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Ann Thorac Surg 2001;72:1603-1609
© 2001 The Society of Thoracic Surgeons

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Original article: cardiovascular

Report of a substudy on warm versus cold cardiopulmonary bypass: changes in creatinine clearance

^a Department of Anesthesiology, Duke University Medical Center, Durham, North Carolina, USA
^b Department of Surgery, Duke University Medical Center, Durham, North Carolina, USA

Accepted for publication August 8, 2001.

* Address reprint requests to Dr Stafford-Smith, Duke University Medical Center, North Hospital, Room 3450, Erwin Road, Durham, NC 27710, USA
e-mail: staff002{at}mc.duke.edu

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. Renal dysfunction remains a major complication of cardiac operations. There is concern regarding the possibility of increased renal injury during warm cardiopulmonary bypass (CPB). Therefore, we tested the hypothesis that warm CPB is associated with a greater reduction in creatinine clearance after cardiac surgery than hypothermic CPB.

Methods. We randomly assigned 300 patients who had elective coronary artery bypass grafting to warm (35.5 to 36.5°C) or cold (28°C to 30°C) CPB. Preoperative and peak postoperative serum creatinine values were recorded. Creatinine clearance was estimated using the Cockroft Gault equation. Univariate and multivariable analyses were performed to test the association of CPB temperature and perioperative change in creatinine clearance.

Results. Demographic variables were similar between groups. Multivariable analysis did not confirm an association between temperature and change in creatinine clearance (p = 0.87).

Conclusions. We did not confirm an association between warm CPB and increased renal dysfunction after cardiac operations compared with hypothermic CPB.

	Introduction

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Renal dysfunction remains a distressingly common complication of cardiac operations. The annual cost of morbidity and mortality related to such renal dysfunction is significant [1]. Patients with increasing degrees of creatinine (Cr) elevation after cardiac operations require disproportionately more resources and are associated with steadily poorer short and long-term outcome and greater expense [2, 3]. Although factors important in the development of acute renal injury, including hypoperfusion, toxin exposure, and renal medullary oxygen imbalance, have been identified, a pathophysiologic mechanism remains unknown [4]. Pharmacologic interventions to prevent or treat acute postoperative renal insufficiency are not available [5, 6]. After cardiac operations, renal dysfunction is an important problem for which a definitive solution remains to be found.

Hypothermia during cardiopulmonary bypass (CPB) commonly is used as an organ protection strategy to reduce metabolism and ischemic stress [7, 8]. Because markers of metabolism are decreased, even with modest reductions in temperature (eg, 34°C) [9], it has been proposed that hypothermia during CPB may be protective for the kidneys [10]. The recent trend toward warm or normothermic CPB has prompted concern regarding preservation of renal function during extracorporeal perfusion [11]. Although this issue has been evaluated, studies regarding postoperative renal function using different CPB temperature management strategies have involved either very small populations [12, 13] or were designed primarily to study other outcomes [14] and have, therefore, not addressed this issue definitively. The effect of hypothermia during CPB on postoperative renal function is not known. Therefore, in a large population of patients enrolled in a prospective, randomized study of CPB temperature and neurologic outcomes [15], we tested the hypothesis that warm CPB is associated with a greater reduction in creatinine clearance (CrCl) after cardiac surgery than cold CPB.

	Material and methods

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After institutional review board approval and informed consent were obtained, 300 patients who had elective coronary artery bypass grafting (CABG) were enrolled between 1994 and 1999 in a study examining neurologic outcomes [15]. Exclusions were renal disease (preoperative serum creatinine [CrPre] more than 177 µmol/L), uncontrolled hypertension, history of cerebrovascular disease with residual deficits, alcoholism, psychiatric illness, pregnancy, less than a seventh grade education, and active liver disease. Patients were randomly assigned preoperatively to warm (35.5°C to 36.5°C) CPB perfusion with intermittent hypothermic (8°C) cardioplegia (warm group) or cold (28°C to 30°C) CPB perfusion with intermittent hypothermic (8°C) cardioplegia (cold group). Demographic data were gathered, including CrPre, history of hypertension, diabetes, chronic obstructive pulmonary disease, cerebrovascular complications, previous myocardial infarction, American Society of Anesthesiologists’ class, preoperative ejection fraction, unstable angina, and intraoperative variables, including CPB duration, intraaortic balloon pump (IABP) use, and mean arterial pressure (MAP). Postoperative variables included use of inotropic agents, transfusion requirements, new Q wave myocardial infarction, and congestive heart failure. Investigators gathering preoperative and postoperative assessments were masked to the temperature assignment of each patient. Only the physicians directly involved with intraoperative patient care were aware of group assignment.

