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Ann Thorac Surg 2010;89:578-584. doi:10.1016/j.athoracsur.2009.10.054
© 2010 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

Intraoperative Hyperglycemia and Postoperative Bacteremia in the Pediatric Cardiac Surgery Patient

James E. O'Brien, Jr, MD*, Jennifer A. Marshall, BSRT, Marcy L. Tarrants, PhD, Richard E. Stroup, Gary K. Lofland, MD

Cardiovascular and Thoracic Surgery Department, The Children's Mercy Hospitals and Clinics, Kansas City, Missouri

Accepted for publication October 23, 2009.

* Address correspondence to Dr O'Brien, Cardiovascular Surgery Department, The Children's Mercy Hospital and Clinics, 2401 Gillham Rd, Kansas City, MO 64108 (Email: jobrien{at}cmh.edu).

Presented at the Fifty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Austin, TX, Nov 5–8, 2008.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Background: Intraoperative hyperglycemia has been found to be associated with a higher incidence of postoperative infections in the adult cardiac surgery population. The goal of this study was to determine the association of intraoperative hyperglycemia and postoperative bacteremia in the pediatric population.

Methods: A retrospective chart review of all cardiac surgical cases for patients 18 years of age or younger requiring cardiopulmonary bypass support between June 2002 and July 2007 yielded 1,132 total cases representing 992 unique patients. Patient demographic and clinical data of interest were collected. Descriptive statistics and regression analyses were performed to investigate the hypothesized relationship between glucose levels and infection rates.

Results: From the 992 patient records examined, 15 patients exhibited a bacteremia within 14 days of surgery (1.5%). The association between the highest glucose during cardiopulmonary bypass and bacteremia reached statistical significance when the glucose level reached 175 mg/dL ({chi}2 = 4.59, 1 degree of freedom; p = 0.032). A patient was more than three times as likely to have a postoperative bacteremia when the glucose level reached this amount or exceeded it (odds ratio, 3.3, 95% confidence interval, 1.04 to 10.39). Ten of the 15 (66.7%) postoperative infections occurred in patients with peak bypass glucose levels of at least 175 mg/dL.

Conclusions: Intraoperative hyperglycemia was found to be associated with a higher risk of postoperative bacteremia in the pediatric cardiac surgery population.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 References
 
Intraoperative hyperglycemia has been found to be associated with a higher incidence of postoperative infections in the adult cardiac surgery population [1, 2]. In addition, appropriate treatment with aggressive insulin management has been shown to decrease the risk of infection in the adult postoperative cardiac patient. The Portland Diabetic Project has shown that normalization of perioperative hyperglycemia in diabetic patients undergoing open heart surgery decreases the incremental morbidity and mortality risks associated with the diabetic population [1].

In the pediatric population, postoperative hyperglycemia has been shown to be associated with increased morbidity and mortality after neurologic trauma and burns and in neonates with necrotizing enterocolitis [3–6]. Hyperglycemia has also been associated with worse outcomes in critically ill patients [7, 8]. In addition, there has been recent evidence that hyperglycemia is also associated with poor outcomes in the pediatric cardiac patient [9].

This study was designed to further examine the risks associated with intraoperative hyperglycemia in the pediatric cardiac surgery population. More specifically, an examination of the incidence of postoperative infectious complications associated with intraoperative hyperglycemia was performed. This investigation was motivated by the underlying hypothesis that in the pediatric population, hyperglycemia during cardiopulmonary bypass (CPB) would increase the risk of the patient exhibiting bacteremia in the postoperative period.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 References
 
Appropriate and necessary approvals from the institutional review board were obtained before study-related activities. A retrospective chart review to collect data from the medical records of all patients 18 years of age or younger at the time of surgery who underwent repair of a congenital heart defect using CPB from June 2002 to July 2007 was performed. Demographic characteristics including age at time of surgery, weight at time of surgery, sex, and cardiac diagnosis were obtained (Table 1). Operative characteristics collected included surgical procedure, CPB and aortic cross-clamp durations. Each surgery was also assigned a score using the Risk Adjustment for Congenital Heart Surgery 1 (RACHS-1) guidelines [10].


