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Eur J Cardiothorac Surg 2005;27:893-898
© 2005 Elsevier Science NL

Evaluation of Cystatin C as a marker of renal injury following on-pump and off-pump coronary surgery

Yasir Abu-Omara, Shafi Mussaa, Madhava J. Naika, Noel MacCarthyb, Sue Standingc, David P. Taggarta,*

a Department of Cardiothoracic Surgery, John Radcliffe Hospital, Oxford OX3 9DU, UK
b Department for Statistics in Medicine, University of Oxford, Oxford, UK
c Department of Clinical Biochemistry, John Radcliffe Hospital, Oxford OX3 9DU, UK

Received 17 August 2004; received in revised form 7 December 2004; accepted 29 December 2004.

* Corresponding author. Tel.: +44 1865 221121; fax: +44 1865 220244. (E-mail: david.taggart{at}orh.nhs.uk).


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Summary
 References
 
Objective: Cardiopulmonary bypass is regarded as an important contributor to renal injury, whereas off-pump surgery is considered less damaging. Cystatin C, a cystine protease inhibitor, is more sensitive and specific than creatinine in the assessment of renal function. We assessed the value of Cystatin C in quantifying clinical and subclinical renal injury following on-pump and off-pump cardiac surgery. Methods: Sixty consecutive patients were recruited: 30 patients undergoing on-pump CABG and 30 patients undergoing off-pump CABG. Blood samples were collected pre-operatively and on days 1, 2 and 4 postoperatively to measure serum creatinine and serum Cystatin C. Urinary samples were collected concurrently to measure microalbumin and N-acetyl-ß-glucosaminidase, denoting changes in renal glomerular and tubular function respectively. Results: The off-pump group were older (65±11 vs. 61±8 years; P=0.046), had a higher mean Parsonnet score (9.4±6.2 vs. 5.4±3.6, P<0.01) and received fewer grafts (2.4±0.9 vs. 3.1±0.7; P<0.01) compared to the on-pump group. The groups were otherwise matched with respect to preoperative renal function and left ventricular function. Patients undergoing on-pump CABG had greater increases in all four parameters of renal injury. Adjustment for preoperative differences increased the size and significance of the effect of off-pump vs. on-pump surgery (percent difference 13%; 95% CI 2–26 for creatinine, and 16%; 95% CI 4–29 for Cystatin C). Cystatin and creatinine were strongly correlated with each other. Conclusions: Avoidance of cardiopulmonary bypass may reduce renal injury particularly in higher risk patients. Cystatin C proved to be a simple and sensitive measure of overall renal function and can be used in the routine assessment of renoprotective strategies.

Key Words: Renal injury • Cardiopulmonary bypass • Coronary artery bypass grafting • Off-pump


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 5. Summary
 References
 
Acute renal failure affects 1–5% of patients and remains a major cause of morbidity and mortality [1–3]. The pathophysiology of renal injury is multifactorial and is related to perioperative renal hypoperfusion and the presence of endogenous and exogenous nephrotoxins (free radicals, proinflammatory cytokines, circulating catecholamines, anaesthetic agents and contrast media). These can result in glomerular and tubular injury especially in the presence of other co-morbidities including preoperative renal impairment, diabetes mellitus, impaired left ventricular function and advanced age [3–5]. The extent of perioperative renal impairment varies from subclinical injury to established renal failure requiring dialysis.

Glomerular filtration rate (GFR) is the best overall index of renal function but requires meticulous collection of urine over a fixed time period, and is therefore often impractical in the clinical setting. Consequently, serum creatinine and creatinine clearance are the most widely used methods of assessment of renal injury. Serum creatinine level is considered specific but not very sensitive as its levels do not significantly increase until the GFR is reduced to less than 50% of normal [6]. In addition, serum creatinine concentration is significantly influenced by several factors including muscle mass, dietary intake, changes in tubular secretion, as well as interference of various drugs and endogenous substances with its assay.

Cystatin C is a cysteine protease inhibitor produced by all nucleated cells. It is a non-glycosylated low molecular weight plasma protein (approximately 13kDa) [7]. As glomerular filtration is the only elimination pathway of Cystatin C, its serum concentration has been used to estimate GFR in various experimental and clinical settings [8,9]. Cystatin C can be measured from a spot serum sample and avoids the meticulous urine sample collections necessary for estimating creatinine clearance. Its assay is less susceptible to methodological interference inherent in the routine method of creatinine estimation. In addition, Cystatin C has less inter-individual variation than serum creatinine allowing earlier detection of impairment in renal function [10]. The urinary level of microalbumin and N-acetyl-ß-glucosaminidase (NAG) has been used as an index of renal glomerular and tubular damage respectively. NAG is a sensitive measure of renal tubular damage as it is present in the lysosomes of the proximal tubule and is not filtered by the glomerulus due to its relatively high molecular mass (>130kDa) [11].

