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Ann Thorac Surg 2005;80:989-994
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Blood Cardioplegia Provides Superior Protection in Infant Cardiac Surgery

Kerstin Åmark, MD a , * , Håkan Berggren, MD, PhD b , Kerstin Björk, CCP b , Annica Ekroth, CCP b , Rolf Ekroth, MD, PhD b , Krister Nilsson, MD, PhD a , Jan Sunnegårdh, MD, PhD a

a Department of Pediatric Cardiology and Pediatric Anesthesia and Intensive Care, The Queen Silvia Children’s Hospital, Göteborg, Sweden
b Department of Thoracic and Cardiovascular Surgery, Sahlgrenska University Hospital , Göteborg, Sweden

Accepted for publication March 23, 2005.

* Address reprint requests to Dr Åmark, Department of Pediatric Cardiology, The Queen Silvia Children’s Hospital, SE-416 85 Göteborg, Sweden (Email: kerstin.amark{at}vgregion.se).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: We hypothesized that blood cardioplegia preserves myocardial metabolism and function more effectively than St Thomas’ crystalloid cardioplegia in infant cardiac surgery.

METHODS: Thirty infants with atrioventricular septal defects were randomly allocated to either blood or crystalloid intermittent cold (4°C) cardioplegia. Arterial and coronary sinus blood was analyzed for lactate and oxygen. Cardiac output (thermodilution) and left ventricular function (echocardiography) were evaluated.

RESULTS: The lactate concentration in coronary sinus blood early after bypass was significantly higher after crystalloid cardioplegia than after blood cardioplegia (2.1 ± 0.3 vs 1.3 ± 0.1 mmol/L, p = 0.006), with a significant myocardial release of lactate after crystalloid but not after blood cardioplegia. Oxygen extraction (arterial–coronary sinus O2 content) was higher early after crystalloid cardioplegia (3.02 ± 0.13 vs 2.35 ± 0.22 mmol/L, p = 0.01), possibly reflecting a difference in oxygen debt. The cardiac index was higher after blood cardioplegia (4.9 ± 0.3 vs 4.0 ± 0.3 L/min–1/m–2, p = 0.04) and echocardiographic grading of left ventricular function was better (4.1 ± 0.17 vs 3.5 ± 0.22 arbitrary units, p = 0.046).

CONCLUSIONS: This study indicates that blood cardioplegia preserves myocardial metabolism and function more effectively than crystalloid cardioplegia in infant cardiac surgery. The clinical significance of this finding is uncertain, but the more than 20% increase in cardiac index in the critical phase during weaning from bypass may be advantageous.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
The prevention of postoperative heart failure is a major issue in cardiac surgery. Extensive work has been done to increase our understanding of its physiologic background and clinical implications in adult surgery. In contrast, our knowledge in pediatric heart surgery is limited, but it suggests that ischemic injury has a greater impact on the immature heart [1].

Cardioplegia (cp) is probably the most important instrument for protecting the heart from ischemic injury and postoperative heart failure. It has been in general use for decades, initially with a crystalloid solution, which was then gradually replaced by blood cp. This trend can be primarily explained by theoretical considerations and by experimental evidence supporting the use of blood cp. However, clinical, prospective, and randomized studies comparing the two modes of cp in relation to clinical end-points are rare and contradictory [2–6] and several centers still use crystalloid cp. In pediatric patients, Young and colleagues [7] found no demonstrable advantages from blood versus crystalloid cp, evaluated by clinical variables and echocardiography. Caputo and colleagues [8] and Modi and colleagues [9] reported that blood cp resulted in less reduction in myocardial adenosine triphosphate and lower plasma troponin I after pediatric heart surgery but did not affect clinical outcome.

