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Ann Thorac Surg 2003;76:2007-2012
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

Preoperative C-reactive protein and outcome after coronary artery bypass surgery

Fausto Biancari, MD, PhD*a, Jarmo Lahtinen, MDa, Samuli Lepojärvi, MSa, Pekka Rainio, MD, PhDa, Esa Salmela, MDa, Risto Pokela, MD, PhDa, Martti Lepojärvi, MD, PhDa, Jari Satta, MD, PhDa, Tatu S. Juvonen, MD, PhDa

a Division of Cardiothoracic and Vascular Surgery, Department of Surgery, University of Oulu and Oulu University Hospital, Oulu, Finland

Accepted for publication June 3, 2003.

* Address reprint requests to Dr Biancari, Division of Cardiothoracic and Vascular Surgery, Department of Surgery, Oulu University Hospital, PO Box 21, 90029 Oulu, Finland
e-mail: faustobiancari{at}yahoo.it


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: C-reactive protein (CRP) is a predictor of early and late outcome after coronary angioplasty, but there is scant data on its impact on the outcome after coronary artery bypass grafting (CABG).

METHODS: The predictive value of preoperative CRP was evaluated in a series of 764 patients who underwent on-pump CABG.

RESULTS: During the in-hospital stay, 13 patients (1.7%) died, 45 (4.5%) developed low cardiac output syndrome, and 28 (3.7%) suffered minor or major cerebrovascular complications. Patients with a preoperative serum concentration of CRP>=1.0 mg/dL had a higher risk of overall postoperative death (5.3% vs 1.1%, p = 0.001), cardiac death (4.4% vs 0.8%, p = 0.002), low cardiac output syndrome (8.8% vs 3.7%, p = 0.01), and any cerebrovascular complication (4.4% vs 3.5%, p = 0.66). Preoperative serum concentration of CRP>=1.0 mg/dL was significantly more frequent among patients with history of myocardial infarction, diabetes, lower limb ischemia, low left ventricular ejection fraction, NYHA class IV, and in those undergoing urgent or emergency operation. At multivariate analysis, preoperative serum concentration of CRP >= 1.0 mg/dL (p = 0.01, O.R.: 6.97) and left ventricular ejection fraction (p = 0.01, O.R.: 0.95) were independent predictors of postoperative death. Postoperative mortality rate was 0.3% among patients with preoperative CRP < 1.0 mg/dL and an ejection fraction >=50%, whereas it was 21.4% among those with a preoperative CRP >= 1.0 mg/dL and an ejection fraction less than 50% (p < 0.0001).

CONCLUSIONS: Preoperative serum concentration of CRP in patients undergoing on-pump coronary artery bypass surgery is an important determinant of postoperative outcome.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Arteriosclerosis is, nowadays, considered a chronic low-grade inflammatory disease. The degree of such an inflammatory process strongly correlates with the extent and severity of atherosclerotic disease [1, 2]. C-reactive protein (CRP) has emerged not only as a relevant marker of this inflammatory process underlying the development of arteriosclerosis, but also as one of the engines of the inflammatory cascade [3].

There is a burden of evidence showing that CRP is an independent predictor of long-term cardiovascular events in healthy subjects [3–5]. Furthermore, increased serum levels of CRP have been shown to predict poor outcome in patients with unstable angina [6] and myocardial infarction [7] as well as with ischemic stroke [8]. Similarly, a number of studies showed that CRP predicts early and late cardiac events after coronary angioplasty [9–13], but scant data exists on its impact on the outcome after coronary artery bypass grafting (CABG) [14, 15].

Herein, we report the results of a study on the prognostic impact of CRP in a large series of patients who have undergone on-pump CABG.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 Acknowledgments
 References
 
From January 2000 to December 2001, 1048 patients underwent on-pump coronary artery bypass grafting in our institution, and 20 of them (1.9%) died during the in-hospital stay. Data on preoperative serum concentration of CRP as well as pre-, intra-, and postoperative variables was available in 764 patients who form the basis of the present study. Selection of patients included in the present study was done solely according to the availability of preoperative CRP values as measured by a single method and of other clinical variables. Data on pre- and postoperative outcome was collected retrospectively, whereas angiographic findings of the status of the coronary arteries as well as all the intraoperative variables were collected prospectively. Patients' characteristics are reported in Table 1.


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  		Table 1. Distribution of Pre- and Intraoperative Risk Factors According to Postoperative Outcome Endpoints

 
Serum concentrations of C-reactive protein were quantified using a Cobas Integra 700 (Latex) (Roche Diagnostics). Since in our institution serum levels of CRP < 1.0 mg/dL are considered normal, in most cases this parameter is not reported in patients' laboratory records with specified values <1.0 mg/dL. Because of this, herein, the analysis was done considering CRP as a categorical variable.

