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Ann Thorac Surg 2009;87:1859-1865. doi:10.1016/j.athoracsur.2009.02.066
© 2009 The Society of Thoracic Surgeons
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Right arrow Cardiac - physiology

Original Articles: Adult Cardiac

Cardiopulmonary Bypass Increases Postoperative Glycemia and Insulin Consumption After Coronary Surgery

Piotr Knapik, MD, PhDa,*, Pawel Nadziakiewicz, MDa, Ewa Urbanska, MDa, Wojciech Saucha, MDa, Miroslawa Herdynska, MDb, Marian Zembala, MD, PhDb

a Department of Cardiac Anesthesia, Silesian Centre for Heart Diseases, Zabrze, Poland
b Department of Cardiac Surgery, Silesian Centre for Heart Diseases, Zabrze, Poland

Accepted for publication February 23, 2009.

* Address correspondence to Dr Knapik, Silesian Centre for Heart Diseases, ul. Szpitalna 2, Zabrze, 41-800, Poland (Email: kardanest{at}sum.edu.pl).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Perioperative hyperglycemia should be avoided in patients undergoing coronary surgery. The aim of our study was to find out what the influence of cardiopulmonary bypass is on postoperative glycemia and insulin consumption in patients with and without diabetes mellitus undergoing coronary artery surgery and whether a marked hyperglycemia in the early postoperative period is among the factors associated with early mortality and morbidity.

Methods: We retrospectively reviewed all patients who underwent first-time coronary artery surgery in our institution during the 11-month period. Among 814 patients, 239 patients (29.4%) had diabetes and 575 patients (70.6%) were nondiabetic. Blood glucose levels were registered every 2 hours in all patients during the first 24 postoperative hours. Outcomes were difficult glycemic control (postoperative blood glucose levels >11.0 mmol/L despite aggressive insulin treatment), hospital mortality, and morbidity (defined as any postoperative complication such as stroke, renal failure, wound infection, perioperative myocardial infarction, ventilation > 24 hours, sepsis, and multiorgan failure).

Results: Glycemic control was significantly worse in patients who underwent coronary artery bypass grafting, in comparison with off-pump coronary artery bypass grafting surgery, particularly in nondiabetic patients. Patients with difficult glycemic control had more serious postoperative complications resulting in higher mortality (2.5% versus 0.4%; p = 0.02). In the multivariate analysis, difficult glycemic control was significantly associated with a female sex (odds ratio [OR], 2.36), presence of diabetes (OR, 2.22), and the usage of cardiopulmonary bypass (OR, 1.81). Mortality was significantly associated with the left ventricular ejection fraction less than 0.35 (OR, 7.38), difficult glycemic control (OR, 7.06), and previous stroke (OR, 5.66). Difficult glycemic control was also significantly associated with postoperative morbidity (OR, 1.87).

Conclusions: Cardiopulmonary bypass increases postoperative glycemia and insulin consumption in both diabetic and nondiabetic patients. The use of cardiopulmonary bypass during coronary artery surgery in diabetic women is associated with a more difficult glycemic control in the early postoperative period. Difficult glycemic control is significantly associated with early mortality and morbidity in patients undergoing coronary artery surgery.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Hyperglycemia is one of the independent factors worsening the prognosis in patients with both acute coronary syndromes and those undergoing coronary artery surgery as diabetes increases the risk of cardiac surgery nearly twofold [1, 2]. A negative influence of hyperglycemia in the perioperative period has been confirmed in both diabetic and nondiabetic patients [2, 3]. Prolonged periods of hyperglycemia cause higher mortality and morbidity, more frequent infections, hemodynamic impairment, and increased platelet aggregation as well as longer and more expensive hospital stays [4–8]. Maintenance of blood glucose levels below 150 mg% in the postoperative period was reported to decrease early perioperative mortality and morbidity after cardiac operations [3]. There is currently no doubt that effective postoperative glycemic control is extremely important to avoid postoperative complications [3, 9, 10].

