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Ann Thorac Surg 1996;62:1146-1151
© 1996 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Effect of Intermittent Warm Blood Cardioplegia on Functional Recovery After Prolonged Cardiac Arrest

Martin Tönz, MD, Otto N. Krogmann, MD, Otto M. Hess, MD, Boris Leskosek, BA, Tomislav Mihaljevic, MD, Ludwig K. von Segesser, MD, Marko I. Turina, MD

Clinic for Cardiovascular Surgery and the Division of Cardiology, University Hospital, Zurich, Switzerland

Accepted for publication May 15, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background. There is some evidence that continuous warm blood cardioplegia offers good myocardial protection; however, the effects of interrupting cardioplegia remain controversial. To study this, we compared the effects of continuous and intermittent antegrade warm (37°C) blood cardioplegia on functional recovery after prolonged cardiac arrest (180 minutes).

Methods. Twenty-four juvenile pigs were randomly assigned into four groups. Group 1 received continuous cardioplegia, group 2 underwent several periods of 15 minutes of cardioplegia interrupted by 5 minutes of normothermic ischemia, and group 3 underwent several periods of 10 minutes of cardioplegia interrupted by episodes of 10 minutes. The hearts of group 4 received no cardioplegia. Left ventricular systolic function was assessed from fractional left ventricular shortening and percentage left ventricular wall thickening, and left ventricular diastolic function was determined from the time constant of relaxation and the constant of myocardial stiffness.

Results. Systolic and diastolic functions were slightly depressed 1 and 2 hours after cross-clamp removal in all four groups, without significant differences among the groups.

Conclusions. These data suggest that antegrade warm blood cardioplegia can be interrupted for up to 10 minutes without obvious negative effects on left ventricular function in the normal myocardium, provided that the intermittent doses of cardioplegia are sufficient to restore the metabolic demands of the arrested myocardium.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Continuous normothermic blood cardioplegia has emerged recently as an alternative method of myocardial protection. This method may, theoretically, be the optimal technique for heart protection because it prevents myocardial ischemia and subsequent reperfusion injury [1]. However, in daily practice, continuous infusion of warm blood cardioplegia may obscure the operating field and therefore must be discontinued for short intervals. A growing number of investigations in recent years have examined the effects of intermittent ischemia during warm blood cardioplegia on myocardial recovery after elective cardiac arrest. However, experimental data in this context are conflicting. Using an isolated perfused pig heart model, Tian and associates [2] found no difference in metabolic and functional recovery with intermittent antegrade warm blood cardioplegia as compared with continuous warm cardioplegia after 90 minutes of cardiac arrest. Landymore and co-workers [3] studied the effects of warm intermittent cardioplegia during a 90-minute arrest in a dog model. They found that systolic function was well preserved, whereas diastolic function and metabolic recovery were impaired during reperfusion. In contrast, Ko and colleagues [4] reported profound tissue acidosis and marked functional deterioration during the immediate recovery period if warm antegrade blood cardioplegia was interrupted for 10 minutes. Inherent to all these studies is the limitation that all animals used for the experiments were healthy, without cardiac diseases. In consideration of these problems, we studied the effects of interrupted "continuous" antegrade warm blood cardioplegia on functional recovery of the myocardium in a pig model, using an excessively long aortic cross-clamping time of 3 hours to stress the myocardial metabolism as much as possible.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Experimental Preparation
Twenty-four domestic pigs weighing between 75 and 85 kg (age, 5 to 6 months) were randomized to receive different modes of myocardial preservation during prolonged cardiac arrest. The animals received humane care according to the principles of laboratory animal care formulated by the Swiss Academy of Science.

Surgical Preparation
After premedication, the animals were anesthetized with volatile anesthetic agents and were mechanically ventilated with a nitrous oxide/oxygen mixture. A three-lead electrocardiogram, an aortic pressure line (through the right carotid artery), a venous sampling line (through the right internal jugular vein), and a pulmonary artery thermodilution catheter (Swan-Ganz Oximetry TD Catheters, Baxter, Irvine, CA) were installed, and then a median sternotomy was performed. The left pleural space was opened to ligate the left hemiazygos vein, which empties directly into the coronary sinus. After resection of the thymus gland, the pericardium was opened and sutured to cradle the heart.