The primary aim of the present study was to determine whether blood cardioplegia preserves myocardial metabolism and function more effectively than crystalloid cp in infants operated on for atrioventricular septal defects (AVSD). Coronary sinus lactate, cardiac output, and echocardiographic evaluation of myocardial function were chosen as outcome variables for this evaluation. We assumed that any difference would be more prominent and easily detected early after cross–clamping. We therefore focused on the period immediately after weaning from bypass. A secondary objective was to determine whether any effect in this period was still detectable after another 60 minutes of follow–up.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Inclusion–Exclusion Criteria
Consecutive infants, referred to us for elective correction of complete AVSD without other major anomalies, were included. Patients with a persistent left superior caval vein to the coronary sinus were excluded. Thirty–two patients qualified for participation. Two were excluded, as parental consent was not obtained. Preoperative clinical data are shown in Table 1.


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  		Table 1. Preoperative Clinical Observations (at Admission)
 
Anesthesia and Cardiopulmonary Bypass (CPB) Technique
Invasive arterial and central venous pressures, electrocardiogram, rectal and nasopharyngeal temperature, inspiratory and expiratory gas concentrations, and pulse oximetry were continuously monitored. Anesthesia was induced with intravenous midazolam and ketamine and pancuronium was used for muscle relaxation. For analgesia, fentanyl was used in combination with isoflurane in a mixture of oxygen and air in the breathing circuit and in the cardiopulmonary bypass sweep gas aiming at a mean arterial pressure of 35 to 40 mm Hg during bypass. Heparin (300 U/kg–1) was given (activated clotting time > 480 s). The CPB prime contained 150 to 300 mL of buffered electrolyte solution, 100 mL albumin 200 mg/mL–1, 100 mL (50 mmol) buffer, 2 mL/kg–1 mannitol (150 mg/mL–1), and heparin 100 U kg–1. Erythrocytes were added for a hematocrit of 25%. The CPB was performed with a nonpulsatile flow at a minimum rate of 2.8 L·min–1 ·m–2 and with a Minimax Plus hollow fiber membrane oxygenator (Medtronic, Anaheim, CA). The alpha–stat blood gas regimen was used.

Weaning from CPB was commenced at a rectal temperature of 36°C and was managed with bolus injections of calcium glubionate 9 mg/mL–1 and dopamine, as indicated by central venous, systemic, and pulmonary arterial pressures and blood gases. The resumption of CPB was indicated if a mean arterial pressure above 40 mm Hg could not be maintained, at arterial hypoxia (SaO2 < 90%), or pulmonary artery pressures equal to systemic arterial pressures. Heparin reversal was achieved by 1 mg of protamine/100 U of heparin administered.

Surgical Technique
A transatrial two–patch repair was performed using a polytetrafluoroethylene patch for the ventricular septum and a pericardial patch for the primum defect. The common atrioventricular (AV) valve was parted to the right and left side and closure of the AV-valve cleft was performed in all cases. Either of two principle surgeons (A and B) participated at all operations.

Postoperative Management
Routine monitoring included the systemic, pulmonary arterial and central venous pressures, electrocardiography, urine production, rectal temperature, pulse oximetry, and blood gases. Morphine and midazolam were continuously infused. Albumin and dopamine (up to 15 µg·kg–1 ·min–1) infusions were used to obtain a mean arterial pressure of greater than 45 mm Hg. Nitric oxide was started if the mean pulmonary artery (PA) pressure exceeded two–thirds of the systemic mean pressure. Weaning from the ventilator was initiated when the patient had adequate mean arterial pressures, a mean PA pressure of less than two–thirds of the mean systemic arterial pressures, and FiO2 less than 40% with stable blood gases.

Study Protocol
Cardioplegia
The children were randomly allocated to blood or crystalloid cp. The crystalloid group had Plegisol (or St Thomas’ II crystalloid cp; Abbott Scandinavia AB, Sweden) with the following content: K+, 16 mM; Ca2+, 2.4 mM; Na+, 120 mM; Cl–, 160 mM; Mg2+, 32 mM; HCO3 –, 10 mM; and pH 7.8. The blood cp group had a mixture of 1 part potassium–enriched Plegisol (60 mmol KCl added to 1,000 mL Plegisol) and 4 parts of blood from the CPB circuit (final K+ concentration of 15 mM). The blood cp was given through the CPB circuit with pressure control (< 200 mm Hg prior to the heat exchanger) and the crystalloid cp by slow injection (< 50 mL per minute).

