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Ann Thorac Surg 1995;59:1429-1433
© 1995 The Society of Thoracic Surgeons

Neurologic Events After Coronary Bypass Grafting: Further Observations With Warm Cardioplegia

Division of Cardiothoracic Surgery, Joseph B. Whitehead Department of Surgery, Emory University School of Medicine, Atlanta, Georgia

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Warm heart surgery has documented myocardial protection benefit, but with an added neurologic threat. It is hypothesized that moderately hypothermic aerobic heart surgery will maintain the myocardial protection and reduce neurologic risk. This study compared 493 patients undergoing coronary artery bypass graft operations with normothermic (35° to 37°C) continuous blood cardioplegia and normothermic perfusion to 379 coronary artery bypass grafting patients with hypothermic (33° to 29°C) continuous blood cardioplegia and hypothermic perfusion to test this hypothesis. There was no difference in age, sex, prior myocardial infarction, hypertension, prior neurologic event, congestive failure, or diabetes. The hypothermic group had more reoperations (24% versus 14%; p = 0.0002), class III/IV angina (83% versus 71%; p = 0.002), a trend to more triple-vessel (54% versus 47%; p = 0.10) and left main disease (18% versus 14%; p = 0.10), lower ejection fractions (0.52 ± 0.15 versus 0.55 ± 0.13), more grafts placed (3.6 ± 1.1 versus 3.4 ± 1.1; p = 0.04), but fewer internal mammary arteries (62% versus 78%; p < 0.0001). Postoperative myocardial infarction rate was 1.2% in the hypothermic group and 1.3% in the normothermic group (p = not significant). Intraaortic balloon pump requirement was 3.4% with hypothermic and 1.4% with normothermic groups (p = 0.05). The incidence of postoperative neurologic events was significantly higher in the normothermic group (4.7% versus 1.8%; p = 0.038). The multivariate correlates of stroke were older age and normothermic cardioplegia, whereas the only multivariate correlate of death was older age. In summary, these data suggest that hypothermic continuous blood cardioplegia provides myocardial protection that is equivalent to normothermic continuous blood cardioplegia, whereas hypothermic aerobic heart surgery may lessen the neurologic risk that was observed associated with strict warm heart surgery.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 1433.

Efforts to reduce neurologic complications of cardiac operations are a priority to maintain patients' quality of life, to eliminate lost patient productivity, and to reduce the overall cost of cardiac surgical care and hospitalization. Normothermic continuous blood cardioplegia combined with normothermic cardiopulmonary bypass (CPB) was identified as a neurologic threat in a randomized prospective study at this institution comparing the technique with cold oxygenated crystalloid cardioplegia [1]. Hypothermic CPB may have provided protection from cerebral ischemia in the oxygenated crystalloid cardioplegia group in that study. This observation provoked reconsideration of normothermic continuous blood cardioplegia and perfusion techniques and the importance of normothermia for the myocardial protection benefit.

A controlled laboratory investigation documented maintenance and possible improvement in myocardial protection by combining hypothermia with continuous blood cardioplegia as compared with normothermia [2]. Based on the above theoretical, experimental, and clinical findings, we applied continuous blood cardioplegia with CPB conducted at moderate hypothermia to reap the myocardial protection benefit and reduce the neurologic risk observed with the normothermic method.

In this report, the clinical results of hypothermic and normothermic continuous blood cardioplegia and perfusion are compared. Myocardial protection as measured by the clinical end points of perioperative myocardial infarction, intraaortic balloon pump requirement, and mortality are examined. Neurologic complications determined by fixed neurologic deficit and postoperative delirium/encephalopathy are likewise compared between the two groups.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Operative Procedure
From August 1992 to April 1994, 379 consecutive patients underwent coronary artery bypass grafting with CPB conducted at moderate hypothermia (33° to 29°C) and myocardial protection provided by continuous blood cardioplegia delivered at similar temperature. Demographic and perioperative clinical data were reviewed in this group of patients. The hypothermic group was compared with a cohort of 493 patients who underwent coronary artery bypass grafting with CPB conducted at normothermia (37° to 35°C) and myocardial protection provided by normothermic continuous blood cardioplegia. This normothermic group was a cohort of the prospective, randomized study conducted between March 1990 and July 1992 [1].

Coronary artery bypass operations were conducted similarly in both groups of patients excepting cardioplegia regimens and systemic temperature management.