Renal function assessment
Serum creatinine (Cr) was measured as part of routine biochemical laboratory investigations for elective CABG patients at Duke University Medical Center. The CrPre value was measured on the day before the operation in all inpatients and within 1 week before the operation in all outpatients scheduled to undergo elective CABG. Serum creatinine was then measured postoperatively within 1 hour of admission to the intensive care unit (postoperative day 0 value). From the following day (postoperative day 1) until the day of discharge, Cr was measured daily in the morning as part of routine laboratory investigations. Serum creatinine was measured using a dry slide enzymatic reflectance technique (Vitros 950, Johnson & Johnson, New Brunswick, NJ) with a normal range of 62 to 124 µmol/L. The Cr data were accessed for the study from a quality assurance database. Peak postoperative Cr (CrPost) was defined as the highest daily in-hospital postoperative value. Peak fractional change in Cr (%Cr) was defined as the difference between the CrPre and CrPost represented as a percentage of the preoperative value. Creatinine clearance (CrCl) values were derived from CrPre and CrPost values using the Cockroft Gault equation [16]. The perioperative change in CrCl (CrCl) was defined as the difference between lowest postoperative CrCl (CrClPost) and preoperative (CrClPre) (CrCl = CrClPost - CrClPre).

Anesthesia and surgery
Anesthesia was managed per the attending anesthesiologist’s preference. Use of agents with potential renal effects (eg, intravenous dopamine, furosemide, or mannitol) was not regulated. Induction and maintenance of anesthesia were achieved with a continuous infusion of fentanyl and midazolam. Supplemental isoflurane (0.5% to 1.0%) was used as required to maintain heart rate and mean blood pressure within 25% of preinduction values. Extracorporeal perfusion was performed using a Cobe CML oxygenator (Cobe Laboratories, Lakewood, CO), a Sarns 7000 Max perfusion pump (3M, Sarns Inc, Ann Arbor, MI), and a Pall SP3840 arterial line filter (Pall Medical Corp, Ann Arbor, MI). Nonpulsatile perfusion was maintained at 2 to 2.4 L/m² per minute. The pump was primed with crystalloid solution (0.9% normal saline) designed to achieve a hematocrit of 0.18 or higher during CPB. Packed red blood cells were added to ensure the desired hematocrit. The arterial carbon dioxide tension was maintained throughout CPB at 35 to 40 mm Hg (uncorrected for temperature), with the arterial oxygen tension maintained at 150 to 250 mm Hg. Mean arterial pressure was maintained between 50 and 90 mm Hg during CPB using intravenous phenylephrine or sodium nitroprusside as required.

Patients in the warm group had a perfusate inflow temperature of 36°C and were actively rewarmed to a nasopharyngeal (NP) temperature of 37°C before separation from CPB. The cold group had an inflow temperature of 28°C and was also actively rewarmed to a NP temperature of 37°C after cross-clamp removal and before discontinuation of CPB. The maximal infusate temperature during rewarming was 37.5°C by protocol. During CPB, myocardial protection was achieved in both groups with antegrade or retrograde blood cardioplegia delivered at 8°C. Myocardial temperature was maintained at 20°C or less during aortic cross-clamping. Mean arterial pressure and NP temperature were measured each minute during CPB and recorded automatically using the ARKIVE Information Management System (Arkive IMS Inc, San Diego, CA). Nasopharyngeal temperature measurements during the rewarming period were summarized as follows: peak temperature, duration (minutes) of temperature higher than 37°C, temperature-time integral (°C.minute) for the period during which the mean temperature was greater than 37°C, highest temperature recorded during the rewarming period, and maximum 5-minute rate of temperature increase during the rewarming period.

Statistical analysis
Baseline and demographic characteristics were compared using the ² test for categoric variables and the t test or Wilcoxon rank-sum test for numeric variables. Significance was assessed to a two-tailed alpha of 0.05.

To compare the association of CrCl with temperature management, multivariable linear regression analysis was used. All demographic variables were considered covariates in the multivariable model, and only significant covariates were retained in the final model. Because CrCl is not normally distributed, we performed a nonparametric analysis on ranked CrCl values to test the robustness of primary findings. A second multivariable regression analysis was also performed to compare the association of percentage Cr with temperature management.

To evaluate the influence of temperature management on high-risk patients, a subanalysis was performed including a subset of patients with CrPre of at least 115 µmol/L. Because of the small size of the patient groups, in this subanalysis we compared preoperative CrCl, peak postoperative CrCl, and CrCl between the groups using univariate tests only. All statistical analyses were performed using the SAS statistical software version 8.0 (SAS Institute Inc, Cary, NC).