Coronary artery surgery may be performed with or without cardiopulmonary bypass. Coronary artery bypass graft surgery with cardiopulmonary bypass (CABG) and off-pump coronary artery bypass graft surgery (OPCAB) have been already compared in several clinical trials. The outcomes are generally similar; however the avoidance of cardiopulmonary bypass seems to be beneficial for certain subgroups of patients [11, 12].

The association between the use of cardiopulmonary bypass and perioperative hyperglycemia is not well defined. We therefore aimed to answer the question, whether the use of cardiopulmonary bypass has an influence on postoperative glycemia and insulin consumption in patients with and without diabetes mellitus after coronary artery surgery. We also aimed to establish whether the appearance of marked hyperglycemia in the postoperative period (despite strict control by insulin infusion) is associated with early mortality and morbidity.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
We performed a retrospective review of data of all patients who underwent first-time coronary artery surgery during the 11-month period. The study was performed in a tertiary-care university hospital, performing approximately 1,700 cardiac surgical procedures per year. The study was approved by the institutional ethics committee, and the individual patient's consent was not required.

Patients
All 848 consecutive, first-time coronary artery patients who underwent first-time coronary revascularization were extracted from the hospital database. After analysis of the clinical data, 34 patients were excluded: 4 were in the critical preoperative condition (cardiogenic shock), 19 patients had incomplete medical records, 10 patients underwent a separate fast-track program and stayed in the intensive care unit less than 12 hours, and 1 patient underwent urgent reoperation and died in the operating theater on the first postoperative day.

Among the remaining 814 patients, 239 patients (29.4%) had diabetes and 575 patients (70.6%) were nondiabetic preoperatively. We further subclassified 239 diabetic patients on the basis of their glucose control at the time of surgery into 112 patients taking insulin (46.9%), 93 patients taking oral medications (38.9%), and 34 patients using dietary control only (14.2%).

Preoperative risk assessment was performed on the basis of EuroSCORE classification, and patients were classified as having low risk (0 to 2 points), moderate risk (3 to 5 points), or high risk (6 or more points) [13].

Blood Glucose Levels
Blood glucose levels were determined by automated analyzer (Bayer M865, Germany) and were registered every 2 hours in all patients during the first 24 postoperative hours. Additional blood samples were taken in between these measurements if necessary, but these results were not included in the statistical analysis. In a given period, 9,076 measurements were performed (mean, 11.2 measurements; 7 to 12 measurements per patient).

All blood glucose measurements in the first 24 hours after admission to the postoperative intensive care unit were collected from the case notes. Intensive care unit charts were analyzed, and the overall insulin requirement for the first 24 postoperative hours (including infusion and bolus doses) was calculated for each patient.

From these data, the peak and lowest glucose levels were identified for each patient. Mean glucose levels (from all 13 measurements) and individual glycemia range (per patient) were also separately calculated for each patient. In the first 24 hours glycemia is managed in our institution with intravenous insulin infusion only, according to the protocol proposed by Furnary and colleagues [3]. Starting from postoperative day 2, glycemia is managed with further insulin infusion (if necessary) or either subcutaneous insulin, oral hypoglycemic medication, or diet.

Data Analysis
Perioperative morbidity and mortality was analyzed. Cumulative incidence of the most common complications (stroke, renal failure, wound infection, perioperative myocardial infarction, ventilation > 24 hours, and sepsis or multiple-organ dysfunction syndrome) was defined as morbidity; for the calculation of early mortality all deaths in the first 30 postoperative days were noted.

Stroke was defined as a new focal or global dysfunction of cerebral function lasting longer than 24 hours. Renal failure was defined as renal dysfunction requiring renal replacement therapy. Wound infection was recognized on the basis of the US Centers for Disease Control and Prevention definition [14]. Myocardial infarction was defined as any new Q wave or disappearance of R wave on postoperative electrocardiogram or troponin I level of 3.9 µg/L or greater within 24 hours of the operation [15]. Sepsis was defined as the clinical signs describing systemic inflammatory response syndrome together with definitive evidence of infection whereas multiple-organ dysfunction syndrome was defined as a severe dysfunction of at least two organ systems lasting for more than 24 hours, as stated by the Consensus Conference of the American College of Chest Physicians and the Society of Critical Care Medicine [16].

