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Eur J Cardiothorac Surg 2008;34:390-395. doi:10.1016/j.ejcts.2008.04.017
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Neil J. Howell
Bruce E. Keogh
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Mild renal dysfunction predicts in-hospital mortality and post-discharge survival following cardiac surgery

Neil J. Howella,b, Bruce E. Keoghc, Robert S. Bonsera,b, Timothy R. Grahama,b, Jorge Mascaroa, Stephen J. Rooneya, Ian C. Wilsona, Domenico Paganoa,b,*

a Department of Cardiothoracic Surgery, University Hospital Birmingham, UK
b University of Birmingham, Birmingham, UK
c National Institute for Clinical Outcomes Research, University College London, UK

Received 3 September 2007; received in revised form 15 April 2008; accepted 21 April 2008.

* Corresponding author. Address: Department of Cardiothoracic Surgery, Queen Elizabeth Hospital, Birmingham B15 2TH, UK. Tel.: +44 121 627 2850; fax: +44 121 627 2895. (Email: domenico.pagano{at}uhb.nhs.uk).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objectives: To assess the impact of preoperative renal dysfunction on in-hospital mortality and late survival outcome following adult cardiac surgery. Methods: Prospectively collected data were analysed on 7621 consecutive patients not requiring preoperative renal-replacement therapy, who underwent CABG, valve surgery or combined procedures from 1/1/98 to 1/12/06. Preoperative estimated glomerular filtration rate was calculated using Cockcroft-Gault formula. Patients were classified in the four chronic kidney disease (CKD) stage classes defined by the National Kidney Foundation Disease Outcome Quality Initiative Advisory Board. Late survival data were obtained from the UK Central Cardiac Audit Database. Results: There were 243 in-hospital deaths (3.2%). There was a stepwise increase in operative mortality with each CKD class independent of the type of surgery. Multivariate analysis confirmed CKD class to be an independent predictor of in-hospital mortality (class 2 OR 1.45, 95% CI 1.1–2.35, p = 0.001; class 3 OR 2.8, 95% CI 1.68–4.46, p = 0.0001; class 4 OR 7.5, 95% CI 3.76–15.2, p = 0.0001). The median follow-up after surgery was 42 months (IQR 18–74) and there were 728 late deaths. Survival analysis using a Cox regression model confirmed CKD class to be an independent predictor of late survival (class 2 HR 1.2, 95% CI 1.1–1.6, p = 0.0001; class 3 HR 1.95, 95% CI 1.6–2.4, p = 0.0001; and class 4 HR 3.2, 95% CI 2.2–4.6, p = 0.0001). Ninety-eight percent (7517/7621) of patients had a preoperative creatinine <200 µmol/l, which is not included as a risk factor in most risk stratification systems. Conclusions: Mild renal dysfunction is an important independent predictor of in-hospital and late mortality in adult patients undergoing cardiac surgery.

Key Words: Cardiac surgery • Renal dysfunction • Survival analysis


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Chronic kidney disease is a major public health problem throughout the world. In the United States it is estimated that 4.7% of the population have chronic kidney disease (CKD) stage 3 or higher, as defined by an estimated glomerular filtration rate (GFR) of <60 ml/min per 1.73 m2, with an estimated 11% of the population having some degree of CKD [1], and there is evidence of a similar incidence in the UK [2]. In addition, CKD remains an unrecognised condition in 80–90% of cases and furthermore, the presence of CKD is one of the most potent risk factors for cardiovascular disease such that patients with CKD have a 10–20-fold risk of cardiac death compared to age and sex matched controls [3–5]. In patients undergoing coronary artery bypass grafting (CABG), chronic renal failure, defined as serum creatinine >200 µmol/l or >2.26 mg/dl and end stage renal dysfunction are recognised risk factors for increased perioperative mortality and are accounted for in the commonly used cardiac risk stratification scoring systems [6,7]. We have previously demonstrated that mild renal dysfunction as defined by a serum creatinine 130–199 µmol/l is an independent predictor of outcome in terms of in-hospital mortality, morbidity and mid-term survival in patients undergoing CABG [8]. However limited information exists on the influence of CKD class on in-hospital and late survival following cardiac surgery. The aim of this study was to investigate the impact of CKD class on outcome of patients undergoing cardiac surgery at our institution.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Patient selection
We reviewed data from the cardiac surgical database which hold clinical information on all patients undergoing cardiac surgery at our unit. The data are acquired prospectively as part of the patients’ pathway and are based upon the minimal dataset defined by the Society for Cardiothoracic Surgery in GB and Ireland with some customised additions.