Both groups had 20 mL/kg–1 of cp given antegradely through a 4F pediatric aortic root cannula (Medtronic, Inc, Minneapolis, MN) and iterated (10 mL/kg–1) every 20 to 30 minutes. The temperature of the blood cp was regulated to 4°C by the heat exchanger of the cardioplegia circuit and the crystalloid cp was kept on ice after being taken out of the 4°C refrigerator. The temperature was not measured at the end of the infusion line.

Blood samples
During surgery, a 20 G Ohmeda Hydrocath (Ohmeda, Duisberg, Germany) polyurethane line infusing heparin (5 U mL–1 at 1 mL/hr–1) was placed in the coronary sinus. Coronary sinus and arterial samples were collected simultaneously at the termination of CPB and after 30 and 60 minutes. Lactate samples were immediately analyzed with a YSI 2300 Stat Plus analyzer (Yellow Springs, OH) and blood gases with an ABL 625 analyzer (Radiometer, Copenhagen, Denmark). The mean of triple analyses was calculated.

Cardiac output measurements
A 3.5 F double–lumen thermodilution catheter (Baxter Healthcare Corp, Irvine, CA) was placed in the main pulmonary artery through the right ventricular wall and connected to a Baxter-Edwards COM-2 cardiac output computer. A Baxter CO set was used to inject 3 mL of cold (< 8°C) 5% dextrose solution into the right atrium. Measurements were made after terminating CPB and after 30 and 60 minutes by one investigator blinded to the type of cardioplegia. The mean of three repeated readings was calculated and indexed to body surface area (cardiac index).

Ultrasound evaluation
An Acuson 128 XP sonography system (Acuson Corp, Mountain View, CA) was used. We routinely performed a transthoracic study the day before surgery, followed by a transesophageal study in the operating room, approximately 20 minutes after the termination of CPB, and a transthoracic study in the intensive care unit early next morning. Two observers, blinded to the type of cardioplegia, reviewed the echocardiograms independently for left ventricular (LV) function and AV-valve regurgitation according to five–grade scales: 5 = normal and 1 = severely impaired function and 0 = no AV-valve regurgitation and 4 = severe regurgitation.

Statistics
The lactate concentration of coronary sinus blood was used as the primary end–point for power calculations. Based on our previous data [10], it was calculated that 26 patients would be required to detect a 30% difference in coronary sinus blood lactate content between the two groups for 80% power with a 5% significance level. Data are presented as means ± standard error of the mean unless otherwise specified. The Student’s t test was used when appropriate. Nonparametric data were analyzed using the Mann-Whitney rank sum test, Fisher’s exact test, and Spearman’s rank correlation. Intergroup analyses were restricted to measurements early after bypass and 60 minutes later according to the primary and secondary aims.

Ethical Considerations
The study was approved by the Ethics Committee at The Sahlgrenska Academy at Göteborg University and was conducted according to the World Medical Association Declaration of Helsinki.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Clinical Course
There was no hospital mortality and 23 of 30 patients had an uneventful clinical course. Two children (one in each cp group) needed reoperation for left AV-valve regurgitation 5 and 14 days postoperatively. Three patients had a prolonged hospital stay due to pleural or pericardial effusions and two due to infection. Further perioperative observations are shown in Table 2.