Two flow probes (Transonic Systems Inc, Ithaca, NY) were positioned around the proximal right coronary artery and the proximal left anterior descending coronary artery. A myocardial thermistor probe (Shily Inc, Irvine, CA) was inserted into the interventricular septum. Catheters were placed in the coronary sinus and the left atrium for blood sampling and pressure monitoring, respectively. An 8F high-fidelity micromanometer tip catheter (Millar Instruments, Houston, TX) was inserted into the left ventricle through the left atrium. A pair of ultrasonic crystals was placed in the anterior left ventricular (LV) free wall for measuring LV wall thickness. A second pair was used to measure the LV external short-axis diameter. The anterior crystal was sutured to the epicardium between the left anterior descending coronary artery and its first diagonal branch, and the posterior crystal was placed directly opposite between the coronary sinus and the posterior interventricular coronary vein. Cardioplegia was delivered through a cannula placed in the aortic root.

After systemic heparin treatment (300 IU/kg body weight), cardiopulmonary bypass was established with an arterial perfusion cannula in the ascending aorta and direct bicaval cannulation for venous return. Disposable human membrane oxygenators (Ultrox; SciMed Life Systems, Inc, Minneapolis, MN) were primed with a heparin-treated starch solution with the addition of 2 million U of aprotinin. Nonpulsatile pump flow was adjusted at a rate of 75 mL•kg-1•min-1, and perfusion temperature was maintained at 37°C. Ties were passed around both venae cavae and snared during aortic cross-clamping.

The right ventricle was vented through the right atriotomy and the left ventricle through a small left atriotomy. Partial pressures of carbon dioxide and oxygen and pH were monitored, and appropriate adjustments were made as required throughout the study.

Myocardial Preservation
The 24 animals were randomized into four groups (Fig 1Go). Group 1 (Warm Cont, n = 7) received antegrade continuous high-potassium warm blood cardioplegia. Blood was taken directly from the oxygenator by a 1/4-inch tube and was infused at 37°C into the aortic root by means of a roller pump at a flow of 2 to 2.5 mL•kg-1•min-1. With this flow rate, the aortic root pressure was 54 ± 6 mm Hg and the coronary sinus oxygen saturation was 87% ± 2% during cardioplegia delivery (coronary sinus oxygen saturation before cardiopulmonary bypass, 38% ± 0.3%). A syringe pump was connected to the 1/4-inch tubing to deliver concentrated potassium and magnesium solution (K+, 0.8 mol/L; Mg2+, 0.15 mol/L) [5]. Potassium and magnesium concentrations of cardioplegia were adjusted to 12 to 14 mmol/L K+ and 2.5 to 3.5 mmol/L Mg2+, respectively. The hemoglobin content of blood cardioplegia was 9.4 ± 0.5 g/dL. Ultrafiltration (Gambro; Gambro Dialysatoren GmbH & Co, Hechingen, Germany) was used during bypass to maintain systemic normokalemia. Group 2 (Warm Int5', n = 6) received the same cardioplegia solution at the same temperature and flow rate as in group 1. However, cardioplegia was interrupted for 5 minutes every 20 minutes. In group 3 (Warm Int10', n = 6), cardioplegia was interrupted for 10 minutes every 20 minutes, ie, for 50% of the aortic cross-clamp time. Aortic cross-clamping was maintained for 180 minutes in all three cardioplegia groups. After release of the aortic cross-clamp, the hearts were reperfused for 30 minutes in a standardized manner. In group 4 (control group; sham-operated animals, n = 5), cardiopulmonary bypass was instituted for 210 minutes without aortic cross-clamping and with an empty beating heart. The animals were weaned from cardiopulmonary bypass with brief catecholamine support (dopamine) and inhalation of nitric oxide to overcome the problems due to excessively high pulmonary arterial pressures during weaning [6, 7].



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  		Fig 1. . Study protocol. Measurements were done at baseline, 1 hour, and 2 hours after release of the aortic cross-clamp. (CONTROL = sham-operated animals with empty beating heart during cardiopulmonary bypass; WARM CONT = continuous antegrade warm blood cardioplegia without interruption; WARM INT5' = intermittent antegrade warm blood cardioplegia with interruptions of 5 minutes; WARM INT10' = intermittent antegrade warm blood cardioplegia with interruptions of 10 minutes.)

 
Measurements
Right atrial pressure, pulmonary artery pressure, left atrial pressure, aortic pressure, left ventricular pressure with its first derivative (dp/dt), LV short axis, LV wall thickness, and myocardial temperature were recorded continuously on a 16-channel computerized recording system (Hellige GmbH, Freiburg im Breisgau, Germany). Baseline measurements were completed after a 30-minute equilibration period. Postbypass measurements were accomplished 1 hour and 2 hours after the release of aortic cross-clamping (see Fig 1Go). Preload conditions were held constant during reperfusion with the aid of volume administration.