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  		Table 1 Study Population Data a
 
For each patient, the CPB perfusion record was reviewed and the highest glucose while on CPB was recorded. From June 2002 until June 27, 2005, a Sure-Step Glucometer (Johnson and Johnson Services, Inc, Langhorne, PA) was used to evaluate the glucose levels of patients during CPB. On June 28, 2005, our institution began to use the Bayer Rapidpoint 400 (Bayer Healthcare, Leverkusen, Germany) for evaluation of glucose levels. The Bayer Rapidpoint 400 is still being used in our operating rooms. Both machines underwent quality control testing on a daily basis as well as on a quarterly basis. During CPB, blood glucose was measured approximately every 10 minutes and at the discretion of the perfusionist from a sample of blood drawn from the CPB circuit.

Protocol for all patients undergoing CPB procedures required them to receive 1 g of cefazolin before incision. Alternative antibiotics were used in cases of patient allergies. Patients continued to receive antibiotics postoperatively until all chest tubes had been removed. The CPB circuit priming solution also included 1 g of cefazolin. During the period of this study, hyperglycemia during CPB was treated at the discretion of the anesthesiologist. Patients were generally treated with insulin only if their glucose level reached in excess of 250 mg/dL. The CPB circuit priming solution included 30 mg/kg methylprednisolone, up to a maximum of 1 g, for each patient.

In addition, the highest recorded blood glucose level for each of the postoperative days was collected from the medical record. The microbiology results for each patient were obtained by querying the database of the microbiology laboratory. All positive cultures, including blood, respiratory, urine, and wound sources, were collected.

A positive blood culture (including positive bacterial, fungal, or yeast culture) reported by the microbiology laboratory during the first 14 days after a patient's surgical procedure was deemed a bacteremia if the patient also experienced signs or symptoms of infection or the infection was treated by the physician. Postoperative hyperglycemia was defined as the number of consecutive days after an operation that a patient experienced at least one glucose value of at least 126 mg/dL, this level being the American Diabetes Association definition of hyperglycemia [11]. Postoperative hyperglycemia was also evaluated by examining the number of days that a patient experienced a glucose level of at least 175 mg/dL, per the findings of this study that showed an association between this glucose level and infection development.

Risk factors for postoperative bacteremia were evaluated using logistic regression; {chi}2 tests were used when examining categorical variables. Statistical analyses were performed using SPSS version 17.0 (SPSS, Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 References
 
One thousand one hundred thirty-two cardiovascular surgical procedures requiring CPB were evaluated for this study. Of those procedures, there were 992 unique patients. A summary of the study population's characteristics can be found in Table 1. The glucose values for the cohort ranged from 64 to 395 mg/dL. Of the 992 unique patients, 15 experienced a positive postoperative blood culture (bacteremia as defined above; 1.51%) within 14 days after surgery.

The incidence of positive respiratory cultures was 17.5% (174 of 992 patients), and the incidence of positive urinary cultures was 6.3% (62 of 992 patients). The incidence of mediastinitis for our cohort of patients was 5 of 992 patients (0.50%), and was not determined to be statistically significant with the variables discussed.

Logistic regression was performed to investigate the relationship between the following variables and the incidence of postoperative bacteremia: patient weight, preoperative glucose level, preoperative hematocrit level, the length of time the patient was on CPB, the lowest hematocrit on CPB, the highest glucose the patient experienced on CPB, the immediate postoperative glucose level, the immediate postoperative hematocrit, and the RACHS-1 score of the procedure. Only the highest glucose on CPB was found to be statistically significant for postoperative bacteremia (Table 2). The analysis showed that each intraoperative increase of 1 mg/dL in glucose level was related to a patient having a 1.0% increased risk of postoperative bacteremia (odds ratio, 1.01; 95% confidence interval, 1.004 to 1.019; p < 0.004). The probability values for all other variables examined were all greater than 0.1; therefore no multivariate analysis was performed. There was no correlation seen with either respiratory or urine cultures and the highest blood glucose levels while on CPB.