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
A total of 300 patients who had elective CABG surgery were enrolled in this study. One hundred forty-nine patients were randomly assigned to the warm CPB group, and 151 patients received cold CPB. Complete creatinine data were unavailable for 2 patients, 1 in each group, and they were excluded from analysis. Both warm and cold groups had similar demographic characteristics, including preoperative CrCl and incidence of Cr of at least 115 µmol/L (Tables 1 and 2). However, patients in the cold CPB group received significantly more perioperative blood transfusions (6.3 U versus 0.7 U; p = 0.01). Demographic variables were also comparable to those reported in other similar populations [3]. As per the study protocol, patients in the cold group had a lower mean NP temperature during CPB than patients in the warm group (30.4°C versus 35.1°C; p < 0.01) (Table 3). However, despite identical protocol-driven rewarming strategies, there were differences in postrewarming NP temperatures between the groups. Specifically, during the late phase of CPB rewarming, patients in the cold group had a higher mean peak temperature (37.6°C ± 0.5°C versus 37.0°C ± 0.7°C; p < 0.001), longer mean duration of temperature above 37°C (28.2 ± 23.4 minutes versus 15.5 ± 23.8 minutes; p < 0.001), and a higher mean temperature-time integral more than 37°C (11.4°C ± 12.2°C versus 5.5°C ± 11.7°C-min; p < 0.001) than patients in the warm group (Table 3).

A power analysis showed that, given this sample size and standard deviation, the study population provided 80% power to detect a CrCl of 6.73 mL/minute. Multivariable regression analysis identified age, weight, preoperative CrCl, and postoperative need for an inotropic agent as variables independently associated with CrCl (Table 4). Similar results were seen in the multivariable analysis of factors associated with percentage Cr (Table 5). Notably, multivariable analysis did not confirm NP temperature during CPB as being independently associated with CrCl (p = 0.87). A multivariable regression analysis of ranked data (Table 6) demonstrated results similar to those in Table 4.

In a subgroup of 100 patients in the cold group, univariate and multivariable linear regression analyses were performed to examine the association of (1) the highest temperature recorded during the rewarming period (MaxTemp) and (2) the maximum 5-minute rate of temperature increase during the rewarm period (RateMax5) with percentage CrCl. Neither of those variables was significantly associated in either analysis (univariate analysis shown in Table 7).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

Other studies investigated the influence of CPB temperature on postoperative renal function [12–14]. Regragui and colleagues [13] studied 30 CABG patients and found no difference in perioperative CrCl changes among three groups randomly assigned to different CPB temperature management strategies (target NP temperature 28, 32, and 37°C). A randomized study by Ip-Yam and colleagues [12] in 24 CABG patients found no effect of bypass temperature (28°C versus 37°C) on postoperative CrCl, fractional excretion of sodium, urinary N-acetyl-ß-D-glucosaminidase, and microalbuminuria, except for an increased cold-induced diuresis with hypothermic CPB. Although those studies [12, 13] were randomized, the small group sizes limit the significance of a negative finding. In a large study evaluating stroke, Singh and associates [14] compared prospectively gathered data from 2,585 normothermic CPB patients with a retrospective hypothermic CPB cohort of 1,605 cases; renal and other demographic variables were assessed as secondary outcomes. They found no significant difference in postoperative renal function between the groups. Renal insufficiency in that study was defined as a creatinine increase of more than 88 µmol/L or oliguria less than 30 mL/m² per hour during the postoperative period. However, in the study by Singh and associates [14], renal dysfunction was a secondary outcome, and there were significant differences in the incidence of important renal risk factors between the study groups, including age, preoperative ejection fraction, and incidence of diabetes. In contrast to previous work, our study included a large number of patients and a randomized prospective study design conferring significant ability to identify even small differences between groups related to bypass temperature management. A power analysis of our study found that, based on the whole group sample size and standard deviation, this study had 80% power to detect a difference in CrCl of 6.73 mL/minute (ie, a 7.4% change as a proportion of preoperative CrCl). Our findings are consistent with other reports; however, this study confirmed that bypass temperature management does not appear to play a major role in perioperative renal protection, given the potential limitations of previous studies. The results of our subanalysis in patients with CrPre of at least 115 µmol/L suggest that this conclusion might also be warranted in this high-risk group.