Data Analysis
Data were recorded digitally on-line with a sampling rate of 300 Hz/channel (Hellige GmbH). Mathematic analysis of the data was performed off-line on a personal computer (Macintosh IIci; Apple Computer Inc, Cupertino, CA). Three beats were averaged for the calculation of systolic and diastolic function indices. End-diastole was defined as the time of the peak R wave and end-systole as the time of aortic valve closure, ie, when the LV pressure fell below the aortic incisural pressure.

Systolic function was evaluated from fractional short-axis shortening and wall thickening. Diastolic function was evaluated from the time constant of relaxation and the constant of myocardial stiffness.

Calculations
Cross-sectional muscle area was used to assess LV wall edema. Left ventricular relaxation was assessed from the time constant of isovolumic pressure decline, starting from maximum negative dP/dt and ending when the pressure had decreased to 5 mm Hg above the end-diastolic pressure. The time constant (T; milliseconds) was calculated according to Mirski [8] as the negative reciprocal of the slope of the exponential relation between LV pressure and time: P = a•e-b•t + P b and T = 1/-b (milliseconds), where P = LV pressure (mm Hg); a = LV pressure at peak negative dP/dt (mm Hg); e = the base of the natural logarithm; b = the slope of the pressure-time relation; t = time (milliseconds); and Pb = the pressure asymptote of the pressure-time relation (mm Hg).

Passive diastolic function was assessed during the period from minimum ventricular wall stress to end-diastole. Left ventricular meridional wall stress was calculated according to Brodie and colleagues [9]. Diastolic myocardial stiffness was determined from the diastolic stress-strain relation using an elastic model with shifting asymptote. First a reference midwall circumference (L1) at a common wall stress of 1 g/cm2 was determined for calculation of wall strain [10]: S = a•eb•L + c, where S = LV meridional stress (g/cm2); a = the elastic constant (g/cm2); b = the slope of the stress-circumference relation (1/cm); L = midwall circumference (cm); and c = the asymptote of the elastic stress-length relation (kdyn/cm2). A computer program on a personal computer (Macintosh IIci; Apple Computer Inc) was used to calculate the constants a, b, and c as well as L1 to provide the closest curve fit of the diastolic stress-circumference relation using a linear regression analysis [11].

Left ventricular wall strain ({epsilon}) was calculated using the Lagrangian strain definition: {epsilon} = (L - L1)/L1, where L = instantaneous midwall circumference and L1 = midwall circumference at a common wall stress of 1 g/cm2.

Diastolic myocardial stiffness was then calculated from an elastic stress-strain model with shifting asymptote: S = a•{epsilon}b•{epsilon} + c, where S = LV circumferential stress (g/cm2); a = the elastic constant (g/cm2); b = the constant of myocardial stiffness; {epsilon} = Lagrangian strain; and c = the asymptote of the elastic stress-strain relation (g/cm2).

Statistical Analysis
All values are expressed as mean ± 1 standard error of the mean. Data were analyzed using a statistical program (StatView 4.0 on Macintosh IIci). Factorial analysis of variance was used to compare data at a given time point, with the Scheffé's F procedure for post hoc testing. Differences within groups were analyzed by repeated-measures analysis of variance for each group separately, and differences between groups and group by time interactions were assessed by two-way analysis of variance. A p value less than 0.05 was considered significant.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
All animals were weaned successfully from cardiopulmonary bypass with brief catecholamine support (dopamine, 10 µg•kg-1•min-1) and inhalation of nitric oxide (up to 40 ppm) to lower pulmonary arterial pressures. Dopamine infusions could be stopped within 15 minutes after weaning.

Hemodynamic Data
There was a slight increase in left atrial as well as pulmonary artery pressure during reperfusion (Table 1Go). Left ventricular end-diastolic pressure increased in all three cardioplegia groups but remained unchanged in the control group. There were no significant changes in heart rate (without Warm Int5') or mean arterial pressures. Coronary artery blood flow increased during reperfusion in all four groups (not significant between groups; results not shown).