For the purpose of this study we included 7621 consecutive patients (between 1/01/1998 and 31/12/06) who did not require preoperative renal dialysis. We excluded patients undergoing thoracic organ transplantation or aortic surgery. GFR was estimated using the Cockroft-Gault formula [9] and adjusted for each 1.73 m2 of body surface area. Patients were then grouped according to chronic kidney disease class as defined by the National Kidney Foundation Disease Outcome Quality Initiative Advisory Board [10]. Based upon this classification patients with a GFR ≥90 ml/min per 1.73 m2 were considered to have normal renal function and were defined as the reference group, patients with GFR of 60–90 ml/min per 1.73 m2 with mild renal dysfunction were defined as group 2, patients with a GFR of 30–59 ml/min per 1.73 m2 with moderate renal dysfunction were defined as group 3 and patients with GFR of 15–29 ml/min per 1.73 m2 with severe renal dysfunction were defined as group 4. Patients with GFR <15 ml/min per 1.73 m2 and on dialysis were excluded from this study.

2.2 Study end points
In-hospital mortality was tracked from our database and post-discharge survival data were obtained from the National Central Cardiac Audit Database which is linked the Office of National Statistics (census date 1/12/2006). In-hospital mortality was defined as death within 30 days of the operation or at any time within the same hospital admission.

New stroke was defined as post non fatal stroke, transient ischaemic attack, or stupor/coma (type 1 neurological deficit) [11] and low cardiac output state (LCOS) was defined as need for inotropic support and/or intra-aortic balloon pump (IABP) postoperatively. New postoperative dialysis was defined as the need for haemofiltration or dialysis in patients not receiving this treatment preoperatively.

2.3 Statistical analysis
Descriptive data are expressed as mean ± 1 standard deviation. The level of statistical significance ({alpha}) was set at 0.05 (two sided). The risk profile in cardiac surgery is commonly assessed using the European risk stratification score system (EuroSCORE) [6]. It contains patient variables, e.g., age, gender and ventricular function, and surgical variables, e.g., operative priority and surgery other than isolated CABG, all known to influence outcome.

We developed prognostic models to examine whether there was an additional effect of CKD class on the incidence of postoperative all-cause in-hospital mortality, postoperative complications and post-discharge survival [12]. In these models we included the EuroSCORE as a continuous variable and diabetes mellitus as patient level covariates and surgeon as a random effect. Although the EuroSCORE accounts in part for the type of procedure performed, the analysis was repeated for each procedure group except the other procedures group due to its small size. All statistical analysis was performed using SAS version 9.2.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 Appendix A
 References
 
Patient demographics and preoperative CKD class are summarised in Table 1 . Abnormal renal function was present in 74% (5671/7621) of patients. Decreasing GFR was associated with increased age, female gender, impaired LV function and patients with worsening renal function also had more severe heart failure and angina symptoms. This resulted in an increase in the mean EuroSCORE per CKD class independent of surgery performed. A total of 5284 patients underwent CABG, 1356 patients underwent valve surgery, 796 patients underwent combined CABG and valve surgery and the remaining 62 patients underwent other procedures or combination of procedures.


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  		Table 1 Preoperative and operative patient characteristics of each CKD Class
 
3.1 In-hospital outcomes
There were 242 in-hospital deaths (overall mortality 3.2%). The breakdown of in-hospital deaths and complications by CKD class is shown in Fig. 1 . Multivariate analysis demonstrated that the EuroSCORE was a strong independent predictor of in-hospital mortality but in addition to this there was a stepwise increase in operative mortality with each CKD class (Table 2 ).


Figure 1
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  		Fig. 1. Complication per CKD class. The incidence of complication (%) is shown per CKD class for in-hospital death, new stroke, need for renal-replacement therapy, post-operative bleeding requiring surgical re-exploration and low cardiac output syndrome (LCOS) requiring inotropes or intra-aortic balloon support.

 

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  		Table 2 Multivariate analysis for in-hospital mortality
 
The CKD class was also found to be an independent predictor of in-hospital mortality when the analysis was repeated for each procedure group, with the strongest association in patients having CABG (Table 3 ).


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  		Table 3 Multivariate analysis for in-hospital mortality by procedure
 
In addition, with increasing CKD class there was an increase in the incidence of postoperative complications including stroke, dialysis, re-exploration for bleeding and low cardiac output syndrome (Fig. 1). Multivariate analysis demonstrated that in addition to EuroSCORE increasing, CKD class was an independent predictor for the composite end point of these complications (Table 4 ).


