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Ann Thorac Surg 2000;69:1914-1919
© 2000 The Society of Thoracic Surgeons

Original articles: Cardiovascular

Clinical evaluation of leukocyte-depleted blood cardioplegia for pediatric open heart operation

Yoshitaka Hayashi, MDa, Yoshiki Sawa, MDa, Motonobu Nishimura, MDa, Hajime Ichikawa, MDa, Koji Kagisaki, MDa, Shigeaki Ohtake, MDa, Hikaru Matsuda, MDa

a Course of Interventional Medicine (E1), Department of Surgery, Osaka University Graduate School of Medicine, Osaka, Japan

Address reprint requests to Dr Sawa, Course of Interventional Medicine (E1), Department of Surgery, Osaka University Graduate School of Medicine, 2–2 Yamada-oka, Suita, Osaka 565–0871, Japan
e-mail: sawa{at}surg1.med.osaka-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Blood cardioplegia (BCP) is widely used for myocardial protection during open heart operation. However, BCP may have a chance to induce neutrophil-mediated myocardial injury during aortic cross-clamping. We clinically evaluated the myocardial protective effect of leukocyte-depleted blood cardioplegia (LDBCP) for initial and intermittent BCP administration in pediatric patients.

Methods. Fifty patients undergoing open heart operation for congenital heart disease between January 1997 and March 1999 were reviewed. Twenty-five were administered LDBCP for myocardial protection during ischemic periods (LDBCP group), and the remaining 25 were given BCP without leukocyte depletion (BCP group).

Results. The difference in plasma concentrations of malondialdehyde between coronary sinus effluent blood and arterial blood just after reperfusion in the LDBCP group (1.68 ± 0.56 µmol/L) was significantly lower than that in the BCP group (2.35 ± 0.62 µmol/L; p < 0.01). The LDBCP group showed significantly lower plasma concentrations of human heart fatty acid-binding protein at 50 minutes after reperfusion (LDBCP group, 103.5 ± 38.7 IU/L; BCP group, 144.8 ± 48.8 IU/L; p < 0.01) and the peak value of creatine kinase-MB during the first 24 postoperative hours (LDBCP group, 17.0 ± 8.5 IU/L; BCP group, 26.0 ± 11.6 IU/L; p < 0.01) than did the BCP group. The maximum dose of catecholamine was significantly smaller in the LDBCP group (LDBCP group, 3.20 ± 2.18 µg · kg-1 · min-1; BCP group, 5.60 ± 2.83 µg · kg-1· min-1; p < 0.01).

Conclusions. These results suggest the usefulness of LDBCP for protection from the myocardial injury that can be induced by BCP administration during aortic cross-clamping.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Current evidence strongly indicates that activated neutrophils contribute to myocardial reperfusion injury after ischemia. Histopathologically, neutrophils have been shown to mechanically obstruct capillaries, thereby inhibiting reperfusion of ischemic tissue, known as the no-reflow phenomenon [1, 2]. The generation of oxygen-derived free radicals, the release of proteolytic enzymes by filtrating neutrophils, or both processes also cause histologic and functional derangement of myocardial tissue [3]. These findings suggest the possible therapeutic effect of leukocyte depletion, which has been found to reduce the extent of myocardial damage after reperfusion [4, 5]. We also have reported the effect of leukocyte-depleted blood reperfusion after ischemia in a neonatal rabbit ischemic heart model, and we demonstrated that both mitochondrial and endothelial damage was reduced by leukocyte-depleted blood reperfusion [6].

Blood cardioplegia (BCP), which was proposed by Follete and colleagues in 1978 [7, 8], is now widely used for myocardial protection during periods of ischemia, as is crystalloid cardioplegia solution. BCP solution is considered superior to crystalloid cardioplegia solution in certain aspects [9, 10]. For example, it can deliver oxygen to the myocardium during the short period before cardiac arrest is achieved, and its components seem to be more physiologic than crystalloid cardioplegia solution [7–10]. On the other hand, BCP solution contains leukocytes and platelets, which may cause capillary plugging after myocardial ischemia and reperfusion during terminal cardioplegia administration [11]. Clinically, we have applied leukocyte depletion to terminal cardioplegia administration (leukocyte-depleted terminal cardioplegia [LDTC]), and we have demonstrated the dramatic myocardial protective effect of LDTC in cases of emergency coronary artery bypass grafting [12] and left ventricular hypertrophy [13]. Possibly, with each administration of BCP, there is the risk of myocardial blood reperfusion inducing neutrophil-mediated reperfusion injury, even in the hypothermic myocardium under ischemia. However, leukocyte depletion for every BCP administration gradually lessens the usefulness of the leukocyte removal filter. It remains unclear whether BCP containing leukocytes may induce myocardial injury before achieving cardiac arrest and during periods of ischemia.