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  		Table 2 Univariate Regression Analysis Probability Values a
 
Further analysis was performed to determine the glucose level above which the risk of developing postoperative bacteremia would be statistically significant. The association between the highest glucose during CPB and bacteremia became statistically significant when the glucose level reached 175 mg/dL ({chi}2 = 4.59, 1 degree of freedom; p = 0.032). Figure 1 illustrates the level at which the association became statistically significant by the use of both the Pearson {chi}2 and Fisher's exact tests. At glucose levels less than 147 mg/dL, the expected count of some cells in the {chi}2 analysis fell below five. Because of this, and for consistency throughout the entire range, the more conservative Fisher's exact test was used to determine the probability values instead of the Pearson {chi}2 test. At a glucose level of 175 mg/dL, the Fisher's exact test probability value fell below 0.05 and stayed below this level from that point onward.


Figure 1
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  		Fig 1. Analysis by {chi}2 test of highest glucose on cardiopulmonary bypass (CPB) and postoperative bacteremia. Analysis was performed to determine the glucose level at which statistical significance was achieved and maintained from that level and greater. The point of significance was found to be at a glucose level of at least 175 mg/dL. The dotted line indicates significance when using Fisher's exact test and the straight line indicates significance when using the Pearson {chi}2 test. (A) Range of glucose levels from 105 to 200 mg/dL during cardiopulmonary bypass are shown. (B) The subset of glucose levels during cardiopulmonary bypass between 160 and 180 mg/dL are shown.

 
A patient was more than three times as likely to be diagnosed with postoperative bacteremia when the glucose level reached or exceeded the level of 175 mg/dL (odds ratio, 3.3; 95% confidence interval, 1.04 to 10.39). Five hundred twenty-two patients had an intraoperative glucose level on CPB less than 175 mg/dL (52.6%), and of these patients, 4 exhibited a postoperative bacteremia (0.8%). There were 470 patients whose highest glucose on CPB was at least 175 mg/dL (47.4%); of these patients, 11 experienced a postoperative bacteremia (2.3%). A listing of the types of bacteremias identified in this study can be found in Table 3.


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  		Table 3 Blood Infections Within 14 Days of Surgery a
 
Demographic data, as well as CPB and RACHS-1 scoring data, for the 15 infected patients can be found in Table 1. The highest intraoperative glucose values for the 15 infected patients ranged from 138 to 336 mg/dL. The medical records of these patients were also examined for possible commonalities, such as prematurity, syndromes, cardiac diagnosis, and procedure performed. The data showed no common connection among the 15 patients. Additional examination of a potential association between the age of a patient at the time of surgery and postoperative bacteremia was undertaken. For this analysis, the data were separated into three groups: neonates (≤30 days), infants (>30 days and ≤1 year), and children (>1 year). Owing to the low number of events in each category, statistical significance could not be determined.

Investigation of the relationship between the number of postoperative days with a hyperglycemic event (blood glucose ≥126 mg/dL) and postoperative bacteremia was carried out. There was no statistical significance found between the number of consecutive postoperative days a patient experienced hyperglycemia and the patient experiencing postoperative bacteremia (p = 0.989). The number of days a patient experienced postoperative blood glucose levels of at least 175 mg/dL was also examined for correlation with postoperative bacteremia. No statistical significance was found during this examination either (p = 0.568).


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 References
 
This study examines the association between intraoperative hyperglycemia and postoperative bacteremia in the pediatric cardiac surgical population. These data show that there is an association between an intraoperative glucose level of at least 175 mg/dL and the development of a postoperative bacteremia.

Although limited to the adult population, it is interesting to note that the American Association of Clinical Endocrinologists and the American Diabetes Association in a joint consensus statement published in June 2009 recommended that "insulin infusion should be used to control hyperglycemia in the majority of critically ill patients in the ICU [intensive care unit] setting, with a starting threshold of no higher than 180 mg/dL" [12]. The recommended threshold for treatment is remarkably near to the level at which our data showed significance for the development of postoperative bacteremia.