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  		Table 4 Multivariate analysis for cardiovascular complications, a composite end-point of either new haemofiltration, new stroke, low cardiac output syndrome or re-exploration for bleeding
 
3.2 Mid-term outcome
Post-discharge survival data were available on 100% of patients. The 5-year unadjusted survival was 93.1% for the reference group, and there was a stepwise decrease in mid-term survival with increasing preoperative CKD (91.1% for class 2, 78.6% for class 3 and 45.7% for class 4, p < 0.0001 (Fig. 2 )). Multivariate analysis demonstrated that the preoperative EuroSCORE was an independent predictor of mid-term survival, and increasing CKD class was found to be an additional independent predictor of reduced survival (Table 5 ). When this analysis was repeated for each procedure group, increasing CKD class remained an independent predictor for reduced late survival and this effect was strongest in patients undergoing CABG (Table 6 ).


Figure 2
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  		Fig. 2. Kaplan–Meier survival curve by preoperative CKD class. The 5-year survival was 93% for the reference group, 91% for CKD class 2, 79% for class 3 and 46% for class 4.

 

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  		Table 5 Multivariate analysis for mid-term survival
 

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  		Table 6 Multivariate analysis for mid-term survival by procedure
 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
Appendix A
 References
 
This study adds to the evidence that even mild preoperative renal impairment has an adverse effect on the survival of patients undergoing cardiac surgery. A number of other reports including our own have shown that mild renal dysfunction is a predictor of adverse outcome in patients undergoing CABG [8,13]. The current study extends this finding to patients without coronary artery disease undergoing valvular surgery.

4.1 Renal dysfunction and in-hospital survival
The adverse influence of preoperative renal dysfunction in patients undergoing cardiac surgery is well accepted, but this is currently addressed in the common risk stratification algorithms only for patients with serum creatinine >200 µmol/l [6], which often represent significant renal dysfunction. More recently it has become apparent that abnormal creatinine levels <200 µmol/l are also associated with reduced survival post-surgery. These studies have also indicated that calculating the preoperative GFR may be a more accurate way of predicting outcome, however the relationship between this marker and outcome is not linear [8,13]. The National Kidney Foundation Disease Outcome Quality Initiative Advisory Board classification of CKD provides clinicians with a straightforward classification of renal impairment based on estimated GFR.

In this study we have grouped patients according to the CKD classification for renal disease, and this has proved to be an independent predictor of adverse outcome in addition to the EuroSCORE for all patients undergoing adult cardiac surgery.

The mechanism in by which renal dysfunction contributes to postoperative mortality is unknown. In this study, the majority of in-hospital deaths were secondary to cardiovascular causes (data not shown) and therefore impaired GFR may simply be a marker of a more advanced cardiovascular disease including increased levels of inflammatory mediators and hypercoagulability [14], endothelial dysfunction [15], arterial stiffness [16] or calcification [17] and left ventricular hypertrophy [18].

A second hypothesis is that renal dysfunction may be secondary to cardiac dysfunction [19–21]. In patients with a reduced cardiac output there is a decline in renal perfusion and an activation of compensatory mechanisms which will lead to renal function impairment [22]. It is of course also possible that the poor outcomes associated with CKD are due to a synergistic effect between cardiovascular cause and consequence.

4.2 Renal dysfunction and complications
In our study increasing preoperative renal dysfunction was associated with a stepwise increase in the incidence of cardiovascular postoperative complications, including stroke, haemodialysis and low cardiac output state in accordance with other studies. This increase in complications may be multifactorial and include decreased drug elimination, hypervolaemia in oliguric patients, hyperkalaemia, anaemia and encephalopathy. We also detected a higher incidence in re-exploration for bleeding in the patients with abnormal renal function and this may be due to associated platelet dysfunction known to occur in patients with renal impairment [23]. All these complications however can be also induced by cardiac surgery related factors including cardiopulmonary bypass (CPB), hypothermia, LCOS and perioperative haemorrhage, and so preoperative renal dysfunction may be a non-specific marker of reduced physiological reserve rather than a cause of adverse events.

4.3 Renal dysfunction and mid-term survival
In addition to an increase in in-hospital mortality, our study shows that increasing CKD class is associated with a decrease in late survival following surgery in addition to the EuroSCORE. There is evidence that renal impairment as defined by a reduction in GFR is a strong risk factor for the development of cardiovascular disease such that patients with CKD have a 10–20-fold risk of cardiac death compared to age and sex matched controls [3], and in this study there was a strong association between CKD class and accepted cardiovascular risk factors (Table 1). This may therefore be identifying patients who require more aggressive secondary prevention following surgery.