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  		Table 1. . Hemodynamic Dataa
 
Dimensional Data
There were no significant differences with regard to preload and afterload during reperfusion among the groups (see Table 1Go). Systolic function decreased slightly during reperfusion when assessed by fractional shortening and wall thickening (Table 2Go; Fig 2Go). End-diastolic diameter and wall thickness remained unchanged during reperfusion (baseline versus 2 hours, end-diastolic diameter (mm): control, 43 ± 3 versus 39 ± 2; Warm Cont, 49 ± 3 versus 48 ± 2; Warm Int5', 54 ± 2 versus 51 ± 3; Warm Int10', 50 ± 2 versus 51 ± 2; not significant; wall thickness (mm): control, 15 ± 1 versus 17 ± 1; Warm Cont, 11 ± 0 versus 12 ± 1; Warm Int5', 12 ± 1 versus 13 ± 1; Warm Int10', 12 ± 1 versus 12 ± 1; not significant).


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  		Table 2. . Dimensional Dataa
 


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  		Fig 2. . Percentage recovery of systolic function 1 hour and 2 hours after release of the aortic cross-clamp. There was a slight decrease in systolic function when assessed by fractional shortening and wall thickening. Data are expressed as mean ± standard error of the mean. (*p < 0.05 versus baseline; abbreviations are as in Figure 1Go.)

 
Derived Data
End-systolic and end-diastolic wall stress did not change in all four groups throughout the experiment (baseline versus 2 hours, end-systolic wall stress (g/cm2): control, 32 ± 6 versus 23 ± 6; Warm Cont, 29 ± 4 versus 31 ± 4; Warm Int5', 36 ± 5 versus 31 ± 7; Warm Int10', 36 ± 7 versus 38 ± 8; not significant; end-diastolic wall stress (g/cm2): control, 14 ± 2 versus 12 ± 2; Warm Cont, 13 ± 3 versus 18 ± 2; Warm Int5', 15 ± 2 versus 15 ± 4; Warm Int10', 13 ± 1 versus 21 ± 3; not significant without Warm Int10' (p = 0.03). Cross-sectional muscle area increased slightly in all groups (Table 3Go). Although the increase was small, it reached statistical significance in all groups except for the control group.


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  		Table 3. . Derived Dataa
 
Diastolic Function Indices
The time constant of LV relaxation tended to increase during reperfusion, without reaching significance (Table 4Go; Fig 3Go). The constant of myocardial stiffness increased in all three cardioplegia groups. The increase was significant in the continuous warm blood group (Warm Cont). The stiffness constant in the control group did not change at all.


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  		Table 4. . Diastolic Function Indicesa
 


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  		Fig 3. . Percentage recovery of diastolic function. There was a slight prolongation of left ventricular relaxation and an increase in myocardial stiffness in all cardioplegia groups 2 hours after release of the aortic cross-clamp. Data are expressed as mean ± standard error of the mean. (*p < 0.05 versus baseline; abbreviations are as in Figure 1Go.)

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Warm cardioplegia has been proposed as a valuable alternative for myocardial protection during open heart operations and has been used recently by a rapidly growing number of cardiac surgeons. Continuous application of the warm cardioplegic solution would be the optimal management for minimizing injury to the myocardium during open heart operations. However, continuous cardioplegia, whether administered in an antegrade or retrograde fashion, has to be interrupted temporarily to provide the surgeon with a bloodless operative field. Thus, a compromise between metabolic and technical requirements must be found with regard to the time for the application of cardioplegia and the duration of interruption during cardiac operations.

To evaluate the potential negative effects of intermittent warm blood cardioplegia, we studied 24 pigs using three different protocols, ranging between 0 and 50% ischemia time. After 3 hours of cardiac arrest, all three protocols showed a similar, although mild depression of systolic and diastolic function. Neither 25% nor 50% interruption of cardioplegic perfusion showed a significant reduction of LV performance compared with continuous administration of the cardioplegic solution.

Effects on Systolic Function
The occurrence of myocardial stunning has been reported by several authors [12, 13] after cardioplegic cardiac arrest. Continuous warm blood cardioplegia ideally would represent a mode of myocardial protection in which no ischemic dysfunction should occur. However, the present investigation clearly showed that a mild LV dysfunction can be observed after 3 hours of continuous warm blood cardioplegia. This functional impairment is probably the result of several different factors, such as permanent hyperkalemia, systemic inflammatory reactions induced by the extracorporeal circulation [14], and nonpulsatile coronary perfusion with impaired autoregulation. The occurrence of mild systolic dysfunction in the sham-operated animals suggests that mechanisms other than stunning, such as the systemic reaction to extracorporeal circulation, may be responsible for cardiac dysfunction after cardiopulmonary bypass.