The decision about which data were going to be extracted and analyzed was made before the start of the trial. All data were extracted from the case notes directly into the computer in a standardized manner. All data of 40 randomly chosen patients (5%) were extracted by a second, independent investigator with the achievement of 94% agreement. The accuracy of data extraction regarding the usage of definitions for perioperative morbidity was assessed in 16 randomly chosen patients (2%) by one of the main authors of the study, who at the time of the assessment, was blinded to the information of which patients were diabetic or nondiabetic and which patients were operated on with cardiopulmonary bypass or off-pump. These data were found to be in 90% agreement with the initial assessment.

Patients who underwent their operation on-pump (CABG) and off-pump (OPCAB) were compared. Analysis was performed separately for nondiabetic and diabetic patients. Comparisons included demographic and clinical data as well as early postoperative mortality, morbidity, and glycemic control. Mean blood glucose levels were also compared between CABG and OPCAB patients for the subsets of nondiabetic and diabetic patients.

Further, patients were stratified according to whether they had elevated blood glucose levels in the early postoperative period with at least one blood glucose in excess of 11 mmol/L during the first postoperative day. This level was chosen because it has been previously confirmed that any blood glucose concentration above this level correlates with an increased mortality risk in diabetic patients after acute coronary artery syndromes [17]. Patients with elevated blood glucose levels were compared with patients who had all blood glucose levels less than 11 mmol/L with regard to their demographic data, mode of operation, and diabetes status, as well as early postoperative mortality and morbidity.

Finally, a multiple logistic regression model was used to investigate the relationship of the outcomes (difficult glycemic control, mortality, and morbidity) with the preoperative and clinical variables. Independent variables that might influence outcomes were cardiopulmonary bypass usage, diabetes mellitus, insulin use, age older than 65 years, left ventricular ejection fraction less than 0.35, EuroSCORE greater than 5, Canadian Cardiovascular Society score of 4, female sex, previous myocardial infarction, previous stroke, peripheral vascular disease, previous percutaneous transluminal coronary angioplasty or stent, arterial hypertension, obesity (body mass index > 30) and—for morbidity and mortality—also difficult postoperative glycemic control (at least one blood glucose > 11 mmol/L during the first postoperative day).

Statistical Analysis
Power analysis was made on the basis of the first 20 studied patients (10 patients in each group). It was calculated that it should be at least 20 patients studied in each group to achieve a power greater than 0.8 and a significance level of 0.05, and to detect 20% difference between groups in terms of the presence of any complication (morbidity) and death in the early postoperative period.

Depending on the statistical distribution, numeric data are shown as either mean and standard deviation or median values and their range, and then compared with the Mann-Whitney U test. Binary data were shown as the number and a percentage and compared with the use of the {chi}2 test. Independent variables that might influence dependent variables (morbidity and mortality) were identified. The effect of independent variables on the outcome variables of interest (difficult glycemic control, morbidity, and mortality) was then calculated by means of univariate logistic regression, and variables with a probability value less than 0.1 were then included in the multivariate logistic regression analysis. For the final analysis a probability value less than 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Patients who underwent their operation on-pump (CABG) and off-pump (OPCAB) had similar demographic and clinical data, with only a few exceptions. Diabetic patients undergoing CABG had a higher mean left ventricular ejection fraction (0.510 ± 0.104 versus 0.486 ± 0.104; p = 0.03). Among nondiabetic patients, fewer patients with a high preoperative risk (EuroSCORE > 5) were found in the CABG group (23.3% versus 38.8%; p = 0.01).