4.4 Implications
This study suggests that surgeons should consider not just a creatinine of over 200 but more subtle changes in GFR as an independent risk factor for patients undergoing cardiac surgery. The addition of renal impairment, defined by mild to moderate reductions in GFR may improve the accuracy of current risk stratification models and that the CKD class may be a straightforward and acceptable method of classifying this. It also raises the possibilities that either improvements in our understanding of the mechanisms underlying progressive renal dysfunction, or improved renal protection strategies during the operative period may possibly improve both in-hospital and late survival following cardiovascular surgery. The association of renal impairment with an increased incidence of postoperative complications may also allow for improved resource planning by those responsible for health care provision.

4.5 Study limitations
The follow-up data obtained from the UK Central Cardiac Audit Database only provide knowledge of survival status with no cause of death and this does not allow differentiation between cardiovascular and other cause mortality.

Large cohort studies are subject to errors due to the inadvertent entry of wrong data into the dataset and unavailability of certain data. We have attempted to limit this by adding a validation step to our data entry for every patient in whom data collection is incomplete and by regular quality assessment of the data entered by re-validating approximately 10% of all entered data. Using these measures our database is 99.7% complete for all analysed fields. These procedures should reduce errors but does not eliminate them completely.

Observational bias, particularly for outcomes defined by clinical interventions, e.g. need for new dialysis, re-operation for bleeding and LCOS which are dependent upon various treatment thresholds used by different clinicians, are another type of error found in database derived studies. Although we have set postoperative protocols for dealing with common complications such biases cannot be entirely removed and are seen in all types of epidemiological studies and are accepted as long as they remain random.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
References
 
Conference discussion

Dr J. Pomar (Barcelona, Spain): Chronic kidney disease has been always associated with an increase of early postoperative risk after open-heart operations. Its prevalence is high mainly in elderly patients and still today remains unrecognised for nearly three of every four patients.

Your series shows that a high number of the patients have some degree of chronic renal disease, and you have been able to clearly demonstrate that even mild preoperative renal impairment may play a role in outcomes after open-heart operations.

I did not find in the manuscript a clear indication whether the fact of the operation being under extracorporeal circulation or not could affect the outcomes.

So my first question would be concerning whether all patients were operated under the extracorporeal circulation or not. The other if there was a difference in outcomes.

And the third and last would be whether you have been using tranexamic acid or aprotinin in those patients and if it was in correlation with the postoperative results.

Mr Howell: We do very little off-pump surgery in our department. Less than 1% of the isolated coronaries were done off-pump, so 99% of the patients undergo on-pump cardiac surgery and the majority use a roller pump.

We have looked at meeting cross-clamp bypass times, and there's no difference in intraoperative variables between groups. For the sake of conciseness and on an intention to treat basis we have only presented the preoperative data and I’m sorry, your last question was?

Dr Pomar: Tranexamic acid.

Mr Howell: Tranexamic acid and aprotinin, of course. This is an important issue. We rarely use tranexamic acid, but we use aprotinin on a regular basis. There is a current debate in the literature regarding the effect of aprotinin on renal dysfunction and renal failure.

We use aprotinin now in almost 100% of all our cases from isolated coronary surgery to complex redo surgery, thoracoabdominal aneurysm surgery and transplant surgery; we use aprotinin unless there's a specific contraindication.

Our practice has changed significantly over the 8-year study period. In 1998 the first aprotinin was used in less than 10% of cases, and that has now risen to almost 100%. We have analysed the in-hospital and late results associated with aprotinin use and we have found no association with adverse events in particular that of renal dysfunction. This is being addressed in a separate manuscript which is currently in press. With regards to this presentation we did not think that the extra information could have been accommodated.


   Acknowledgments
 
We would like to thank Ms V. Barnett for collecting the data and managing the database, Mr U. Dandekar for his work in validating entered data, Dr R. Zakheri for the initial data collection regarding renal function and Professor N. Freementle for statistical advice. Data on renal function were kindly provided by Dr R. Cramb, University Hospital Birmingham, and long-term survival data by Dr D. Cunningham, NHS Health and Social Services Centre, UK.


   Footnotes
 
{star} Mr Neil Howell has been supported by British Heart Foundation Grant Q2707/23.

{star}{star} Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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