysis to examine the role of postoperative eGFR (using the MDRD equation) [11] on 5-year survival. We found postoperative eGFR divided into five categories according to the National Kidney Foundation Kidney Disease Outcomes Quality Initiative [12, 18] was associated with worse long-term survival when eGFR was less than 60 mL · min^–1 · 1.73 m^–2.

We found no increased risk of mortality for patients with mild acute kidney injury (eGFR 60 to 89). We did observe a 76% increased risk of mortality for patients with postoperative eGFR 30 to 59 after CABG surgery, a more aggressive fourfold risk with eGFR 15 to 29 and a sevenfold risk for a patient in renal failure (eGFR less than 15). Most importantly, our multivariate analyses demonstrated postoperative eGFR is a marker for poor survival after controlling for baseline patient and disease characteristics including baseline eGFR.

Most reports have focused mainly on preoperative renal function, demonstrating creatinine clearance or eGFR before cardiac surgery was associated with worse short- and long-term survival [3–6, 19, 20]. As our analysis focused on renal consequences after CABG surgery, we cannot directly compare to these studies; however, we found only eGFR less than 60 was associated with higher mortality.

The outcomes reported in Table 1 help the clinician to better identify patients at risk of acute kidney injury after CABG surgery, and Table 2 helps clinicians to understand the perioperative associations of acute kidney injury after CABG surgery and the high risk of mortality. The proposed mechanisms for acute kidney injury after cardiac surgery are related to hypotension, ischemia, and toxins (including inflammation, free hemoglobin, serum ferretin, and exposure to contrast dye) [1, 21, 22]. Recently, Schiffrin and colleagues [23] summarized the negative feedback mechanisms at play between chronic kidney disease, hypertension, and dyslipidemia and the progression toward renal failure. However, the cause and effect mechanism of worsening renal function still needs to be elucidated. Although the cause and effect mechanism needs to be elucidated, we know that a majority of patients decline in renal function and in approximately half of these patients acute renal failure or injury will develop. We recently reported a prediction rule for patients with normal or near-normal renal function (eGFR 60 or greater) in whom developed severe acute kidney injury (eGFR less than 30). We discovered baseline patient variables including older age, female sex, congestive heart failure, use of intra-aortic balloon pump were among the strongest risk factors. Other risk factors included hypertension, diabetes mellitus, peripheral vascular disease, prior CABG surgery, and white blood cell count [7].

The recent study by Welten and colleagues [8] among patients having temporary or persistent renal dysfunction after abdominal aortic surgery helps to validate our findings. Welten reported that patients with greater than 10% drop in creatinine clearance, whether temporary (corrected on day 3) or persistent, had a fourfold to sevenfold increased risk of 30-day mortality and a twofold risk of 10-year mortality [8]. These findings help to hold value to the use of postoperative eGFR based on the highest post-procedure creatinine level as a marker for higher mortality. Patients having moderate to severe acute kidney injury (eGFR less than 60), regardless of recovery, are at increased risk of mortality compared with patients who have normal or near-normal renal function (eGFR 60 or greater). Based on these two findings, physicians should closely monitor patients with eGFR less than 60 after the procedure until renal function recovers. Each institution should discuss triggers for nephrology consults for patients with acute kidney injury present either before or after cardiac surgery.

There are preoperative, intraoperative, and postoperative processes of care that should be considered after identifying patients at risk for acute kidney injury. Such processes include intraoperative red blood cell transfusion (increasing free hemoglobin and ferretin exposure) and prolonged cardiopulmonary bypass time [24–27]. The Cleveland Clinic suggested that nephrotoxic drugs, ionic contrast dye exposure, and volume imbalances all can result in acute kidney injury during the hospitalization [28]. Other preventative measures that have been proposed is performing the surgery off pump [29, 30]. In the postoperative period, the use of the natriuretic peptide nesiritide improved postoperative eGFR and 6-month survival [31].

There are limitations to our study. First, we could not identify causality in the development of worsening eGFR. Efforts described previously have attempted to elucidate the factors associated with the development of acute kidney injury after CABG surgery; however, causality has not reported to date. Second, we calculated eGFR based on the highest postoperative creatinine value and did not have access to the range of creatinine values for each patient. Since postoperative eGFR was obtained after the surgery and before discharge, our closest time-to-event analysis was measured from the operative date. Because we did not capture the date and time of the highest creatinine value to estimate GFR, we are unable to model postoperative eGFR as a time-dependent covariate. However, we recalculated our time-to-event analysis 30 days after CABG; we discovered all categories of eGFR less than 90 were significantly different from eGFR 90 or greater, except for 60 to 89 eGFR. We did not have follow-up on the recovery or nonrecovery from acute kidney injury. This information will be valuable in the future to model the mortality resulting from patients with tempory acute kidney injury compared with patients who have persistent acute kidney injury. Welten and coworkers [8] reported that both patients with temporary or permanent acute kidney injury had a fourfold to sevenfold increase risk of short- and long-term mortality. Additional renal function markers during the perioperative admission would allow us to identify whether or not patients recovered from impaired renal function before discharge. We prospectively enrolled patients in this study as part of the NNECDSG regional registry cohort, which collects and reports data on 100% of the cardiac procedures in northern New England. Therefore, biases resulting from patient enrollment or data collection are not likely limitations of this study.

In summary, we found postoperative eGFR less than 60 (mL · min^–1 · 1.73 m^–2) was associated with worse 5-year survival. We demonstrated postoperative eGFR is an adequate measure in identifying acute kidney injury and the subsequent risk of mortality. Clinical care teams should monitor preoperative and postoperative renal function using calculated eGFR, preoperatively risk-stratify patients utilizing preoperative risk prediction tools [2, 7, 32–35], and improve processes to prevent the occurrence of acute kidney injury after the procedure.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Research was funded by the Northern New England Cardiovascular Disease Study Group.

	References

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments 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 Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Richard P. Cochran Anthony P. Furnary Karyn S. Kunzelman David C. Charlesworth Bruce J. Leavitt Lawrence J. Dacey Robert E. Helm John H. Braxton Robert A. Clough Robert F. Dunton Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Brown, J. R. Search for Related Content PubMed PubMed Citation Articles by Brown, J. R. Related Collections Cardiac - other Related Articles