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Ann Thorac Surg 2000;70:175-181
© 2000 The Society of Thoracic Surgeons

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Original articles: Cardiovascular

Association between postoperative hypothermia and adverse outcome after coronary artery bypass surgery

^a Department of Cardiothoracic Anesthesia, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
^b Department of Biostatistics, The Cleveland Clinic Foundation, Cleveland, Ohio, USA

Address reprint requests to Dr Insler, Department of Cardiothoracic Anesthesia, The Cleveland Clinic Foundation, 9500 Euclid Ave, G-58, Cleveland, OH 44195
e-mail: inslers{at}ccf.org

	Abstract

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Background. We examined the effect on outcome of mild hypothermia (< 36°C) upon intensive care unit (ICU) admission on patient outcome after coronary artery bypass grafting (CABG) with cardiopulmonary bypass (CPB).

Methods. We performed a retrospective database analysis of 5,701 isolated CABG patients requiring CPB, operated upon from January 1995 to June 1997. Patients were classified as either hypo- (< 36°C) or normothermic ( 36°C) upon ICU admission. ICU admission bladder core temperature (BCT) versus outcome was evaluated. Outcome measures included mortality, resource utilization (mechanical ventilation time, ICU and hospital length of stay, and postoperative packed red blood cell transfusion), and major morbidity (cardiac, renal, neurologic, or major infection).

Results. Overall, patients admitted to the ICU with BCT < 36°C had a significantly greater mortality (p = 0.02), prolonged mechanical ventilation (p = 0.007), packed red blood cell transfusion (p = 0.001), ICU (p = 0.01), and hospital (p = 0.005) length of stay.

Conclusions. BCT of less than 36°C, upon ICU admission, has a significant association with adverse outcome after CABG with CPB.

	Introduction

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Recent clinical evidence has shown that even the presence of mild hypothermia (ie, 36°C) in the immediate postoperative period of noncardiac surgeries is associated with multiple physiologic derangements that may lead to adverse outcomes including increased postoperative discomfort, surgical bleeding, wound infection, and longer hospital stay [1, 2].

Mild hypothermia of less than 35°C is not an uncommon consequence of general anesthesia and surgery [3]. It is well recognized that general anesthesia and the stress of surgery inhibit normal thermoregulatory control mechanisms. Without preventative actions, a mild decrease in temperature is expected in patients undergoing prolonged surgical procedures. This temperature decline can be exaggerated in surgical procedures in which major body cavities (eg, thoracic, abdominal) are exposed to a cold operating room (OR) environment.

With routine perioperative temperature maintenance, it has been shown that approximately one-half of noncardiac surgical patients still have temperature reductions intraoperatively and on recovery room admission to less than 36°C [1], and approximately one-third of all such patients have temperatures falling below 35°C [1, 4].

Before separation from cardiopulmonary bypass (CPB), the usual practice is to return cardiac surgical patients to or near normothermia (ie, 37°C). But unless active and aggressive measures are undertaken to maintain patient normothermia in the subsequent period of chest closure and transport out of the operating room, a slow temperature decrease will occur, leading to varying degrees of hypothermia upon arrival in the intensive care unit (ICU) [5].

Although there is recent literature regarding hypothermia and adverse outcome in patients recovering from general and regional anesthesia in noncardiac surgical patients, there have been no studies examining the association between hypothermia and outcome after CPB in coronary artery bypass grafting (CABG) patients. The purpose of this analysis was to investigate whether the adverse outcomes seen in noncardiac surgery patients who were allowed to become mildly hypothermic were seen in cardiac surgical patients.

	Material and methods

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Retrospective statistical analyses were performed on a sample of 5,701 isolated CABG patients.

Anesthetic management was left up to the discretion of each individual anesthesiologist. Although general guidelines were included, preoperative sedation with midazolam (0.005 to 0.05 µg/kg) was administered intravenously in the operating area as needed. Intravenous induction agents included midazolam (0.05 to 0.15 µg/kg), fentanyl (7 to 10 µg/kg), with or without etomidate (0.1 to 0.3 µg/kg), and pancuronium (0.1 to 0.15 mg/kg). Maintenance of anesthesia included up to 1.5% of inspired isoflurane before, during, and after CPB. Pancuronium was administered to maintain neuromuscular blockade at less than two twitches on a train-of-four monitor. Additional midazolam or fentanyl was administered during maintenance as needed. While on CPB, pump flows were maintained within a range of 2.0 to 2.5 L/min/m² and mean arterial blood pressure (MAP) maintained within a range of 60 to 80 mm Hg. CPB was not discontinued unless bladder core temperature (BCT) was measured at 37.0°C or more. No active warming measures were instituted after CPB. Patients were admitted directly to the ICU upon completion of the procedure. Patients admitted to the ICU with BCT less than 36.0°C were treated with forced air warming blankets until BCT more than 36.0°C was achieved.

