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Ann Thorac Surg 2000;70:1301-1307
© 2000 The Society of Thoracic Surgeons

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Original articles: cardiovascular

Effect of induction and reperfusion with warm substrate-enriched cardioplegia on ventricular function

^a Departments of Surgery and Anesthesia, University of California, San Francisco, San Francisco Veterans Affairs Medical Center, San Francisco, California, USA
^b Departments of Cardiovascular Surgery and Cardiovascular Anesthesia, Kaiser Permanente Medical Center, San Francisco, California, USA

Address reprint requests to Dr Wallace, Anesthesiology Service (129), Veterans Affairs Medical Center, 4150 Clement St, San Francisco, CA 94121
e-mail: awallace{at}cardiacengineering.com

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Background. This study tested the hypothesis that induction and reperfusion with warm substrate-enriched (IRWSE) blood cardioplegia improves postoperative left ventricular (LV) function in patients undergoing elective coronary bypass surgery (CABG).

Methods. After giving informed consent, 67 patients scheduled for CABG surgery were randomized to either IRWSE + cold blood (CB) or CB alone. IRWSE cardioplegia consisted of 37°C substrate-enriched (glutamate, aspartate, hyperkalemic) anterograde and retrograde blood cardioplegic solution followed by non-substrate-enriched cardioplegic solution given at 4°C to 8°C. LV function was measured with ventriculograms, volume conductance catheters, echocardiography, and multiple gated (image) acquisition.

Results. The end-systolic pressure-volume relationship was improved postbypass in the IRWSE + CB group (CB, 1.5 ± 0.74 mm Hg/mL vs IRWSE + CB, 2.1 ± 1.2 mm Hg/mL; p = 0.042). The postoperative ejection fraction (EF%) was better preserved in the CB group (CB, 65 ± 11.53% vs IRWSE + CB, 58.62 ± 11.75%; p < 0.04).

Conclusions. Our results demonstrate a transient improvement in LV systolic function in the immediate postbypass period in CABG patients in the IRWSE + CB group. The intraoperative benefits of the IRWSE + CB technique did not persist in the postoperative period.

	Introduction

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Induction and reperfusion with warm substrate-enriched blood cardioplegia (IRWSE) is used to provide optimal myocardial protection in high-risk patients with either poor ventricular function or preoperative unstable angina and ischemia [1, 2]. However, the use of these techniques has been generalized and induction and reperfusion with substrate-enriched cardioplegic solutions is used routinely by many cardiac surgeons [3].

The effect of warm induction and reperfusion and the addition of metabolic substrates remains unclear. Rosenkranz and associates demonstrated in dogs [4] that induction with warm cardioplegic solution resulted in greater myocardial oxygen consumption than cold induction in energy depleted hearts. It has been shown to improve the rate of spontaneous defibrillation [5] and enrich metabolic recovery [2]. In unrandomized trials, IRWSE has been used successfully in patients during acute myocardial infarctions [1, 6]. However, findings in humans to date have demonstrated few clinically significant differences in the effects of induction and reperfusion with warm substrate-enriched versus cold cardioplegic regimens.

We tested the hypothesis that IRWSE improves postoperative left ventricular (LV) function in patients undergoing elective coronary artery bypass grafting (CABG) surgery. IRWSE plus standard cold blood cardioplegia (CB) was compared with CB alone in a prospective, randomized clinical trial with blinded analysis.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Study population
The study was approved by the medical ethics committee (June 19, 1992), and informed consent was obtained from 67 patients scheduled for CABG surgery. All patients were operated on by one of three surgeons (W.M., T.M., K.F.) at Kaiser Permanente Medical Center in San Francisco, and all operations were monitored by one anesthesiologist (A.W.) who checked protocol adherence and collected cardiac function data. Exclusion criteria included: (a) left bundle branch block limiting electrocardiogram (ECG) analysis; (b) end-stage renal failure requiring dialysis; or (c) those scheduled for repeat operations or valvular surgery. Patients with poor ventricular function, as demonstrated by depressed ejection fraction or history of congestive heart failure, were actively recruited.