Previous studies have examined the effect of hyperglycemia on morbidity and mortality in the pediatric population. Yates and colleagues [9], in a study of high-risk neonates and infants undergoing cardiac surgery, demonstrated that hyperglycemia in the postoperative period was associated with an increased risk of morbidity and mortality. Although their study did not examine bacteremia as an individual outcome, it was incorporated into a composite morbidity score.

Different conclusions on the effect of hyperglycemia on postoperative adverse effects were drawn from a study by Rossano and associates [13]. Their group examined glucose levels in the first 24 hours postoperatively for 93 infants undergoing arterial switch operations. This study found that postoperative hyperglycemia did not appear to be detrimental to the patients, and patients in the group with a lower average glucose were more likely to have an adverse event. The incidence of bacteremia was not examined in isolation, nor were the glucose levels while on CPB included in the analysis. The study population was also a homogeneous group of neonates (with a known risk for consequential hypoglycemia), whereas our study includes a much larger and heterogeneous population.

Polito and associates [14] examined intraoperative and postoperative variables for 378 pediatric patients who underwent procedures of RACHS-1 category 3 or greater and their association with morbidity and mortality. This study found that intraoperative glucose levels of 75 mg/dL or less were associated with an increased incidence of a patient reaching the composite morbidity-mortality end point, of which infection was included. However, this study did not find an association between intraoperative hyperglycemia and the composite morbidity-mortality end point. Of the intraoperative glucose variables examined, none were significantly associated with the primary study end point of patient length of stay. However, the duration of hyperglycemia in the first 72 hours postoperatively was significantly associated with longer hospitalization.

There are multiple studies in the adult postoperative cardiac surgical population demonstrating increased morbidity and mortality in association with hyperglycemia [1, 15–17]. Gandhi and associates [2] examined the relationship between intraoperative glycemic levels and postoperative complications. It was found that intraoperative hyperglycemia was associated with a higher incidence of a patient reaching a study event (death or infectious, neurologic, renal, cardiac, or pulmonary complications within 30 days of surgery). Lantham and colleagues [16] reported that for postoperative cardiac surgery patients, the greatest risk for developing a surgical site infection was among those patients with hyperglycemia (glucose >200 mg/dL) or undiagnosed diabetes. Estrada and associates [17] found perioperative hyperglycemia (in both diabetic and nondiabetic patients) to be associated with longer postoperative lengths of stay and increased hospitalization charges and costs. This study also stated that a target glucose range of less than 150 mg/dL was favorable for maintaining euglycemia. Van den Berghe and associates [18] found that controlling the glucose levels in patients to a range of 80 to 100 mg/dL reduced mortality during intensive care unit stay from 8.0% to 4.6%.

One of the proposed mechanisms for the association between hyperglycemia and increased risk of infection is the nonenzymatic glycation of proteins. This occurs at a blood glucose level of 180 mg/dL [19–24]. Black and colleagues [19] examined the glycation of immunoglobulin in rats. This study found that immunoglobulin that had been glycated was inactivated and therefore predisposed the rats to a higher incidence of infection. Our study demonstrated a correlation between glucose levels of 175 mg/dL or greater and postoperative bacteremia. This is very near the level at which glycation reportedly occurs.

There are many hypotheses as to why patients experience hyperglycemia while on CPB, including hyperthermia, hyperoxia, decreased insulin secretion, hypokalemia, and hypocalcemia [25–28]. In addition, the administration of catecholamine-based inotropic agents as well as glucocorticoids has been implicated as a cause for hyperglycemia during CPB [29].

There were several limitations to this study. This study was retrospective and was thus limited by the data collection processes and liable to the possibility of incomplete collection. An additional limitation to this study was the heterogeneity of our population; specifically in procedure complexity, age, and weight. The ages and weights of our patients encompassed a wide range; however age was not found to be associated with the development of a postoperative bacteremia. For more accurate and complete data, a prospective trial would need to be implemented.

Importantly, our data show an association between hyperglycemia on CPB and postoperative bacteremia. They do not show causation. It is possible that this association also involves a factor outside the scope of this study. It is possible, however, that the treatment of hyperglycemia may mitigate the effect of the other contributing factor by decreasing the method by which the risk is imparted to the patient. Therefore, hypothetically, the elimination of hyperglycemia during higher complexity procedures may mitigate some of the increased risk associated with this cohort by disrupting a cascade of events leading to an increased risk of infection.