Outcome was defined by mortality, one or more major morbidities, and hospital resource utilization represented by initial ICU endotracheal/mechanical ventilation time (ETT), units of packed red blood cells transfused in the ICU (PRBC), intensive care unit length of stay (ICU LOS), and hospital length of stay (HLOS). Major morbidity definitions were: cardiac, low cardiac output, ie, sustained cardiac index (C.I.) less than 1.8 L/min/m², despite adequate fluid replacement and inotropic support for 4 hours or more, or new myocardial infarction (electrocardiogram with creatinine kinase MB band of 50 IU or aspartate aminotransferase 80 U/L) requiring the use of an intraaortic balloon pump (IABP) or ventricular assist device (IABP and assist devices were required when vasoactive drug support failed to achieve a C.I. of > 2 L/min/m² or a mean arterial blood pressure of > 60 mm Hg without significant side effects, eg, persistent arrhythmias); prolonged mechanical ventilatory support; renal, oliguric (< 400 mL in a 24-hour period) or anuric renal failure, or institution of renal dialysis or ultrafiltration in the absence of preoperative dialysis; neurologic, documented focal or global deficit or patient died without awakening; major infection, culture proven sepsis, sepsis syndrome, septic shock, mediastinitis, major wound infection, or pneumonia; death (including all deaths during the hospitalization for the operation, regardless of length of stay).

After establishing the range of ICU admission BCT to be 30.6°C to 39°C, receiver operating characteristics (ROC) analyses were used to examine the sensitivity and specificity for temperature relationship on mortality. Once the differential temperature was generated, patients were classified as either hypothermic (H) or normothermic (N) relative to whether their BCT was above or below this cutoff.

The two BCT groups (H, < 36°C; N, 36°C) were compared using univariate logistic regression analysis (for binary outcome, such as mortality) and analysis of variance (ANOVA, for continuous outcomes, such as ICU LOS). To adjust for patient differences during the evaluation of the effect of BCT on various outcome measures, multivariate analyses included a preoperative severity scoring system (SS) [6] as a covariate in logistic regression and ANCOVA. This scoring system includes risk points based on emergent procedures, serum creatinine, severe left ventricular dysfunction, reoperation, operative mitral valve insufficiency, age, prior vascular surgery, chronic obstructive pulmonary disease, anemia, operative aortic valve stenosis, weight, diabetes, and cerebrovascular disease. This severity score can potentially range from 0 to 33, but scores of 18 or more are rare. To determine if the effect of BCT on outcome was influenced by preoperative patient severity, this interaction was included in the analysis. To illustrate trends, patients were categorized based on their preoperative severity score, in groups that included at least 500 patients (0 to 1, low risk; 2 to 3, marginal risk; 4 to 6, moderate risk; > 6, high risk) to allow estimated rates to be at most ±5% within each severity classification. In addition, any intraoperative variables that were related to BCT were included in all multivariate analyses.

To compare the preoperative (eg, age) and intraoperative (eg, CPB time) characteristics of these patients, Wilcoxon rank sum and ² tests were performed to determine which characteristics were related to the BCT classification.

Odds ratio (OR) and their 95% confidence intervals were calculated using logistic regression estimates. To reduce the influence of outliers, continuous variables such as initial ETT, initial ICU LOS, and HLOS were converted with base-10 logarithms for ANCOVA analysis.

Secondarily to these analyses, to determine if outliers solely influenced the significant results, the highest and lowest 5% of BCT were excluded from analyses. Statistical computations utilized SAS version 6.12 (SAS Institute, Cary, NC) and summary statistics are presented as mean ± SD, medians and interquartile ranges (the 25th and 75th percentiles), and medians and their 95% confidence intervals (CI) for continuous outcome measures.

	Results

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The study included a sample of 5,701 consecutive isolated CABG patients (4,537 primary surgeries [79.6%] and 1,164 redo surgeries [20.4%]) operated upon from January 1995 through December 1997 and entered into the departmental database. The average patient age was 64.3 years (± 0.1 years) and the study sample was comprised of 76.8% males. The average preoperative severity score was 2.9 (± 0.04). The overall hospital mortality rate for this population sample was 1.8% and the overall major morbidity rate (one or more individual morbidities) was 7.4%. The outcome measures for the entire sample are summarized in Table 1.