Anesthetic management
Patients received premedication (midazolam (up to 0.1 mg/kg IM) and morphine sulfate (up to 0.2 mg/kg IM), and cardiovascular medications were continued on routine schedule. Anesthesia was induced and maintained with midazolam (up to 0.4 mg/kg IV), sufentanil (up to 20 µg/kg IV), vecuronium, and oxygen (FiO₂ = 1.0). Prebypass, blood pressure, and heart rate were controlled between ± 20% of the average of three preoperative blood pressure measurements.

Cardiopulmonary bypass was performed using a membrane oxygenator, centrifugal pump, and moderate hemodilution, with a calculated flow rate of 1.8 to 2.4 L/min/m². Blood pressure during bypass was maintained between 40 and 80 mm Hg; elevations in blood pressure not responsive to the anesthetic protocol were treated with nitroprusside and decreases in blood pressure (despite adequate pump flow) were treated with phenylephrine. Distal anastomoses were performed during cardioplegic arrest. Proximal anastomoses were performed while rewarming with a partial occlusion clamp on the aorta.

If possible, patients were weaned from bypass without inotropic or vasopressor support to allow pre- to postbypass comparisons of ventricular function without the compounding variable of inotropic support. Postbypass, a cardiac index below 1.6 L/min/m² despite pulmonary capillary wedge pressure (PCWP) greater than 20 mm Hg was treated with dobutamine 5 µg/kg/min. If this dose of dobutamine was inadequate, additional inotropic support was chosen at the discretion of the clinician.

Cardioplegia protocols
IRWSE + CB group
Normothermic cardiopulmonary bypass was begun. In patients randomized to the IRWSE + CB group, the aortic cross-clamp was placed and cardioplegic arrest was obtained by infusing warm (37°C) glutamate- (13 mmol/L) and aspartate- (13 mmol/L) enriched, hyperkalemic (25 mEq/L) blood cardioplegic solution administered sequentially via the aortic root, then via the coronary sinus catheter. Initial antegrade infusion rate was 300 mL per minute for 2 minutes (600 mL), followed by retrograde infusion of 400 mL at a flow rate adjusted to maintain coronary sinus perfusion pressure at 40 mm Hg. Immediately after the warm induction, systemic cooling to 28°C was begun. Non-substrate-enriched (K⁺ 10 mEq/L) cardioplegic solution at 4°C to 8°C was then substituted and infused at 250 mL per minute antegrade for an additional 3 minutes (750 mL). Cold multidose cardioplegia was reinfused every 20 minutes or on completion of each distal anastamosis by perfusing down the graft (50 mL per graft), as well as antegrade (200 mL) and retrograde (200 mL). Systemic rewarming was initiated on completion of the second to last distal anastomosis. Before release of the aortic cross-clamp, warm substrate-enriched cardioplegic solution was infused antegrade via the aorta and down the grafts for 2 minutes at a flow rate of 150 mL per minute (300 mL), followed by retrograde delivery of 200 mL at a flow rate adjusted to maintain coronary sinus pressure at less than 40 mm Hg. An additional 400 mL of warm noncardioplegic blood was perfused retrograde before release of the aortic cross-clamp. Table 1 provides a comparison of complete cardioplegia contents for the IRWSE + CB and CB groups.

Randomization
A single random sequence was generated by computer before the study. The surgeon was notified of the cardioplegic technique assignment just before going on bypass. Analysis personnel were blinded to cardioplegic group assignment.

12-lead ECG
A 12-lead ECG tracing was recorded preoperatively, immediately postoperatively in the intensive care unit, and daily on postoperative days 1 and 2. Minnesota codes I1 or I2 were used to identify new Q waves [7].

Holter monitoring
Patients were monitored using a three-channel AM Holter ECG recorder (Series 8500 with Marquette Laser Holter Analysis System SXP software version 5.8; Marquette Electronics, Milwaukee, WI) preoperatively, intraoperatively, and for 2 days postoperatively [8–10].