The angiographic status of the coronary arteries/segments was graded according to the following criteria: 1, no stenosis; 2, stenosis <50%, 3, stenosis of 50% to 69%; 4, stenosis of 70% to 89%; 5, stenosis of 90% to 99%; 6, vessel occlusion; and 7, the vessel is not visualized. These scores were assigned to the following vessels/segments: on the left side, the left main coronary artery, the anterior descending artery divided in proximal, middle, and distal segments, the first and second diagonal arteries, the ramus medianus, the circumflex artery divided in proximal, middle, and distal segments, and the first and second obtuse marginal branches; and on the right side, the right coronary artery divided in proximal, middle, and distal segments. The overall coronary angiographic score was calculated by summing the score of each of these arteries/segments. The minimum overall possible score is 15 and the maximum is 105.

Statistical analysis was performed using a SPSS statistical software (SPSS vs 10.0.5, SPSS Inc, Chicago, IL). Continuous variables are reported as the mean ± standard deviation. The {chi}2 test and the Fischer's exact test were used for univariate analysis of categorical data. The Mann–Whitney test and the Kruskal–Wallis test were used to assess the distribution of continuous variables in different subgroups. A receiver operating characteristics curve was used for identification of the best cut-off value of left ventricular ejection fraction in predicting postoperative adverse outcome. Logistic regression with the help of backward selection was used for multivariate analysis. Only the preoperative variables where p < 0.05 at univariate analysis were included in the regression model. The limited number of patients with known preoperative left ventricular ejection fraction value restricted the multivariate analysis to 443. A p less than 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 Acknowledgments
 References
 
Thirteen patients (1.7%) died during the in-hospital stay, cardiac causes being the main cause of death in ten of them. Thirty-four patients (4.5%) developed low cardiac output syndrome, and seven of them required intraaortic balloon pump insertion. Twenty-eight patients (3.7%) suffered of any minor or major cerebrovascular complications, 14 (1.8%) having had transient ischemic attacks or stroke. The impact of clinical variables, according to univariate analysis, on postoperative death, low cardiac output syndrome and any postoperative cerebrovascular complications is summarized in Table 1.

One hundred and fourteen patients had a preoperative serum concentration of CRP >= 1.0 mg/dL. The distribution of preoperative serum concentration of CRP is shown in Figure 1. Patients with preoperative serum concentration of CRP >= 1.0 mg/dL had a significantly higher risk of overall postoperative death (p = 0.001, specificity: 85.6%, sensitivity: 46.1%, accuracy: 84.9%), cardiac death (p = 0.002, 4.4% vs 0.8%, specificity: 85.5%, sensitivity: 50.0%, accuracy: 85.1%) and to develop low cardiac output syndrome (p = 0.01, specificity: 85.7%, sensitivity: 29.4%, accuracy: 83.2%) (Table 1). Patients with a preoperative serum concentration of CRP >= 1.0 mg/dL had a slightly higher risk to experience any cerebrovascular complication (4.4% vs 3.5%, p = 0.66).



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  		Fig 1. Distribution of preoperative serum concentration of C-reactive protein.

 
Table 2 summarizes the distribution of preoperative serum concentration of CRP < or >= 1.0 mg/dL among other preoperative clinical risk factors. The incidence of preoperative serum concentration of CRP >= 1.0 mg/dL was significantly higher among patients with history of myocardial infarction, diabetes, lower limb ischemia, low left ventricular ejection fraction, NYHA class IV, and in those who have undergone urgent or emergency operation (Table 2).


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  		Table 2. Distribution of C-Reactive Protein < or >= 1.0 mg/dL Among Other Preoperative Risk Factors

 
When only preoperative variables were included in the multivariate analysis, serum concentration of CRP >= 1.0 mg/dL (p = 0.01, O.R.: 6.97, 95%C.I.: 1.45 to 33.42) and left ventricular ejection fraction (p = 0.01, O.R.: 0.95, 95%C.I.: 0.91 to 0.99) were the only independent predictors of postoperative death. Left ventricular ejection fraction (p < 0.0001, O.R.: 0.93, 95%C.I.: 0.91 to 0.96) and redo operation (p = 0.008, O.R.: 10.70, 95%C.I.: 1.84 to 62.22) were independent predictors of development of low cardiac output syndrome, and history of myocardial infarction (p = 0.03, O.R.: 4.20, 95%C.I.: 1.15 to 15.26) was the only independent predictor of postoperative cerebrovascular complications.

Figure 2 depicts the increase in risk of postoperative death by increasing preoperative serum concentration of C-reactive protein and decreasing preoperative left ventricular ejection fraction.



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  		Fig 2. Progressive increase of postoperative mortality rate by increasing preoperative serum concentration of C-reactive protein and decreasing preoperative left ventricular ejection fraction in 443 patients (p<0.0001).