There has been a recent revival of interest in off-pump coronary artery bypass grafting (CABG). It is being increasingly used as an alternative to conventional CABG aiming to reduce the mortality and morbidity associated with cardiopulmonary bypass. Following the introduction of new surgical techniques and technologies, about a fifth of CABG is now performed off-pump, and the proportion is likely to increase [12].

The efficacy of cystatin c in quantifying changes in renal status following cardiac surgery has not been tested. We assessed the value of this marker, in addition to urinary microalbumin and NAG, in quantifying clinical and subclinical renal injury following cardiac surgery with and without the use of cardiopulmonary bypass (CPB).


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 5. Summary
 References
 
2.1. Patient groups
Following informed consent, 60 consecutive patients undergoing first-time coronary artery bypass grafting (CABG) were recruited prospectively. Thirty patients underwent conventional CABG using CPB (ONCABG) and 30 had off-pump CABG (OPCABG). All the operations were performed by a single surgeon (DPT). In general, we favoured OPCABG in older sicker patients.

2.2. Cardiopulmonary bypass
Following full anticoagulation with Heparin given at a dose of 300IU/kg to maintain an activated clotting time of 400–600s, CPB was instituted using ascending aortic cannulation and a two-stage right atrial venous cannulation. A roller pump (Jostra HL 20) and hollow-fibre membrane oxygenator (Affinity NT, Medtronic, Inc.) were used. The extracorporeal circuit was primed with 1000ml of Hartmann's solution and 2500IU heparin. CPB was maintained with non-pulsatile flow with a flow rate of 2.4l/m2 per min at normothermia with temperature allowed to drift to 34°C. Arterial line filtration was not used. Cardiotomy suction was used. Acid–base was managed with alpha stat control. Myocardial protection was achieved with intermittent antegrade cold crystalloid cardioplegia. On completion of all distal anastomoses, the aortic cross-clamp was removed and the proximal anastomoses performed with partial aortic clamping.

2.3. Off-pump technique
Complete anticoagulation with Heparin was achieved as in the ONCABG group. Regional myocardial immobilisation was achieved with a suction stabilizer (Octopus, Medtronic, Inc. or Guidant, Cardiothoracic Systems, Inc.). The target coronary vessels were snared proximally with a silastic sling. An intracoronary shunt (Guidant AxiusTM) was only used when there was haemodynamic compromise during construction of the anastomosis (usually the distal right coronary artery). Increments of metaraminol and/or colloid were used as dictated by the haemodynamic condition. Visualization was enhanced by using a surgical blower-mister device (Medtronic Clearview®, Medtronic, Inc.). Where possible, patients had total arterial revascularisation using skeletonised internal mammary and composite radial arteries.

2.4. Specimen collection
A 10ml sample of urine and 4ml sample of blood were obtained from each patient at four time points: preoperatively, and days 1, 2 and 4 postoperatively. These results were subsequently used for calculation of the area under the curve (see below). Serum markers of renal injury included serum creatinine and Cystatin C levels. The urinary level of microalbumin, represented as the ratio to urinary creatinine in the same sample, was measured as an index of renal glomerular damage. NAG level was measured in each urinary specimen, also expressed as the ratio to urinary creatinine, as an indicator of renal tubular damage.

2.5. Laboratory methods
Plasma creatinine was measured using a kinetic Jaffe method modified to reduce the effect of non-creatinine Jaffe-reacting chromogens. Urinary microalbumin was measured by a bromocresol green method and was expressed as the ratio to urinary creatinine. These analyses were carried out on an Abbott AEROSET analyser.

Urinary NAG activity was measured with a comercially available kit (PPR Diagnostics Ltd, London, UK) using 2-methoxy-4-(2-nitrovinyl)-phenyl-2-acetomido-2-deoxy-beta-D-glucopyranoside as a substrate. This is hydrolysed by NAG to give a chromogenic product which is measured in an alkaline solution at 540nm. The activity is expressed as a ratio to urinary creatinine measured by an enzymic assay using creatininase and peroxidase and automated on a VITROS analyser (Johnson and Johnson). Plasma Cystatin C was measured on a Cobas FARA by particle-enhanced turbidimetric (PET) assay (DAKO Ltd, Cambridgeshire, UK).

2.6. Statistical analysis
Baseline data for the two groups is presented as mean±standard deviation or as proportions for categorical data. These are compared using t-tests or Mann–Whitney U-test for non-normal data and Fisher's exact tests for categorical data. All measures of renal function were positively skewed and were log transformed to improve approximation to the normal distribution and comparisons were therefore for geometric means. The geometric means of all the biochemical markers at the specified time-points were plotted.