Transesophageal echocardiography
A 5-MHz phased-array transesophageal transducer (Omniplane; Hewlett Packard, Palo Alto, CA) was positioned at the mid-papillary short-axis view of the left ventricle. Echocardiographic ejection fraction (EF) was measured prebypass and postbypass using a NOVA Microsonics Image Vue System (Carmel, IN).

Laboratory analysis
Arterial and coronary sinus blood samples were obtained before bypass, just after weaning from bypass, and at 15 minutes after weaning. Samples for determination of creatine phosphokinase MB isoenzyme (CPK-MB) were drawn before bypass, immediately after weaning from bypass, then every 8 hours for 3 days. Blood samples were analyzed by the clinical laboratory at Kaiser Permanente Medical Center. Myocardial infarction required a CPK-MB isoenzyme concentration greater than or equal to threshold (100 units/L) [9], new Q waves (Minnesota code I1 or I2), or autopsy evidence of acute infarction.

Volume conductance catheter
A 7-F, open-lumen, pigtail, 12-pole multielectrode catheter (LVCA) (7212-12; Webster Laboratories, Baldwin Park, CA) and a columinal 2-F (Mikro-Tip SPC-320; Millar Instruments, Houston, TX) catheter transducer was placed through a Touhy-Borst Adapter (USCI 004813; Bard, Covington, GA) into the right superior pulmonary vein and advanced into the left ventricle. A Leycom (Rijnsburg, The Netherlands) Sigma-5-DF Volume Conductance Signal Generator using dual-field mode with symmetric 10-mm interelectrode spacing calculated the conductance signal. Blood conductance was measured using 5 mL of blood in a four-electrode cuvette before assessment of volume measurements. Stroke volume (SV) from thermodilution cardiac output was compared to SV from the volume conductance catheter and used to define alpha (). All volume conductance-derived measurements were corrected using [11, 12].

Systemic arterial pressure (radial arterial catheter FA-04020; Arrow, Reading, PA) and pulmonary arterial pressure (93A-131H-7F; Baxter Edwards Swan Gantz, Deerfield, IL) were measured with pressure transducers (33-600F; Baxter) amplified by a Hewlett Packard Merlin System (Hewlett Packard, Palo Alto, CA). All pressure transducers were calibrated with a mercury manometer and zeroed to the level of the right atrium. Data were collected at 200 Hz, with 10-µs interchannel delay for slew minimization, using National Instruments (Austin, TX) NB-MIO-16H A/D board and LabView (Austin, TX) software on a MacIntosh (Cupertino, CA) Quadra 950 computer.

Definitions of measures of contractility
End-systole was defined as the point of maximal elastance, and end-diastole as the point of maximum ventricular volume [13]. The slope of the end-systolic pressure-volume relationship (ESPVR) was defined as E_ES. The end-diastolic pressure-volume relationship (EDPVR) was assumed to be a straight line with slope defined as E_ED [11, 12]. Measurements of E_ES and E_ED were obtained by tightening ligatures around the superior and inferior vena cava to retard flow to the heart. Two measurements of E_ES and E_ED were obtained before bypass. On achieving stable hemodynamics (systolic blood pressure, 80 mm Hg; Cardiac Index, 1.6 L/min/m²) after weaning from bypass, an additional set of two measurements of contractility were obtained. Fifteen minutes later, a final set of two measurements of E_ES and E_ED were obtained.

Data analysis
Comparisons of means were analyzed by analysis of variance. Incidence comparisons were analyzed using Fisher’s exact test (two-tailed). A value of p less than or equal to 0.05 was considered statistically significant. All values are expressed as mean values ± SD. The study was designed to have an 80% power to show a 50% reduction in the change in ventricular function.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Demographics
Sixty-seven patients were enrolled and 62 completed the study. Five patients were excluded for technical reasons. Coronary sinus canulation was impossible in 4. One patient’s aortic cannulation was difficult, making continuation in the study inappropriate. Patient demographics (Table 2) and prebypass cardiac function (Table 3) did not differ significantly between the two study groups.