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  		Table 2. Perioperative Data
 
Metabolic Variables
Lactate levels in coronary sinus blood were 2.1 ± 0.3 mmol/L immediately after bypass in the crystalloid group and 1.3 ± 0.1 mmol/L in the blood cp group (p = 0.006). The calculated difference between arterial and coronary sinus lactate concentrations showed the release of lactate (coronary sinus > arterial concentration) after crystalloid cp but not after blood cp (–0.55 ± 0.15 vs –0.03 ± 0.04 mmol/L, p = 0.002) (Fig 1A). The oxygen extraction (defined as arterial oxygen content minus coronary sinus oxygen content) was significantly higher in the crystalloid group than in the blood cp group (3.02 ± 0.13 vs 2.35 ± 0.22 mmol/L, p = 0.01) immediately after bypass (Fig 1B). None of these differences remained 60 minutes later (Figs 1A and 1B).



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  		Fig 1. Mean and standard error of the mean are shown. (A) The difference between arterial and coronary sinus lactate concentrations (mmol/L) immediately after bypass and after 30 and 60 minutes, showing the release of lactate in the crystalloid group. (B) The difference between arterial and coronary sinus oxygen concentrations (mmol/L) immediately after bypass and after 30 and 60 minutes, illustrating higher oxygen uptake in the crystalloid group. {blacksquare} = blood cardioplegia (cp); {square} = crystalloid cp.

 
Cardiac Output
Cardiac index (cardiac output indexed for body surface area) was higher with blood cp after terminating CPB (4.9 ± 0.3 vs 4.0 ± 0.3 L/min–1/m–2, p = 0.04). Sixty minutes later, there was no longer any detectable difference between the groups (Fig 2A). A number of variables of relevance for cardiac output measurements and LV function are listed in Table 3. These variables were analyzed for group differences. Two of them, serum calcium and pulmonary artery pressure, differed significantly between groups and they were analyzed with regression analysis in relation to cardiac index. No significant correlation was found (calcium vs cardiac index: r = 0.28, p = 0.18; and mean pulmonary artery pressure vs cardiac index, r = 0.075, p = 0.7).



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  		Fig 2. Mean and standard error of the mean are shown. (A) Cardiac index by thermodilution immediately after bypass and after 30 and 60 minutes. (B) Left ventricular function by arbitrary grading (5 = normal function and 1 = severely impaired function) preoperatively (at admission), after bypass, and the next day. {blacksquare} = blood cardioplegia (cp); {square} = crystalloid cp.

 

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  		Table 3. Variables of Hemodynamic Importance Immediately After CPB and 60 Minutes Later
 
Echocardiography
There was no preoperative difference in left ventricular function between groups. All but two patients had normal grading (5/5). Both had slightly below normal function (4/5) and had been allocated evenly (one to each group). Postoperatively, approximately 20 minutes after CPB, function was significantly better in the blood cp group than in the crystalloid group (4.1 ± 0.17 vs 3.5 ± 0.22 arbitrary units, p = 0.046). The next morning, no significant difference was seen (Fig 2B). The variables in Table 3 were also analyzed in relation to the grading of LV function. There was no significant correlation between serum calcium levels or mean pulmonary artery pressure and the grading of ventricular function: r = 0.17 (p = 0.40) and r = –0.07 (p = 0.75), respectively.

Left AV-valve regurgitation after CPB was graded 2.0 ± 0.1 in the crystalloid group and 1.4 ± 0.2 in the blood cp group (p = 0.01) and the next morning it was 1.8 ± 0.2 and 1.4 ± 0.2, respectively (p = 0.18). The right AV-valve regurgitation was 0.7 ± 0.2 (crystalloid cp) and 0.5 ± 0.1 (blood cp) (p = 0.46) after CPB and 0.4 ± 0.2 and 0.5 ± 0.1 the next morning (p = 0.44).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
The principal finding in this study was that blood cardioplegia (cp) provided superior protection of myocardial metabolism and function compared with crystalloid cp when measured directly after weaning from bypass. This difference soon disappeared but may be potentially advantageous in a critical phase of heart surgery.