Cardioplegia solution composition was as follows:

• Hypothermic
  • 4:1 blood:cardioplegia
    • 1,000 mL Plasmalyte
      
    • 20 mEq NaHCO₃
      
    • 1.5 g dextrose
      
    
    
  • High K = 100 mEq KCl/L
    
  • Low K = 30 mEq KCl/L
    
  
  
• Normothermic
  • 4:1 Blood:cardioplegia
    • 1,000 mL 5% dextrose
      
    • 18 mEq MgSO₄
      
    • 12 mEq THAM
      
    • 20 mL CPD
      
    
    
  • High K = 100 mEq KCl/L
    
  • Low K = 30 mEq KCl/L
    
  
  

Cardioplegia was delivered by a 4:1 blood:cardioplegia delivery system with core and cardioplegia temperature maintained at 35°C in the normothermic group and 33° to 29°C in the hypothermic group. In both groups, high-potassium blood cardioplegia (final concentration, 20 mEq/L) was infused into the root of the aorta immediately on cross-clamping the aorta at 350 mL/min and a pressure of 100 to 300 mm Hg until diastolic arrest was achieved. Electromechanical arrest was maintained by low-potassium (4 mEq/L) cardioplegia delivered continuously into the coronary sinus through a retrograde coronary sinus catheter (Gundry retroplegia cannula; DLP, Inc, Grand Rapids, MI). Coronary sinus pressure was kept near 40 mm Hg and flow rates ranged from 40 to 250 mL/min.

In both groups, there were some patients in whom the cardioplegia delivery was stopped for short periods (2 to 5 minutes) to facilitate visualization for construction of the distal coronary anastomoses. All distal anastomoses were performed first. In the hypothermic group, a terminal dose (100 mL) of 37°C high-potassium cardioplegia was administered just before cross-clamp removal to provide the initial warm reperfusion in a state of electromechanical arrest. In both groups, the majority of proximal anastomoses were performed under partial aortic occlusion.

Systemic temperature management during CPB was different in the two groups. Systemic temperature was regulated by a water bath heater/cooler (Hematherm; Cincinnati Sub Zero, Cincinnati, OH). In the hypothermic group, core temperatures were reduced (33° to 29°C) before aortic cross-clamping and rewarming occurred during the terminal 15 minutes of the cross-clamp interval. In the normothermic group, core temperatures were maintained in the range of normothermia (35° to 37°C) throughout the CPB run.

Cardiopulmonary bypass materials and methods were the same in both groups: roller pumps (Cinco heart-lung machines, Wakefield, MA), membrane oxygenators (COBE Excel, adult membrane lung; COBE Cardiovascular, Arvada, CA), and single aortic and atrial cannulation techniques. Pump flows were maintained at 2.2 to 2.5 L/m² during normothermic perfusion. At temperatures less than 32°C, flow rates were decreased to as low as 1.8 L/m² if in-line venous saturation was greater than 90%. Perfusion pressure was maintained at 50 to 70 mm Hg at temperatures greater than 32°C and 40 to 60 mm Hg less than 32°C. Initial heparinization was accomplished with 4.0 mg/kg and was supplemented as needed to maintain an activated clotting time greater than 300 seconds.

Anesthesia was accomplished by high doses of fentanyl citrate supplemented with midazolam hydrochloride, and all patients were paralyzed using vecuronium bromide. Vasoactive and inotropic agents delivered in the operating room were used to maintain acceptable hemodynamic parameters as determined by the operating surgeon and cardiac anesthesiologist.

Statistical Methods and Data Collection
The database was compiled and analyzed within the Emory Cardiovascular Data Center and consisted of information obtained from patient chart review performed at the end of each individual's hospitalization. All statistical testing was done with BMDP software. Results are reported as the mean ± the standard deviation or proportions. Continuous measures were compared by unpaired t tests and categoric measures, by ² statistical analyses. Multivariate analysis was performed by step- wise logistic regression.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
There were no significant differences in the clinical descriptors of sex, prior myocardial infarction, hypertension, diabetes mellitus, prior neurologic event, or preoperative Canadian class of heart failure between the two groups (Table 1). The hypothermic group was older, had more severe preoperative angina and worse ejection fraction, and included more reoperations. A trend toward more triple-vessel disease and left main disease also was observed in the hypothermic group.