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
Acknowledgments
 References
 
Identification of factors associated with an increased risk to develop complications after surgery is of main importance for an adequate preoperative patients selection, indicating the need of optimization of patients' condition before surgery or cancellation of the operation for those with an excessively high operative risk. Furthermore, identification of such risk factors and their inclusion in specific methods of risk stratification permits evaluation of the quality of treatment. Major efforts have been made to develop scoring methods for patients undergoing cardiac surgery, however, the complexity of surgical and anesthesiologic management of these patients along with the burden of extracardiac comorbidities makes any attempt to preoperative risk stratification rather difficult. Although a few scoring systems have been shown to be good predictors of outcome after cardiac surgery, they invariably suffer a certain inaccuracy in predicting the individual risk of postoperative death [16–18]. This leads to continuous efforts to identify those risk factors and stratifying risk models which better predict the risk of postoperative mortality and morbidity.

During the last decade, CRP has emerged as an important predictor of cardiovascular events in healthy subjects and in those with known coronary artery disease. Interestingly, CRP has been shown to be a strong predictor of early and long-term outcome after percutaneous coronary intervention [9–13]. Furthermore, it is also an important predictor of the outcome after peripheral vascular surgery [19–21]. A few studies showed an increased risk of adverse postoperative events in children and adults with increased preoperative serum levels of CRP undergoing cardiac surgery [22–26]. However, only two recent small studies have specifically addressed this topic in patients undergoing CABG. Gaudino et al. [14] showed in a series of 113 patients that those with preoperative levels of CRP > 0.5 mg/dL did not have an increased risk to develop postoperative adverse events [14]. Milazzo et al. [15] showed in a series of 86 patients who underwent CABG that patients with a preoperative serum level of CRP>=0.3 mg/dL had a significantly increased risk to experience late ischemic events. However, this small series also showed that preoperative CRP levels did not have any impact on the immediate outcome of these patients.

The present study showed that preoperative serum concentrations of CRP>=1.0 mg/dL is associated with a significantly increased risk of overall postoperative death, cardiac death and low cardiac output syndrome. Interestingly, preoperative serum concentration of CRP was an independent predictor of postoperative death along with left ventricular ejection fraction. Figure 1 shows the clear differences in postoperative mortality rates with increasing CRP concentrations and decreasing left ventricular ejection fraction. It is worth noting that preoperative serum levels of CRP>=1.0 mg/dL was particularly associated with lower left ventricular ejection fraction, New York Heart Association class IV, and the need of urgent/emergency operation. This observation suggests that beside the well recognized association between CRP and coronary artery disease, the former may be also a marker of depressed ventricular function in these patients.

Peripheral levels of proinflammatory cytokines have been shown to increase in direct relation to increasing heart failure symptomatology [27, 28]. Also CRP is significantly increased in the serum of patients with chronic heart failure [27, 29–31] and it is an independent predictor of readmission to the hospital and mortality [26]. Niebauer and colleagues [29] observed an increase in endotoxin levels in patients with chronic heart failure during acute edematous exacerbations events, which was associated with significantly increased concentrations of inflammatory markers such as CRP. The authors suggested that this increase in plasma endotoxin is likely due to bacterial translocation from the bowel as a result of altered gut permeability secondary to mesenteric venous congestion [29]. Activation of the immune system can also be related to peripheral hypoxia occurring in chronic heart failure, but this mechanism does not seem to be the most important trigger of cytokine production [32]. However, the exact sites and mechanisms of production of inflammatory mediators in patients with chronic heart failure are not yet clearly identified.

The partially retrospective nature represents a major limitation of this study. The lack of specified CRP values below 1.0 mg/dL in most patients of this series is another relevant limitation. In fact, this prevented the analysis of the data considering CRP as a continuous variable and the identification of a cut-off value for prediction of postoperative adverse outcome. Because of this, CRP was, herein, necessarily considered as a categorical variable. Anyway, a cut-off value of 1.0 mg/dL demonstrated a good specificity and accuracy for prediction of postoperative adverse events, but its sensitivity was unsatisfactory. A large prospective study by Chew et al. [10] showed that the 30-day mortality rate after percutaneous coronary intervention was 4.1% among patients with preprocedural serum levels of CRP > 1.01 mg/dL, whereas it was 0.2% among those with preprocedural CRP <= 1.00 mg/dL, thus somewhat substantiates the value of a cut-off level of CRP of 1.0 mg/dL as herein used.

In conclusion, preoperative serum concentration of CRP in patients undergoing on-pump coronary artery bypass surgery is an important determinant of postoperative outcome. It is not yet clear whether CRP is just a marker of the severity of coronary artery disease or it may also represent a potential target for preoperative optimization of patient's conditions.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
References
 
Dr Biancari was supported by a grant of the Einar and Karin Stroems Foundation which is kindly acknowledged.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

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