The areas under the curve (AUC) for all the biochemical markers over days 1, 2 and 4 were calculated as a summary measure of post-operative renal function. Data collection was 98% complete. Missing data for the urinary NAG and microalbumin measures for two patients at day 2 and 4 different patients at day 4 was replaced using single imputation based on available outcome and covariate data.

The AUCs were compared between the two groups using multivariate linear regression. Age, sex and the baseline measure of the outcome variable being analysed were included in a base model. Other baseline data (left ventricular function category >50, 30–49 and <30%, New York Heart Association (NYHA) heart failure grade, Canadian Cardiovascular Society (CCS) angina grade, Parsonnet score, presence of diabetes, number of grafts) were tested for addition to the model in a forward stepwise procedure with the criteria for inclusion being a significant improvement in the fit of the model at P<0.1 level. Where several variables could yield such an improvement the one which most increased the explained variance in the data (R squared) was included.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 5. Summary
 References
 
Sixty patients were recruited in the study with baseline characteristics summarised in Table 1. Thirty patients underwent ONCABG and 30 underwent OPCABG. None of the OPCABG cases were converted to ONCABG. Patients in the OPCABG group were older (65.1 vs. 60.5 years, P<0.05), had higher Canadian Cardiovascular Society (CCS) grading for angina and higher perioperative Parsonnet scores (9.4 vs. 5.4, P<0.05). They received fewer grafts than the ONCABG group (2.4 vs. 3.1, P<0.01). Only 53% of patients in the OPCABG group had three vessel disease compared to 80% of those undergoing ONCABG. None of the other perioperative variables were found to be significantly different between the two groups.


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  		Table 1. Baseline characteristics of patients treated with on-pump and off-pump coronary artery bypass grafting
 
3.1. Renal function in on-pump and off-pump CABG
Serum creatinine was in the normal range pre-operatively for all the patients (Table 2). Serum creatinine peaked at day 2 postoperatively. Three patients in the off-pump group and five in the on-pump group developed a transient rise in serum creatinine postoperatively that returned to normal. No patients required postoperative dialysis or haemofiltration.


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  		Table 2. Geometric means of preoperative parameters of renal function in the on-pump and off-pump groups
 
Cystatin C levels also demonstrated a rise on days 2 and 4 postoperatively. Similarly, urinary NAG and microalbumin levels were elevated in the postoperative period compared to preoperatively, the latter returning to baseline by the fourth postoperative day (Fig. 1).



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  		Fig. 1. Plots of the geometric means of all the biochemical parameters preoperatively and on days 1, 2 and 4 postoperatively (a) serum creatinine (b) serum Cystatin C (c) urinary N-acetyl-ß-glucosaminidase (NAG):creatinine ratio (d) urinary microalbumin:creatinine ratio.

 
The AUC for all the biochemical parameters are shown in Table 3. Unadjusted analysis of these measures demonstrated better preservation of renal function in the OPCABG group but the differences observed were not statistically significant at the P<0.05 level. Adjusted models (see Section 2.6) show larger and more significant differences in favour of OPCABG (Table 4).


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  		Table 3. Weighted means of measures of renal function following on-pump and off-pump coronary artery bypass grafting
 

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  		Table 4. Percentage difference in markers of renal function between patients treated with on-pump compared to off-pump coronary artery bypass grafting
 
Table 5 summarises the correlations between the measures of renal function used at baseline and postoperatively. Cystatin and creatinine are highly correlated and each also shows a moderately strong correlation with the NAG/Creatinine ratio but less with the MA/Cr ratio. The MA/Cr and NAG/Cr ratios are highly correlated with each other.


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  		Table 5. Correlation between the measures of renal function at baseline and postoperatively expressed as correlation coefficient (P-value)
 
All models meet statistical assumptions well except for the presence of one outlying data point in each analysis. Removal of the outlier reduced the observed effects but this was not marked except in the case of creatinine, where the effect of a 13% higher postoperative creatinine in the on-pump group was reduced to a 7% increase. There is no reason to believe that the outlying values are incorrect, particularly since the same individual is outlying for cystatin and for creatinine—independent measures of renal function. The latter patient was a 71-year-old lady with three vessel coronary disease and impaired left ventricular function. She underwent ONCABG with intraoperative insertion of an intra-aortic balloon pump. The early postoperative period was complicated by cardiac tamponade requiring re-exploration. She did not receive renal replacement therapy, and serum creatinine returned to normal 15 days postoperatively.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
5. Summary
 References
 
Our study demonstrated a significant increase in serum and urinary markers of renal dysfunction in patients undergoing both ONCABG and OPCABG. Most markers peaked at 1–2 days postoperatively reflecting the time of maximal postoperative renal injury. The rise in NAG:creatinine ratio as well as microalbumin:creatinine ratio confirms tubular and glomerular injury. This was accompanied by a corresponding rise in serum Cystatin C and creatinine.