During the period of this study it was not standard practice for the glucose levels of patients to be controlled with insulin during CPB unless the levels were in extreme ranges (>250 mg/dL). In the future, further scrutiny will be given to intraoperative glucose levels being monitored and potentially controlled more closely. This new information may therefore result in a decrease in the incidence of postoperative bacteremia. A prospective, randomized trial, separating patients into cohorts of different glucose and insulin protocols, would be needed to examine this topic further.

The measurement of postoperative blood glucose levels was also not standardized and was left to the discretion of the physician. This may help to explain why postoperative hyperglycemia was not found to be significant for the development of bacteremia. It is possible that instituting future postoperative protocols for glucose evaluation may find statistical significance for developing an infection during this time frame as well.

This work lays the foundation for an expanded study to investigate the effects of hyperglycemia on morbidity and mortality after pediatric cardiac surgery. The impetus to investigate the effects of hyperglycemia is the possibility that tight glucose control may impart an outcomes advantage in children after cardiac surgery as has been demonstrated in adults [1, 16, 30].

In conclusion, the highest glucose on CPB was found to be associated with bacteremia in the postoperative period. This association became statistically significant at a glucose level of at least 175 mg/dL. A future prospective, randomized trial would be necessary to examine the effect of glucose management designed to prevent hyperglycemic episodes on postoperative bacteremia in the pediatric cardiac surgery patient.


   Discussion
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
References
 
DR J. WILLIAM GAYNOR (Philadelphia, PA): Thank you very much, Jim, that was very nice. As you noted, perioperative hyperglycemia has been identified as a risk factor for adverse outcomes, including infection and neurodevelopmental dysfunction in adults. However, findings in adult studies do not necessarily translate to pediatric patients. In your study, you have shown in a patient population ranging from newborns to adolescents that even modest levels of intraoperative hyperglycemia are associated with an increased risk of postoperative bacteremia. However, as you noted, glucose metabolism, especially in the brain, is very different in neonates compared to adults. Previous studies at the Children's Hospital of Philadelphia, Boston Children's Hospital, and Texas Children's Hospital have differed from your conclusions and identified no adverse effects of even marked perioperative hyperglycemia both in terms of infection and neurodevelopmental outcomes. However, hypoglycemia is associated with worse outcomes, especially an increased risk of postoperative seizures. So given that we know that there are differences in glucose metabolism in your cohort, is the relationship between hyperglycemia and postoperative infection the same for neonates as for adolescents, who may act more like adult patients?

In the manuscript, which I thank you for letting me see, you report that you evaluated the relationship between postoperative hyperglycemia and infection. In contrast to the results just presented, you identified no association between early postoperative hyperglycemia and infection. This is consistent with studies from our institution and other institutions. You hypothesized in the manuscript that the mechanism by which hyperglycemia increases the risk of infection is nonenzymatic glycosylation of proteins. If this is indeed the mechanism, it should be operative in both the intraoperative period and postoperative period. That is, hyperglycemia both during surgery and early after surgery should result in the same risk of protein dysfunction and increase the risk of infection. So my second question is, how do you reconcile the discrepant findings for intraoperative and early postoperative hyperglycemia in terms of the risk of infection?

And finally, also in the manuscript you call for a prospective trial of tight glucose control in children undergoing cardiac surgery. We know that tight control in this patient population, particularly in newborns, increases the risk of hypoglycemia. So given the known and well-documented adverse effects of hypoglycemia in newborns, do the uncertain benefits of avoiding hyperglycemia justify accepting the known risk of treatment-induced hypoglycemia in this population?

Thank you very much. It is a great study.

DR O'BRIEN: Thank you, Bill, for your kind comments and for your typically insightful questions. In answer to your first question involving the neonates and the difference with the neonatal population in terms of their glycemic reserve, we analyzed three different age groups: the neonatal population, that being a month and younger, and then an infant, being from a month to a year, and then older than a year. What we did show was that there was no difference in any incidence of bacteremia. But what we need to do, as you suggest, is go back and look at those three different age groups and see if the association between hyperglycemia in the neonates is the same as it is with the older population, or is what we are seeing in the adolescent and pediatric age group similar to what is found in adults, and the neonates are different.