Interruption of warm blood cardioplegia did not show any further impairment of LV function compared with the continuous administration of cardioplegia. Thus, intermittent administration of antegrade warm blood cardioplegia for 10 minutes is sufficient to restore the metabolic demands of the arrested heart without evidence of aggravating the ischemic injury, even after 3 hours of aortic cross clamping. This is in accordance with the results of Tian and colleagues [2], who found that myocardial energy metabolites and intracellular pH did not show a cumulative effect during the administration of intermittent warm blood cardioplegia for 90 minutes. Whether there is some ischemic preconditioning that prevents cumulative damage to the myocardium with intermittent cardioplegia remains unclear [12]. Inadequate doses of warm blood cardioplegia might have been the reason for the bad functional recovery of the arrested hearts in the study of Ko and co-workers [4] as compared with our study.

Effects on Diastolic Function
Previous investigations [15, 16] have indicated that diastolic function indices are more sensitive than systolic function indices to changes in LV perfusion and ischemic injury. Diastolic function has been separated into relaxation, filling, and passive elastic properties. The present investigation shows clearly that relaxation is slightly, although not significantly, prolonged after warm antegrade cardioplegia, confirming the results of previous studies [4, 17]. The passive elastic properties changed in a similar fashion, ie, the constant of myocardial stiffness increased during reperfusion in the three cardioplegia groups but remained unchanged in the control group. This change in stiffness was accompanied by an increase in LV end-diastolic pressure and LV end-diastolic stress despite a similar end-diastolic diameter. This suggests that the increase in filling pressure was due to a change in the passive elastic properties. The increase in LV cross-sectional area indicates wall edema, which could well lead to diminished ventricular compliance [18, 19]. The effect of the stunned myocardium on diastolic function is less clear, but might be involved as well (chronic ischemia). However, no correlations were observed between myocardial stiffness and systolic function or relaxation, suggesting that myocardial edema is the major determinant of the changes in stiffness after prolonged cardiac arrest despite myocardial protection with warm cardioplegia.

Limitations
Even with a very long aortic cross-clamp time, a normal heart may behave differently with regard to the effects of intermittent ischemia compared with a diseased heart. Caldarone and associates [20] showed that even aging had a significant effect on tolerance to cardioplegic arrest. Lichtenstein and colleagues [1] administered cardioplegia in an antegrade fashion in their initial report on warm heart operations. In clinical practice, continuous warm blood cardioplegia is used predominantly in a retrograde fashion, although a number of clinical trials on antegrade warm cardioplegia have been published in recent years [21–24]. Because the distribution of blood flow [25] and myocardial metabolism [26] differ significantly if cardioplegia is administered through the coronary sinus, our results cannot be transferred to this mode of cardioplegia delivery.

Clinical Implications
There are several conclusions that can be drawn from the present study. (1) Antegrade intermittent warm blood cardioplegia can be performed without obvious negative effects on LV function in the healthy myocardium, even with prolonged aortic cross-clamping, provided that adequate doses of cardioplegia are used to meet the metabolic demands of the arrested myocardium. (2) Despite optimal myocardial perfusion with continuous warm blood cardioplegia, there is a mild systolic dysfunction (stunning?) of the reperfused myocardium. (3) Changes in passive elastic properties appear to be due to the occurrence of myocardial edema. (4) Short interruptions of antegrade warm "continuous" cardioplegia are not associated with negative functional sequelae, supporting the data of recent clinical studies [21–24]. However, because the purpose of warm continuous cardioplegia is to avoid ischemia, interruptions have to be limited as much as possible [27].


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Tönz, Clinic for Pediatric Surgery, University Hospital, 3010 Bern, Switzerland.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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  12. Bolling SF, Olszanski DA, Childs KF, Gallagher KP, Ning XH. Stunning, preconditioning, and functional recovery after global myocardial ischemia. Ann Thorac Surg 1994;58:822–7.[Abstract]
  13. Bolli R. Mechanism of myocardial "stunning." Circulation 1990;82:723–38.[Abstract/Free Full Text]
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  15. Sigwart U, Gerbic M, Payot M, Goy J-J, Essinger A, Fischer A. Ischemic events during coronary artery balloon occlusion. In: Rutishauser W, Roskamm H, eds. Silent myocardial ischemia. Berlin: Springer-Verlag, 1984:29–36.
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  17. Cannon MB, Vine AJ, Kantor HL, et al. Warm and cold blood cardioplegia. Comparison of myocardial function and metabolism using 31p magnetic resonance spectroscopy. Circulation 1994;90(Suppl 2):328–38.
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