Metabolic Findings
Lactate is normally extracted by the heart in proportion to its extracellular and arterial concentration. In healthy adults, the heart extracts approximately 40% of the coronary arterial supply of lactate [11]. In conjunction with surgical trauma, lactate extraction decreases and, after cardiac surgery, the heart extracts little or no lactate [10]. This change is largely the effect of impeded pyruvate dehydrogenase activity, preventing pyruvate from entering the Krebs cycle [12]. The change is amplified by ischemia, which provokes the release of lactate from the heart. In the present study, neither cp group exhibited the extraction of lactate. Instead, after crystalloid cp a significant release of lactate occurred, but this was not found after blood cp. The observation that lactate was released from the heart 40 minutes after declamping the aorta and reperfusion with unrestricted perfusion with fully oxygen-saturated blood suggests that the aerobic metabolism needs time to recover. The findings after crystalloid cp resemble our previous observation regarding cerebral metabolism after deep hypothermic arrest [13]. The difference in oxygen measurements between the groups is compatible with more profound ischemia in crystalloid cardioplegia with protracted myocardial oxygen debt.

Myocardial Function
The LV function was evaluated in two ways: first by measuring cardiac index and second by echocardiography. Cardiac output was higher immediately after terminating CPB when blood cp had been used. This is in line with improved protection with less impaired LV function and less early postoperative mitral regurgitation. However, LV function is only one of a number of factors that determine cardiac output. Our analyses indicate that cardioplegia type was the only significant independent variable for cardiac index after weaning from bypass.

Quantitative echocardiographic methods for the calculation of LV function are often used. When designing the present study, they were not considered optimal in patients with this particular heart defect due to preoperative difficulty in defining the left ventricular volume and postoperatively to abnormal movements of the septum from residual pulmonary hypertension or large VSD patching.

The echocardiography images were therefore evaluated with arbitrary assessment. The same approach was chosen in the only previous randomized study, including an evaluation of LV function, by Young and colleagues [7]. However, they found no functional differences between the two cp regimens. The difference in findings could be related to their more heterogeneous population and shorter ischemic times than in the present series.

Study Design and Limitations
When designing this study, we wanted to minimize interindividual variation in factors that could obscure the evaluation of cardioplegia effects. We therefore included infants with the same malformation, operated electively and within a narrow age range. Caputo and colleagues [8] chose a similar approach, including only VSDs operated at 5 to 6 months. We chose AVSDs, since they generally require longer cross-clamping times, to amplify any difference in protective efficacy. In contrast to our patient selection, Young and colleagues [7] included a wide variety of malformations in children aged between 1 day and 15 years.

This study coincided with the introduction of blood cp in our pediatric practice. To facilitate the introduction, it was decided to keep the technique as simple as possible, excluding, for example, warm induction, terminal rewarming ("hot shot"), and metabolic intervention with amino acids. It is therefore possible that the advantages of blood cp could have been greater with a more sophisticated approach [14–16].

One study limitation relates to the use of concentration differences between arterial and coronary sinus blood to evaluate myocardial metabolism. When this measure is positive, it reflects myocardial uptake and, when it is negative it indicates a release from the myocardium. However, the actual uptake or release is also determined by blood flow. In this study, coronary blood flow was not measured, because no technique for clinical use in infants was available. Great caution should therefore be employed in the interpretation of data. The different values for oxygen extraction (mean values 3.02 vs 2.35 mmol/L) would correspond to a 22% difference in coronary blood flow, which is conceivable. In contrast, the difference in lactate values (means –0.55 vs –0.03 mmol/L) would correspond to an 18-fold difference in coronary blood flow. This is not conceivable and it can be concluded that most of the lactate difference between groups cannot be explained by differences in coronary blood flow (Fig 1A) but instead by metabolic differences related to cardioplegia type.