In terms of the mechanism and why we see a difference with intraoperative as opposed to postoperative hyperglycemia, although I didn't show the data, we did look at our postoperative hyperglycemia and also did not find an association there as other groups have shown.

We are all aware that the physiology on cardiopulmonary bypass is obviously different; there is an altered physiologic state with a revved-up immune system. And it is conjecture, but maybe there is some additive effect with the physiology on bypass in addition to the hyperglycemia that puts the patient more at risk for developing postoperative bacteremia or has more of an effect on immunomodulation causing there to be an increased risk. But this is certainly an area that is wide open for investigation.

In order to see if tight glucose control with an aggressive insulin management or glucose management while on bypass is beneficial, we certainly would need a prospective trial. Now, in terms of what levels to look at, I think one would have to look at various levels. If you can extrapolate from the adult guidelines for nondiabetic patients, they pick a level of 180 mg/dL. This seems logical because it corresponds to the level in some of the animal studies, which show some of the immunomodulation effects of hyperglycemia. As you alluded to, the nonenzymatic glycosylation, the effect on the neutrophils, et cetera, seems to take place at about 180. Now, our data would seem to indicate that you might need even tighter control, but you certainly in the neonatal population would have to set levels with a cautious eye towards the risk of hypoglycemia, which is much more real in the neonatal population.

DR DAVID A. FULLERTON (Aurora, CO): Just a couple of questions. Acknowledging it is a retrospective study and it is sometimes difficult to track down some of these variables, but the first question that occurred to me was, when did the bacteremia occur? Was this the sort of thing that happened early postoperatively or is this some kid that is parked in a corner that has had a lot of problems? Secondly, is there any way that you have been able to control for other factors that may contribute to infection, the degree of illness after the operation or before the operation, use of inotropes, et cetera? Thirdly, although you were able to control for the RACHS score, is there any way to drill into more precision on which of the kids actually became bacteremic?

Thank you.

DR O'BRIEN: Thank you for your questions. In terms of the first question, these are fairly early postoperative septicemia episodes. We are looking at a large population, and it is a retrospective study, but our mean length of stay for this population is on the order of a week. Certainly there were some patients who had a longer postoperative stay, but overall, the incidence of bacteremia was an early bacteremia that was seen during these short postoperative stays.

This study serves as a foundation for us to go on and examine some further aspects in the data in terms of broader outcome measures, but also in terms of the covariates that are involved. So looking at the RACHS scores and other covariates, such as the effect of blood transfusion during bypass, to see if that had an effect on the rate of infection and also on hyperglycemia, we need to go back and look at that. But even if there is an association with a third unknown factor, it is possible that the hyperglycemia is what is imparting some of the risk from those other factors, be that the high RACHS score or blood transfusions. It is possible the hyperglycemia is a causative link for part of that risk, and therefore if you control that hyperglycemia, hypothetically do you mitigate some of the risk associated with those unknown factors?

DR CARL L. BACKER (Chicago, IL): Jim, your study may have raised more questions than you have answered, but one of the things I was struck by was your relatively low incidence of clinically significant infections. I wonder if you could just briefly tell us two things: (1) what is your strategy for antibiotic dosing, and (2) what is your strategy for the use of steroids, which of course can elevate the glucose, but have beneficial antiinflammatory effects?

DR O'BRIEN: Thank you, Carl. Our antibiotic strategy is simply Ancef perioperatively. At the present time we are using Ancef for the length that the chest tubes are in place, but I think we are going to start to tailor that down, as we all are being pressured by hospitals in terms of their ID surveillance in order to decrease the use of antibiotics. But it is simply the use of Ancef at the present time.

All the patients do receive steroids on pump dosed at 30 mg/kg up to a dose of a gram. That does certainly have the chance to raise the glucose levels on bypass and also obviously has an immunomodulatory effect, but it is the same throughout the whole patient population.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

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