In a comparison of CABG and OPCAB patients, glycemic control (expressed by mean postoperative glycemia, insulin consumption, glucose range, peak glucose levels, and amount of patients who reached very high glucose levels) was significantly worse in patients who underwent CABG, particularly in a group of patients without diabetes (Table 1).


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  		Table 1 Glycemia Control in Patients Undergoing Coronary Artery Bypass Grafting and Off-Pump Coronary Artery Bypass Grafting Surgery
 
Comparison of demographic and clinical data of patients with elevated (at least one result > 11 mmol/L) and not elevated blood glucose levels is shown in Table 2. Patients with difficult glycemic control (elevated glucose levels) were more likely to have diabetes (41.7% versus 22.9%; p < 0.01), be of the female sex (34.9% versus 16.6%; p < 0.01), and undergo CABG (75.9% versus 65.7%; p < 0.01). In addition, patients with elevated glucose levels clearly had worse postoperative glucose control (Table 3) and more serious postoperative complications such as perioperative myocardial infarction, intraaortic balloon pump use, or prolonged mechanical ventilation, resulting in higher mortality (Table 4). Multivariate analysis revealed that difficult glycemic control after coronary surgery was significantly associated with the female sex (odds ratio [OR], 2.36), the presence of diabetes (OR, 2.22), and the use of cardiopulmonary bypass (OR, 1.81; Table 5).


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  		Table 2 Preoperative Clinical Data in Patients With Elevated Blood Glucose Level (>11 mmol/L) and the Remaining Patients
 

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  		Table 3 Glycemia Control in Patients With Elevated (>11 mmol/L) and Not Elevated Blood Glucose Levels
 

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  		Table 4 Operative Data and Complications in Patients With Elevated (>11 mmol/L) and Not Elevated Blood Glucose Levels
 

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  		Table 5 Predictors of Difficult Glycemia Control, Morbidity, and Mortality After Coronary Surgery
 
Identification of independent variables influencing other outcomes of interest was also started with the univariate analysis. For the mortality, univariate analysis selected elevated blood glucose levels, insulin use, left ventricular ejection fraction less than 0.35, EuroSCORE greater than 5, and previous stroke as suitable variables for the multivariate analysis. For the morbidity, univariate analysis selected elevated blood glucose levels, insulin use, age older than 65 years, EuroSCORE greater than 5, female sex, peripheral vascular disease, and arterial hypertension as suitable variables for the multivariate analysis. Elevated blood glucose levels, however, were strongly correlated with the insulin use, and the EuroSCORE variable was clearly dependent on age, sex, and peripheral vascular disease, so insulin use and EuroSCORE were not included in the multivariate analysis.

Results of multivariate analysis for mortality and morbidity are also shown in Table 5. Early mortality was significantly associated with the left ventricular ejection fraction less than 0.35 (OR, 7.38), difficult glycemic control (OR, 7.06), and previous stroke (OR, 5.66). Postoperative morbidity was significantly associated with the presence of peripheral vascular disease (OR, 1.89), difficult glycemic control (OR, 1.87), age older than 65 years (OR, 1.84), and female sex (OR, 1.80).


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Our results confirm previous suggestions that cardiopulmonary bypass has a negative influence on glucose homeostasis [18]. The use of hypothermia may exacerbate this effect [19]. Our results are also in agreement with the recent study (with a sample size similar to ours) confirming that avoidance of cardiopulmonary bypass significantly reduced the number of postoperative complications in diabetic patients [20]. According to our data, various factors indicating overall quality of glycemic control (such as glucose range, peak glucose levels, or the percentage of patients who reached very high glucose levels) were worse if cardiopulmonary bypass was used. This difference was even more obvious in nondiabetic patients—this could probably be caused by the permanently increased glucose levels in the diabetic group. Apart from that, it has been previously confirmed that glucose homeostasis is already disturbed in many nondiabetic patients undergoing coronary artery bypass graft surgery [18].