A striking finding of this study was that patients undergoing conventional CABG had a greater increase in the four parameters of renal injury although the off-pump group were the higher risk patients. Patients undergoing OPCABG demonstrated decreased microalbuminuria and smaller increases in the other three parameters of renal injury compared to the ONCABG group. Adjustment for age, gender, number of grafts, Parsonnet score and left ventricular function increased the size and significance of the detrimental effect of on-pump vs. off-pump surgery. This suggests that avoidance of CPB reduces postoperative renal dysfunction in higher risk patients undergoing CABG.

Serum creatinine, the most commonly used parameter for the assessment of renal function, has many limitations. It has a low sensitivity and its assay is influenced by numerous factors resulting in wide inter-individual variability. Serum Cystatin C, has been shown to be more sensitive and specific than creatinine in a variety of clinical settings [8,9]. In this study there was a strong preoperative correlation in the summary measures of creatinine and cystatin which increased significantly postoperatively. This may have been due to the problems in a single measure of creatinine which were less important when a weighted average of several measures was available post-operatively.

Urinary NAG and microalbumin levels have been used in the assessment of differential tubular and glomerular injury respectively [13,14]. However, in our study, microalbumin levels were more strongly correlated with NAG than with other measures of renal function.

A theoretical reduction in the incidence and severity of postoperative renal impairment has been proposed by eliminating factors related to the use of CPB especially in high risk patients [15–18]. However, the current evidence for off-pump surgery reducing postoperative renal injury is conflicting. A randomised study of 50 patients by Ascione and colleagues [19] demonstrated a significant renoprotective effect of OPCABG as assessed by creatinine clearance, NAG and microalbumin levels. Measurements, however, were only performed up until and including the second postoperative day. In another randomised study of 40 low-risk patients, Tang and associates demonstrated no significant differences in the urinary excretion of microalbumin and retinol binding protein between ONCABG and OPCABG despite a trend of less injury in the latter [13]. They concluded that avoidance of CPB confers no renoprotective effect in low-risk patients. In a small observational study Loef and colleagues [14] measured perioperative glomerular and tubular function up until the second postoperative day in 12 patients undergoing ONCABG and 10 undergoing OPCABG. They demonstrated a significant reduction in transient renal injury with OPCABG. However, as in our study, the number of patients in these studies was relatively small and the patients represent a low-risk population.

A prospective randomised comparison of 200 unselected patients undergoing off-pump vs. conventional CABG reported no difference in the postoperative incidence of renal failure between the two groups [20]. However, several large observational studies including a higher proportion of high-risk patients have demonstrated a significant reduction in the frequency of renal failure in patients undergoing off-pump CABG [16,18,21]. This is consistent with the results from a recent meta-analysis of outcomes following off-pump CABG [22].

While the critics of OPCABG argue that its benefits are marginal, its advocates [18,23] contend that larger benefits are likely to accrue in higher risk patients in whom the adverse consequences of CPB are most marked [24].

4.1. Limitations
There were several limitations to this study. Our cohort of patients was not randomised and therefore the two groups were not perfectly matched. Importantly, however, patients undergoing OPCABG were the higher risk group. Adjustment for the differences between the two groups is therefore important to reduce bias in the estimates obtained. We therefore believe that the adjusted analyses are more likely to represent a true measure of the association between off-pump surgery and a reduction in renal injury.

Repeat analyses with the removal of outliers somewhat reduced the observed associations. This emphasises that the exact effect size cannot be estimated precisely from this study but also highlights that the results are not markedly changed by such factors and are all consistent with a substantial protective effect of CPB avoidance on renal function.

All the patients had normal preoperative renal function as judged by serum creatinine. As one of the principal findings of the present study are biochemical differences in markers of renal dysfunction, the direct clinical significance is less clear as none of the patients required dialysis or haemofiltration. It is possible, however, that renal dysfunction would be more extreme in individuals with compromised preoperative renal function.


   5. Summary
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Summary
References
 
Our study suggests that OPCABG is associated with a reduction in renal injury using sensitive biochemical markers. Cystatin C proved to be a sensitive and simple measure of overall renal function and can be used in the routine assessment of various renoprotective strategies. Further large studies examining the potentially less damaging effects of OPCABG in higher risk patients are clearly justified.


   Acknowledgments
 
This project was funded by the Oxfordshire Health Services Research Committee.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 5. Summary
 References
 

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