Diastolic function
Intraoperative diastolic ventricular function as measured by the E_ED was not affected by choice of cardioplegia (Table 3) but did stiffen with both types of cardioplegic arrest. E_ED increased in both the CB (0.03 ± 0.05 mm Hg/mL, p = 0.04) and IRWSE + CB (0.03 ± 0.04 mm Hg/mL, p = 0.0009) groups.

Timing
The total operating room time (CB, 4.8 ± 1.0 hours vs IRWSE + CB, 4.7 ± 0.6 hours; p = 0.80) and bypass time (CB, 112 ± 22 vs IRWSE + CB, 116 ± 25 minutes; p = 0.54) were similar in the two groups (Table 4). Aortic cross-clamp time was significantly shorter in the CB group (CB, 67 ± 14 minutes vs IRWSE + CB, 73 ± 15 minutes; p = 0.041), but patients in the CB group required significantly more defibrillation attempts (CB, 3.1 ± 2.1 vs IRWSE + CB, 1.7 ± 1.6; p = 0.0052). The time to return to normal sinus rhythm depends on how the data are analyzed. If the time to return to normal sinus rhythm is timed from removal of the cross-clamp, then return was more rapid in the IRWSE + CB group (CB, 457 ± 324 seconds vs IRWSE + CB, 92 ± 745 seconds; p = 0.019). But, several patients in the IRWSE + CB group returned to normal sinus rhythm during the warm reperfusion phase before removal of the aortic cross-clamp, thus achieving a negative time. If the time to return to normal sinus rhythm begins at reperfusion (ie, the start of warm [normothermic] reperfusion in the IRWSE + CB group, and at the time of aortic cross-clamp removal in the CB group), then the return time does not differ between the two groups (CB, 457 ± 324 seconds vs IRWSE + CB, 392 ± 745 seconds; p = 0.67) (Table 4).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The primary finding of this study was that the IRWSE + CB cardioplegic regimen caused a transient unsustained improvement in left ventricular systolic function in the immediate postbypass period. Systolic function immediately after bypass, as measured by E_ES, was improved in the IRWSE + CB group. Five to 7 days postoperatively, the CB group had better ejection fractions than those of the IRWSE + CB group by MUGA scanning. There was no difference in the number of Q wave or CPK-MB diagnosed myocardial infarctions. The expected incidence of myocardial infarction defined by CPK-MB greater than or equal to 100 U/L is 19% [9], and the study had a combined incidence of 3%. The expected incidence of Q wave MI is 6% [9], and the study had 8%. There were no deaths or strokes in the study population.

Comparison with the results of others
Clinical studies of cardioplegic technique range from randomized, controlled, to nonrandomized, uncontrolled trials of multiple permutations of techniques. For example, there are two randomized controlled trials of cold maintenance cardioplegia with a warm component. In 20 patients undergoing CABG surgery, Teoh and associates [14] found that terminal warm blood cardioplegia improved myocardial ATP, glycogen stores, lactate extraction, and diastolic function (as measured by left atrial pressure and left ventricular end-diastolic volume index), while cold blood cardioplegia without terminal warm blood infusion improved creatinine phosphate. Roberts and associates [5] studied 45 low-risk patients undergoing CABG surgery. Cold blood cardioplegia with terminal warm reperfusion resulted in a significantly higher incidence of spontaneous defibrillation (12 of 15) than either of the other two techniques (5 of 15 with standard cold cardioplegia and 6 of 15 with warm cardioplegic induction) (p < 0.05). The present study confirms the reduced requirement for defibrillation attempts, but differs by demonstrating short-term improvements in left ventricular systolic function in the IRWSE + CB group and longer term improvements in ejection fraction (EF%) in the CB group.