Our study has limitations related to measurement of renal function and CPB management. Although this study suggests that hypothermic CPB is not associated with greater renal protection compared with warm CPB, other prospective studies using a variety of tests of renal function to address this issue are required. Although this study was not prospective, because it tests a hypothesis that was developed after the study was initiated, study patients were randomly assigned and data for all variables, including Cr, were gathered prospectively. This study was not double-blinded, as the anesthesiologists and surgeons involved with the patients were aware of the temperature management. In this type of study, it would not be possible to double-blind the intraoperative personnel to temperature management. A second concern is that our study investigated only one aspect of renal function, ie, filtration, and not other homeostatic roles of the kidney, including osmolality, electrolyte and acid-base regulation, and production and release of several enzymes and hormones. In addition, it can be speculated that there are more sensitive markers of renal injury than Cr, eg, urinary N-acetyl ß-D-glucosaminidase. However, our group has shown that the renal marker we selected for study, CrCl, is a sensitive marker that correlates well with postcardiac surgery morbidity and mortality [17]. Moreover, the association of markers of subtle renal injury, such as urinary N-acetyl ß-D-glucosaminidase, with adverse postoperative outcome has not been established, and a recent study [18] suggested that those markers might not predict postoperative renal injury accurately. It is possible that higher NP temperatures might have masked a potential hypothermic benefit during CPB rewarming in the cold group. Most important in understanding the significance of the findings of this study is that the standard CPB rewarming protocol used in this study resulted in a temperature overshoot in patients who had cold relative to warm CPB. Identical rewarming management in both groups, (ie, warming to an NP temperature of 37°C before separation from CPB) resulted in a temperature overshoot in the cold group. The evidence we present is clinically relevant despite the limitations of the different rewarming patterns between the two groups. We suggest that the overshoot of temperature is inherent in any standard hypothermic temperature management protocol that does not control for the original CPB target temperature. Although patients with preexisting renal dysfunction (CrPre > 177 µmol/L) were excluded from the primary neurologic outcomes study, we chose for our secondary analysis, a subgroup of patients at higher risk for perioperative renal injury because of elevated CrPre (> 115 µmol/L) [17]. Given our small sample size (n = 41) of high-risk patients, we had 33% power to detect a 20% difference in CrCl between the groups. Our conclusions in this group can, therefore, only be considered suggestive. Despite the limitations listed above, we believe that our study strengthens evidence from previous studies suggesting that warm CPB compared with cold CPB does not pose a major risk of acute renal injury during cardiac operation.

These findings contradict traditional views on hypothermia and organ protection and merit further evaluation. Possible explanations for the absence of a renal protective effect from hypothermia during CPB could relate to a counterbalancing of any benefit from a reduction in metabolic rate by an increase in renal blood flow, with resulting greater solute delivery, requiring increased renal tubular transport and possibly even delivery of more potentially injurious emboli. That effect has been demonstrated in an animal model. In a study of 6 dogs, Deal and colleagues [19] found increased renal blood flow and embolic count during hypothermic versus normothermic CPB. They suggested that that effect would place the dogs at higher risk of renal dysfunction. We recently demonstrated that transcranial Doppler–detected embolic count during CPB is directly associated with postoperative creatinine increase [20]. Although these studies suggest a possible mechanism for our findings, further evaluation is warranted in this area by investigating the full spectrum of renal function over a range of CPB temperatures.

In summary, in a large population of primary elective CABG patients, we could not confirm that warm CPB is associated with greater postoperative decrease in creatinine clearance after cardiac operations compared with hypothermic CPB. Although this finding was similar in a subset of high-risk patients (CrPre > 115 µmol/L), the same conclusion cannot be made confidently in all patients with preexisting renal dysfunction, as we excluded patients with a CrPre higher than 177 µmol/L. Although the magnitude of CrCl reduction below which changes become clinically significant has not yet been established, the power of this study indicates that a major finding has not been missed. This study suggests that commonly used warm (36°C) CPB perfusion does not pose a greater risk of renal injury compared with traditional moderate hypothermic perfusion during CPB in primary elective CABG patients. However, this conclusion is based on only one aspect of renal function and deserves further investigation using a variety of tests of renal function over a wide range of CPB temperatures.

	Acknowledgments

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This work was supported in part by National Institutes of Health grants R01-AG09663-4 (MFN), GM08600-02 (JGR), and MO1-RR-30 (National Center for Research Resources, Clinical Research Centers Program, National Institutes of Health) and the Division of Cardiothoracic Anesthesia and Critical Care Medicine of the Department of Anesthesiology, Duke University Medical Center (DUMC), Durham, NC. The authors gratefully acknowledge the assistance of Alina M Grigore, MD, Cardiothoracic Anesthesia Fellow (1998–2000), and David Kaemmer, CCP, Senior Clinical Perfusionist, and the secretarial efficiency of Ms LaTanya Rhames, Department of Anesthesiology, DUMC, in the preparation of this manuscript.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mark F. Newman Peter K. Smith Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Swaminathan, M. Articles by Stafford-Smith, M. Search for Related Content PubMed PubMed Citation Articles by Swaminathan, M. Articles by Stafford-Smith, M. Related Collections Extracorporeal circulation