Comparisons of demographic and baseline patient characteristics indicated that BCT was related to several variables, as demonstrated in Table 2. Within the isolated CABG population, it was determined that older age, female gender, smokers, lower preoperative hematocrit, smaller body surface area, and greater preoperative severity score were the most significantly (p < 0.001) related to lower BCT. BCT is also negatively, but weakly, correlated with preoperative severity score (Spearman correlation = 0.07; p < 0.001), indicating that colder patients tend to be associated with higher preoperative severity scores. There is a significant, but relatively weak, correlation between preoperative severity and CPB time (r = 0.01, p < 0.001). Patients in N had significantly longer time (minutes) on CPB as compared with H (p < 0.001) but require significantly less OR time (minutes) to complete the surgery (p < 0.001). Overall, 20.4% (1,163) of the procedures examined were redo CABG. H was comprised of 21.2% (338) redo procedures (828), which did not differ significantly from N.

View larger version (87K): [in this window] [in a new window]   Fig 1. After adjusting for overall preoperative patient severity, bladder core temperature was significantly related to: (A) mortality; (B) PRBCs; (C) initial ICU length of stay; and (D) initial mechanical ventilation. (E) There was a significant interaction between preoperative severity score and bladder core temperature relating to hospital length of stay.

	Comment

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The results of this retrospective database analysis demonstrate that after isolated CABG surgery with CPB, patients returning to the ICU with mild hypothermia (< 36°C) are at increased risk of adverse outcomes in the postoperative period. These outcomes include prolonged ETT, ICU, LOS, and HLOS, increased need for postoperative PRBC, and increased mortality.

Hypothermia is a common occurrence of general anesthesia and surgery [4, 8], particularly so when major body cavities are open for prolonged periods of time. In addition, the use of cold intravenous fluids, the extent of operative dissection, prolonged wound closure time, exposure to a cold ambient OR temperature, and hypothermic CPB all compound the problem. It has been reported that up to 60% of patients undergoing general anesthesia and surgery, postoperatively, may have BCT of less than 36°C on admission to a PACU/ICU [1, 5].

It has been widely appreciated among neuroscientists that mild brain cooling (2°C to 5°C) is capable of conferring dramatic protection from ischemic brain injury [9]. But, it is unclear as to the cause of cerebral injury after cardiac surgery and CPB. Theoretical mechanisms of cerebral injury after CPB are currently thought to involve three factors: (1) macro or micro emboli [10], (2) perioperative hypoperfusion, or low flow [10], and (3) a systemic inflammatory response stimulated by CPB [10–12]. Although it is true that transient ischemia can cause cerebral infarction, it seems more plausible that the majority of ischemic results (ie, strokes) are caused by a macroembolic event, such as an atheromatous plaque, permanently occluding a major vessel. While hypothermia has been shown to reduce infarct size in the setting of transient middle cerebral artery occlusion, infarct size is not affected in the setting of permanent vessel occlusion [13]. The inability to demonstrate an effect of temperature on neuropsychologic outcome [13] suggests that transient ischemia does not play a major role in this injury either.

There has been a trend towards normothermic CPB over the past 5 years. Traditionally, CPB has been performed under hypothermic conditions (active cooling). In fact, debate continues over whether or not mild hypothermic CPB, moderate hypothermic CPB, or normothermic CPB results in better neurologic outcome. Interestingly, there is evidence that that hypothermia actively enhances endotoxin release from ischemic gut mucosa and that this endotoxin release may have an adverse effect on brain tissue [14].

Although mild hypothermia may decrease overall metabolic demand and oxygen consumption and increase tolerance time for tissue ischemia, it is also associated with multiple physiologic derangements including coagulopathy [15], increased incidence of wound infection [16], prolonged hospital stay [2], and a left shift of the oxyhemoglobin dissociation curve [17]. Mild hypothermia (0.5°C to 1.3°C less than normal core temperature) has been shown to increase circulating catecholamines four- to sevenfold, and increase respiration and metabolic rate up to twofold, leading to generalized systemic vasoconstriction, arrhythmias, ensuing hypertension, and decreased cardiac output [18]. In addition, shivering, which may begin at temperatures less than 1°C below BCT, is associated with large increases in total body oxygen consumption and potential cardiovascular compromise [19]. These stresses may become evident when poorly tolerated. After cardiac surgery, patients may have a diminished ability to increase oxygen delivery and cardiac output because of depressed myocardial function and decreased oxygen carrying capacity (secondary to hemodilution, surgical bleeding [1, 8], and left-shifted oxyhemoglobin dissociation curve [2]) perhaps exacerbated by hypothermia.