In contrast, several nonrandomized studies of substrate-enriched warm induction/reperfusion cardioplegia techniques report success. In 80 patients undergoing CABG surgery, substrate-enriched, warm reperfusion technique was used and discussed; however, this study lacked a control group [1]. Similarly, a nonrandomized study of 23 patients in which 12 received warm glutamate-enriched cardioplegia before cold cardioplegia and 11 received cold cardioplegia without glutamate demonstrated a higher cardiac index and shorter inotropic support in the IRWSE + CB group. Another nonrandomized study comparing the use of aspartate-enriched warm reperfusion with crystalloid cardioplegia for cardiac transplant donor heart preservation reported a higher rate of spontaneous defibrillation associated with the technique [15], but no other statistically significant differences.

Critique of methods
Sample size
The present study is relatively small, with only 67 patients enrolled and 62 completing the study. We attempted to include patients with depressed ventricular function but had an average EF% of 60. The study was designed using ventricular function as the outcome variable in an effort to have sufficient power with a smaller sample size. This study was not designed to have sufficient power to determine a difference in clinical outcomes of myocardial infarction, death, or congestive heart failure, and we did not detect a difference.

Measures of ventricular function
We used multiple measures of ventricular function, including both common clinical indices (EF% measured by angiography, echocardiography, and MUGA scanning) and nonclinical indices (E_ES, E_ED). Our intent was to provide a clinical basis from which to compare nonclinical indices and to determine if the two types of measurements yielded a consistent pattern in findings. Unfortunately, the improved systolic function in the IRWSE + CB group detected by measurement of E_ES persisted for less than 15 minutes. The EF% measured by postbypass echocardiography and postoperative MUGA did not support an improved ventricular function with IRWSE + CB. Both cardioplegic techniques were associated with a stiffening of end-diastolic function (E_ED).

Volume conductance measurements
The present study used volume conductance measurements of left ventricular function as an outcome variable. Previous clinical studies have demonstrated changes in systolic and diastolic function with hypertrophy and pacing [16], inotropes [17], and myoplasty [18]. While the use of volume conductance technology in human investigation is limited, it has been used extensively in animals and some validation studies have been performed in humans. Volume conductance catheter and biplane angiography measurements of volume in patients correlate well (Vcc = 0.94 V angio + 5.3 mL, r = 0.94, p < 0.001) [19, 20].

Summary
Induction and reperfusion with warm substrate-enriched cardioplegia caused a statistically significant increase in the incidence of spontaneous defibrillation and improved immediate postbypass systolic function (E_ES). Systolic function as measured by EF% was better in the CB group 5 to 7 days postoperatively. The IRWSE cardioplegia technique adds expense, complexity, and prolongs cross-clamp time. There is no prolonged clinically significant benefit of induction and reperfusion with substrate-enriched cardioplegia over cold blood cardioplegia. If postoperative ventricular function is used as the gold standard, cold blood cardioplegia was a better method of myocardial preservation. There may be a subset of patients with very poor postbypass function or preoperative ischemia in which the transient improvements in E_ES from the IRWSE technique are significant and may help in weaning from bypass, but there is little evidence to support this theory.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
This trial was designed as an independent assessment of induction and reperfusion with the substrate-enriched blood cardioplegia technique of Gerald D. Buckberg, MD. The cardioplegia regimen was designed in cooperation with Dr Buckberg to model his technique. All other study design, data collection, analysis, interpretation, and publication were done independently of Dr Buckberg. This work was supported by the International Anesthesia Research Society: B.B. Sankey Award; the Foundation for Anesthesia Education Research: Young Investigator Award; Kaiser Foundation Research; and the Ischemia Research and Education Foundation. We would like to thank Stan Glantz, PhD, and Elizabeth X. Li, MS, for their help with statistical analysis 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 B. Ratcliffe M. Terry McEnany Keith Flachsbart Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wallace, A. W. Articles by Mangano, D. T. Search for Related Content PubMed PubMed Citation Articles by Wallace, A. W. Articles by Mangano, D. T.