Multivariate determinants of stroke were older age and normothermic cardioplegia (odds ratio, 1.10; 95% confidence interval, 1.05 to 1.15 per year of age, p < 0.0001; and odds ratio, 1.76, 95% confidence limits, 1.14 to 2.71 for normothermic group, p = 0.0073). Older age was the only multivariate correlate of death (odds ratio, 1.16; p < 0.007). When additional clinical variables of diabetes, angina, hypertension, and sex were forced into the multivariate model, the warm cardioplegia group remained a multivariate correlate of stroke with an odds ratio of 1.65 (95% confidence interval, 1.03 to 2.66).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Proponents of normothermic continuous blood cardioplegia provide rational arguments for its benefit combined with normothermic perfusion and have coined the term ``warm heart surgery'' as a description of the technique [3]. The cornerstone argument for normothermic continuous blood cardioplegia focuses on the detrimental effects of hypothermia on enzyme systems and biochemical reactions in the myocardium and the importance of normothermic aerobic electromechanical arrest for optimal myocardial protection. Additionally, normothermic perfusion is touted to reduce disturbance in the coagulation cascade while avoiding the vasoactive events associated with temperature changes, providing an improved perioperative course [4].

Laboratory investigation has confirmed improved protection by normothermic continuous blood cardioplegia when compared with other hypothermic ischemic regimens [5, 6]. The prospective, randomized Emory Warm Blood Cardioplegia Trial, which was designed to define the clinical myocardial benefits of warm heart surgery, documented effective myocardial protection but uncovered increased neurologic risk with the technique [1]. In elective coronary artery bypass grafting operations, warm heart surgery provided equivalent myocardial protection as determined by postoperative mortality, Q-wave infarct, and intraaortic balloon pump requirement, but displayed a threefold increase in neurologic events when compared with those patients undergoing hypothermic CPB with oxygenated crystalloid cardioplegia for myocardial protection.

Progress in myocardial protection must provide better ventricular function preservation at no expense to the remainder of the biologic system. Hypothermic continuous blood cardioplegia with hypothermic perfusion may avoid these neurologic hazards of normothermia. This study was conducted to compare hypothermic continuous blood cardioplegia and hypothermic perfusion with normothermic continuous blood cardioplegia and normothermic perfusion to establish the benefit of hypothermic aerobic heart surgery. The study examined the two techniques for elective coronary artery bypass grafting operations with antegrade induction and then continuous retrograde cardioplegia for improved distribution of cardioplegia in the setting of proximal coronary occlusion.

The two groups displayed similarity in preoperative variables except that there were significantly more older patients, poorer ejection fractions, worse angina, and more reoperations in the hypothermic group. Even though the two study groups were nonrandomized and not concurrently treated, the techniques employed in each group were identical with regard to operation, perfusion, anesthesia, and preoperative and postoperative care. The current cold group study was initiated immediately as soon as the Emory Warm Blood Cardioplegia Trial had been completed [1]. The temperature of CPB and of the cardioplegia infusion was the only major variable that was changed for the cold group. The comparison of the data of the two groups we believe is valid. If any bias exists it would be in favor of the warm group as the patient descriptors suggest that the cold group had a higher incidence of factors increasing surgical risks.

A change in cardioplegic solution did occur between the normothermic and the hypothermic groups. This was done because of the suggestion that an elevated blood glucose level may lead to an increased susceptibility to injury during transient cerebral ischemia [7]. The normothermic cardioplegia had been based on 5% dextrose whereas the cardioplegia for the hypothermic group was based on Plasmalyte. This led to a lower glucose level in the cardioplegia infusion and consequently lower systemic levels of glucose while on bypass in the hypothermic patients. This was also the case in our previous randomized trials of normothermic versus hypothermic cardioplegia techniques. Systemic glucose levels were monitored in our previous randomized trials, and multivariate analysis revealed that systemic glucose levels were not a multivariate predictor for stroke in this large series [1, 8]. It also should be noted that in the Toronto trial of warm versus cold antegrade continuous blood cardioplegia, 5% dextrose was used as the base cardioplegia solution. This trial (which in fact was performed at very mild hypothermia, not normothermia) had stroke levels that were equivalent to those of the hypothermic groups in the Emory series, despite the use of higher levels of glucose [9]. Systemic glucose levels were not systematically monitored and recorded in the hypothermic group in the current study.

Operative data revealed a slightly higher number of grafts in the hypothermic group reflecting the prevalence of more triple-vessel disease. Fewer internal mammary arteries were used for bypass conduits in the hypothermic cohort, which, although it may have long-term implications, did not affect the immediate postoperative course of these patients. The duration of aortic cross-clamping and CPB were similar between the groups.

Myocardial protection as assessed by Q-wave infarct was similar between the groups; however, a trend to slightly higher mortality in the hypothermic group was observed. An increased incidence of clinical descriptors suggesting more severe disease and increased risk (poorer ejection fraction, worse angina, older age, and higher number of reoperations) were present in the hypothermic group and likely played a role in the slightly increased mortality and more frequent use of intraaortic balloon pumping. Statistical comparison did not reveal a significant difference in mortality among the two groups, and the only multivariate correlate of mortality was older age.