Clinical Implications
Our study was not designed to evaluate major clinical endpoints. To obtain adequate statistical power for this purpose, far larger samples have to be included. Even so, our data demonstrate a more than 20% difference in cardiac index and LV function. This effect, if also present in patients with borderline functional reserves, could be decisive for the postoperative course and survival.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was conducted using donations from the Freemason Founding Asylum Direction in Göteborg (Frimurare-Barnhusdirektionen), the Göteborg Children’s Clinic Research Fund, and the Swedish Heart and Lung Foundation.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Imura H, Caputo M, Parry A, Pawade A, Angelini GD, Suleiman M-S. Age–dependent and hypoxia–related differences in myocardial protection during pediatric open heart surgery Circulation 2001;103:1551-1556.[Abstract/Free Full Text]
  2. Wandschneider W, Winter S, Thalmann M, Howanietz M, Deutsch M. Crystalloid versus blood cardioplegia in coronary by-pass surgery. A prospective, randomized, controlled study in 100 consecutive adults J Cardiovasc Surg 1994;35(suppl 1–6):85-89.[Medline]
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  4. Elwatidy AMF, Fadalah MA, Bukhari EA, et al. Antegrade crystalloid cardioplegia vs antegrade/retrograde cold and tepid blood cardioplegia in CABG Ann Thorac Surg 1999;68:447-453.[Abstract/Free Full Text]
  5. Jacquet LM, Noirhomme PH, Van Dyck MJ, et al. Randomized trial of intermittent antegrade warm blood versus cold crystalloid cardioplegia Ann Thorac Surg 1999;67:471-477.[Abstract/Free Full Text]
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  7. Young JN, Choy IO, Silva NK, Obayashi DY, Barkan HE. Antegrade cold blood cardioplegia is not demonstrably advantageous over cold crystalloid cardioplegia in surgery for congenital heart disease J Thorac Cardiovasc Surg 1997;114:1002-1009.[Abstract/Free Full Text]
  8. Caputo M, Modi P, Imura H, et al. Cold blood versus cold crystalloid cardioplegia for repair of ventricular septal defects in pediatric heart surgerya randomized controlled trial. Ann Thorac Surg 2002;74:530-535.[Abstract/Free Full Text]
  9. Modi P, Suleiman M-S, Reeves B, et al. Myocardial metabolic changes during pediatric cardiac surgerya randomized study of 3 cardioplegic techniques. J Thorac Cardiovasc Surg 2004;128:67-75.[Abstract/Free Full Text]
  10. Svensson S, Svedjeholm R, Ekroth R, et al. Trauma metabolism and the heart. Uptake of substrates and effects of insulin early after cardiac operations J Thorac Cardiovasc Surg 1990;99:1063-1073.[Abstract]
  11. Carlsten A, Hallgren B, Jagenburg R, Svanborg A, Werkö L. Myocardial metabolism of glucose, lactic acid, amino acids and fatty acids in healthy human individuals at rest and at different work loads Scand J Clin Lab Invest 1961;13:418-428.[Medline]
  12. Schofield PS, McLees DJ, Kerbey AL, Sugden MC. Activities of cardiac and hepatic pyruvate dehydrogenase complex are decreased after surgical stress Biochem Int 1986;12:189-197.[Medline]
  13. van der Linden J, Astudillo R, Ekroth R, Scallan M, Lincoln C. Cerebral lactate release after circulatory arrest but not after low flow in pediatric heart operations Ann Thorac Surg 1993;56:1485-1489.[Abstract]
  14. Toyoda Y, Yamaguchi M, Yoshimura N, Oka S, Okita Y. Cardioprotective effects and the mechanisms of terminal warm blood cardioplegia in pediatric cardiac surgery J Thorac Cardiovasc Surg 2003;125:1242-1251.[Abstract/Free Full Text]
  15. Carrier M, Pellerin M, Perrault LP, et al. Cardioplegic arrest with L-arginine improves myocardial protectionresults of a prospective randomized clinical trial. Ann Thorac Surg 2002;73:837-842.[Abstract/Free Full Text]
  16. Kjellman U, Björk K, Ekroth R, et al. {alpha}-ketoglutarate for myocardial protection in heart surgery Lancet 1995;345:552-553.[Medline]
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