The possibility of postoperative shivering as a cause of adverse postoperative outcome is noteworthy. Shivering may occur in response to intraoperative hypothermia along with a resetting of thermoregulatory centers [20]. Shivering also occurs in some patients actively rewarmed and who remain normothermic during surgery, but often is absent in patients presenting distinctly hypothermic [20]. Yared and associates [21] found that dexamethasone, administered pre-CPB, reduced the incidence of postoperative shivering independent of core temperature (CT) in cardiac surgery patients, thus supporting the role of an inflammatory response in the etiology of shivering. We were not able to evaluate what percentage of CABG patients in this study demonstrated postoperative shivering. Given that 5% to 76% of postoperative cardiac surgery patients experience shivering [20–22], and that it may be secondary to either a thermoregulatory or an inflammatory response, it is impossible to say that shivering, even in mildly hypothermic patients, did not contribute to the prolonged ETT, ICU, H LOS, and mortality demonstrated in this analysis.

The two clinical subsets examined were different in that, preoperatively, patients in the H group were found by univariate analysis to be of older age, be of the female gender, be smokers, have lower baseline hematocrit, have smaller body surface area (BSA), and have higher preoperative SS. These results are in agreement work done by Baker and associates [8], who found that lower BSA and female gender were related to postoperative hypothermia after CPB. Frank and associates [4] demonstrated age correlated positively with the magnitude of intraoperative temperature drop. It may be evidence that BSA, which is seen more frequently in older age, female patients, is in fact a predictive value for postoperative hypothermia. The other factors that we found predictive, lower baseline hematocrit and history of smoking, may also be related to the previously described risk factors. It is more than a coincidence that smoking, which is related to development of chronic obstructive pulmonary disease, may be directly related to lower BSA (thinner). Additionally, lower hematocrit may be epiphenomenal with the female gender, older age, and lower BSA [8]. It is, therefore, not possible to state that these results are independent predictors of postoperative hypothermia.

It was found that intraoperatively, H patients actually had a shorter duration of CPB as compared with N patients. The time required to complete the surgery, ie, longer time from separation from CPB to ICU admission, was longer in the H group. The longer time it takes to complete the surgical procedure, the longer the patient is subject to a cold OR environment, especially in the older age patient [11], may dramatically impact the development of postoperative hypothermia.

The multiple logistic regression model developed (after adjusting for preoperative SS) did not find the univariate, pre-, and intraoperative variables to be of significance when evaluating the relationship of BCT with outcome. The use of the preoperative SS [8] as a sole covariate in the multiple logistic regression analysis was considered appropriate because all of the variables examined between the two groups were included in the development of the SS. Therefore, in a sense, all of the variables found in Table 1 are included in the SS.

One interesting result was that patients considered to be of moderate and high risk were found to have lower BCT and longer total HLOS. This indicates that the effect of H on total HLOS increased as preoperative patient SS increased. These higher risk patients may tend to be elderly and of smaller BSA. The elderly may have a decreased ability to compensate for H, and this may prolong the effect of parenterally administered drugs. H may also exacerbate the preexisting condition of these patients, thus necessitating more aggressive and prolonged hospitalization.

Our results indicate that overall, patients considered N had a significantly less risk of mortality (p = 0.02), plus a reduced requirement for postoperative PRBC (p = 0.001), prolonged ETT (p = 0.007), ICU LOS (p = 0.01), and HLOS (p = 0.005). We initially believed that this would have been more of a consequence in our higher risk patients, but we explored a range of temperatures versus patient preoperative severity score for CABG patients [8]. We found that overall, mild postoperative hypothermia was associated with adverse outcomes (in relation to mortality, PRBC, ETT, ICU LOS, and HLOS) regardless of preoperative patient acuity. The exception was that H patients of greater preoperative severity (> 4) had significantly longer HLOS.

In view of the current trend of early extubation and accelerated recovery from CABG surgery to shorten ICU and HLOS, these results are particularly pertinent. The results imply that isolated CABG patients, regardless of acuity, may benefit from normothermia as measured on ICU admission. It may, therefore, be advantageous to take steps to maintain BCT in the physiologic range after separation from CPB, especially manipulating those variables that are most easily changed.

Improved awareness and timely intervention may play a pivotal role in decreasing adverse outcome secondary to mild, inadvertent hypothermia in patients undergoing CABG. Further prospective studies will be required to validate the hypothesis formulated in this retrospective analysis.

	References

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