In general, differences between myocardial protection regimens are better detected in the setting of metabolically compromised myocardium, when maximal protection of the myocardium is required to ensure adequate postoperative ventricular function [10]. In laboratory investigation of acute myocardial ischemia, hypothermic continuous blood cardioplegia delivery has demonstrated equivalent to improved protection of overall ventricular function when compared with normothermia [2]. Continuous delivery to provide aerobic electromechanical arrest and avoidance of ischemic intervals appears to be the element responsible for observed benefit of aerobic myocardial protection with temperature exerting only mild significance.

The effectiveness of hypothermic continuous aerobic blood cardioplegia for myocardial protection was demonstrated in this investigation because results similar to those of the normothermia group were achieved in higher risk patients. Also, hypothermia may provide a second tier of protection when cardioplegia must be interrupted to improve visibility for construction of distal anastomoses. Hypothermia allows such ischemic intervals to occur under more favorable metabolic circumstances.

Postoperative neurologic complications remain an important concern for cardiac surgeons. A reduced incidence of neurologic injury was identified in the hypothermic group in this study in comparison to a similar population in the Emory Warm Blood Cardioplegia Trial [1]. Multivariate analysis demonstrated an odds ratio of 1.76 for neurologic events in the normothermic group and also identified old age as a correlate for stroke. In addition, the warm heart surgery and warm cardioplegia were found to be independent of other correlates of stroke previously reported from this institution [11]. The majority of neurologic events presented as focal deficit on neurologic examination, suggesting an embolic nature of perioperative cerebral embarrassment. Including the observed difference in incidence of neurologic complications, a difference in the impact of these events on survival was observed with 1 in 3 of the normothermic stroke victims dying in the postoperative period.

Neurologic injury related to CPB is often thought to be due to embolization into the cerebral vasculature during the operation. Embolic events that can occur during CPB can arrive from microscopic debris contained in the CPB circuit, atheroemboli from native atherosclerotic aorta, intracardiac thrombi, and air within the CPB circuit. All these and others can be etiologic agents of embolic cerebral injury during CPB. Cardiopulmonary bypass at normothermia produces substantially higher cerebral blood flow when compared with extracorporeal circulation at moderate hypothermia [12, 13]. Such a circumstance could produce increased exposure to a larger number of embolic events over a given time in the normothermic group, thereby increasing the probability of neurologic injury. Intracerebral vascular occlusive disease and perfusion pressure variations while on CPB also can produce areas of focal intracerebral ischemic injury.

Hypothermia has long been established as a neuroprotective agent [14]. Cerebral ischemic injury is attenuated even with mild degrees of hypothermia as measured clinically, morphologically, and biochemically [15, 16]. The neurologic risk of CPB and the neuroprotection of hypothermia provide a framework for understanding different neurologic outcomes after normothermic perfusion. The neurologic hazards of normothermic CPB initially were unappreciated in the earlier reports on application of warm heart surgery [3].

It is likely that several factors are responsible for the poorer cerebral tolerance of CPB at normothermia. Cerebral ischemic injuries produced at normothermia display larger zones of infarction, more severe cellular acidosis, and higher concentrations of neuronal injury markers when compared with equivalent injuries produced at hypothermia [15–17]. These investigations have demonstrated that cerebral ischemic events, whether embolic or occlusive, produce less cerebral injury when the brain temperature is lowered at the time the ischemic insult is incurred [15]. This observation is particularly true if the current ischemia is transient in nature [18]. This likely explains the clinical improvement to normalcy often observed after some early ``strokes'' when air embolization or hypoperfusion is suspected as the cause rather than in strokes due to larger particulate or thrombus embolization. It is likely that less well tolerated cerebral ischemia at normothermia and possibly an increased cerebral perfusion/emboli burden combined are responsible for the difference in neurologic complications observed with warm heart surgery.

In conclusion, this study suggests that reducing the systemic perfusion temperature while on CPB may lessen the neurologic risk that has been observed with strict warm heart surgery. It also suggests that continuous hypothermic blood cardioplegia can provide myocardial protection that is equivalent to that observed with continuous normothermic blood cardioplegia. The clinical recommendation of this report is that as a patient's risk of perioperative stroke is increased, especially in the elderly, the systemic temperature of CPB should be lowered appropriately, which could reduce the incidence of perioperative stroke.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Forty-first Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 10–12, 1994.

Address reprint requests to Dr Craver, The Emory Clinic, 1365 Clifton Rd, Atlanta, GA 30322.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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