Vermes and associates [21] indicated that the situation may be totally opposite and OPCAB surgery may be associated with an increased early postoperative morbidity in patients with diabetes. The results of this paper could have been influenced by the fact that more high-risk patients were scheduled for OPCAB surgery. In our study, the situation was similar—diabetic patients with high preoperative EuroSCORE were scheduled more often to the OPCAB technique (39% versus 23%; p = 0.01), but patients operated on without the use of cardiopulmonary bypass still had a similar, but slightly lower, number of postoperative complications (12.1% versus 8.8%; p = 0.21).

Despite all these facts, the mean blood glucose level curves were usually comparable in our CABG and OPCAB patients. This could be partially explained by the fact that comparison of the whole curves (instead of individual time points) usually "blunts" the statistical difference. Even if the curves were similar, mean blood glucose levels were consistently and repeatedly lower in the OPCAB group.

In our study, patients with elevated postoperative levels of blood glucose (defined as at least one result > 11 mmol/L) had strikingly more postoperative complications (particularly those associated with low cardiac output: adrenaline use, intraaortic balloon pump use, or perioperative myocardial infarction) and much higher mortality (2.5% versus 0.4%; p = 0.02). The negative effect of high glucose levels on postoperative complications was previously highlighted in many studies, including the study published by Van den Berghe and associates [10], publications by the Furnary group [3, 4], and many others [1, 9, 22, 23].

There are, however, some important limitations to our study. On the basis of our data it may not be concluded how hyperglycemia affects the prognosis of patients with specific complications, as the majority of these complications were associated with low cardiac output. Retrospective data extraction is another limitation to this study; however, in a set proportion of patients this process was repeated to confirm the acceptable quality of the hospital database. The arbitrary decision to use a cutoff point of 11 mmol/L was made because this value is easy to remember for the staff ("by all means, a blood glucose of 200 mg% should not be exceeded!") and—as previously explained—this level significantly increases the risk of death in diabetic patients with acute coronary syndromes [17].

No propensity score analysis was performed in our study. This is important, as for various comparisons we performed the groups of patients compared were usually not similar with respect to potential risk factors, but most important comparisons were performed separately for diabetic and nondiabetic patients.

Tight glucose control is limited clinically by the fact that postoperative hypoglycemia may be easily induced [24]. This is extremely dangerous in the first 24 postoperative hours, when each cardiac surgical patient is not fully alert for at least part of the time. Therefore, we always observe some patients with elevated blood glucose levels in the postoperative period.

Multivariate analysis of all significant preoperative and operative variables of both diabetic and nondiabetic patients was able to show that such factors as dangerously high blood glucose levels are more likely to happen in patients with diabetes or of the female sex, and after the operation with the use of cardiopulmonary bypass. Moreover, dangerously high blood glucose levels are among the few factors significantly associated with early mortality and morbidity in patients undergoing coronary artery surgery. This finding is supported by many previous papers, as diabetes significantly increases the risk of cardiac surgery [25, 26] and increased glucose levels are harmful if they appear in a preoperative [27], intraoperative [28], or postoperative period [5]. According to one study, the worst option is to perform coronary artery surgery in patients with undiagnosed diabetes, as these patients more frequently require resuscitation, reintubation, and prolonged postoperative ventilation [29].

The fact that female sex is a significant risk factor for perioperative morbidity was quite surprising to us; however, for some reason early results of coronary surgery are significantly worse in women [30] and women are at greater risk for acquiring surgical site infections in comparison to their male counterparts [31].

The results of our study indicate that cardiopulmonary bypass has a negative influence on postoperative glycemia and insulin consumption in both diabetic and nondiabetic patients. Postoperative complications are more common if elevated glucose levels appear despite aggressive control of glycemia by insulin infusion. This could happen particularly to women with diabetes, so the use of cardiopulmonary bypass in this group requires strict glycemic control in the early postoperative period. Elevated blood glucose levels in the postoperative period should be aggressively treated, as they are among the few factors significantly associated with early mortality and morbidity in patients undergoing coronary artery surgery.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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