The dose of BCP is determined on the basis of the patient’s body weight, and frequent leukocyte depletion can be applied to such low-body-weight patients as neonates and infants. In the present study, we clinically evaluated the usefulness of leukocyte-depleted blood cardioplegia (LDBCP) for initial and intermittent administration to determine the degree of myocardial protection during pediatric open heart operation.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Study population
Fifty pediatric patients undergoing open heart operation for congenital heart disease at Osaka University Hospital between January 1997 and March 1999 were enrolled in this study. Twenty-four were boys, and twenty-six were girls. Their ages ranged from 3 months to 10 years, with a mean of 1.8 years, and they weighed 4.5 to 17.3 kg, with a mean of 9.73 kg. The parents or guardians of all participants gave informed consent for this study, and we followed the guidelines of our internal review board. Disease conditions comprised ventricular septal defect (n = 18), tetralogy of Fallot (n = 16), double-outlet right ventricle (n = 5), endocardial cushion defect (n = 2), transposition of the great arteries (n = 2), congenital aortic stenosis (n = 4), tricuspid atresia (n = 1), double-inlet right ventricle (n = 1), and endocardial cushion defect with tetralogy of Fallot (n = 1).

Median sternotomy was performed, and cardiopulmonary bypass (CPB) was instituted in all patients. CPB was established with two venous drainages from the superior vena cava and the inferior vena cava, and arterial blood was returned to the ascending aorta. The CPB circuits were composed of a roller pump, a hollow-fiber microporous membrane oxygenator, a heat exchanger, an arterial filter, a venous reservoir, arterial and venous cannulas, and tubing lines, which were primed without blood components. CPB was controlled by {alpha}-stat management, with blood flow rates of 120 to 150 mL·kg-1·min-1 to maintain the mean arterial pressure between 50 and 70 mm Hg, using vasoactive agents if necessary. We measured the blood temperature in the arterial line just after it passed through the heat exchanger and controlled it at 28°C.

Study groups
The 50 patients were randomly divided into two groups. Twenty-five were administered LDBCP for myocardial protection during ischemia (LDBCP group), and the remaining 25 were given BCP without leukocyte depletion (BCP group). To not reflect the influence of the different surgical procedures, each group was subdivided into three groups according to the type of congenital heart disease as follows: ventricular septal defect, tetralogy of Fallot, and other congenital heart diseases. Characteristics of patients in each group, ie, age, sex, body weight, CPB time, aortic cross-clamping time, and the number of cardioplegia infusions, did not differ significantly between the LDBCP group and the BCP group (Tables 1, 2).


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  		Table 1. Comparison of Basic Data Between BCP and LDBCP Groupsa

 

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  		Table 2. Comparison of Basic Data According to Disease Subgroupsa

 
Cardioplegia administration
Oxygenated blood was obtained from the oxygenator reservoir and mixed with cold potassium crystalloid cardioplegia solution (500 mL of Lactate Ringer’s Solution, 40 mEq/L of potassium chloride, and 5 mL of 2.2% sodium citrate buffer solution: Na+, 30 mEq/L; K+, 40 mEq/L; Ca++, 3 mEq/L) using double-head coupled roller pumps (HCP-5000; Senko Medical Co, Ltd, Osaka, Japan). Cardiac arrest was achieved by aortic cross-clamping and an initial antegrade administration of 2:1 blood-crystalloid cardioplegia solution containing a final concentration of 16 mEq/L potassium, and 0.8–1.0 mEq/L calcium which was infused into the aortic root through a cardioplegia cannula. Myocardial protection during ischemia was obtained by intermittent antegrade or retrograde administration of 4:1 blood-crystalloid cardioplegia solution. Retrograde cardioplegia solution was infused into the coronary sinus through a cardioplegia cannula. The initial dose of cardioplegia solution was 10 mL/kg of body weight, and then a half-dose was reinfused every 20 minutes. The hematocrit value was maintained at approximately 20%. The myocardial temperature was monitored at the ventricular septum and maintained less than 15°C with topical cooling if necessary. We measured the temperature of the cardioplegia solution in the cardioplegia line just after it passed through the heat exchanger and maintained it at 15° to 20°C. Terminal BCP administration, with or without leukocyte depletion [12, 13], was not applied in any patients.

In the LDBCP group only, a newly developed leukocyte removal filter (BC-1; Pall, East Hills, NY) for coronary perfusion with heparin-anticoagulated blood was incorporated into the system just after the oxygenator reservoir for leukocyte depletion (Fig 1; Table 3).



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  		Fig 1. Schematic of leukocyte-depleted blood cardioplegia procedure.

 

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  		Table 3. Specifications of the Leukocyte Removal Filter

 
Measurements
The cardioplegia solution was sampled at each administration from both the inlet and outlet of the leukocyte removal filter. Leukocytes and neutrophils were counted, and the depletion ratio was calculated to evaluate the efficiency of leukocyte depletion after several periods of cardioplegia administration.

Arterial blood and coronary sinus effluent blood were obtained just after myocardial reperfusion, and we measured the plasma concentrations of malondialdehyde (MDA) using an ion-pairing high-pressure liquid chromatography method [14]. The coronary sinus effluent blood to arterial blood difference in MDA has been generally used as an index of myocardial lipid peroxidation [14]. (A retrograde cannulation through the coronary sinus was not applied to any patients in the ventricular septal defect group. Thus, we did not measure plasma MDA concentrations of the patients in the ventricular septal defect group.)

We previously reported that the human heart fatty acid-binding protein (HH-FABP) could be observed in the plasma soon after myocardial reperfusion and that it may be an early indicator of myocardial damage after cardiac surgical procedures [15]. Arterial blood was obtained 50 minutes after reperfusion, and HH-FABP concentrations were measured for comparison between groups using a sandwich enzyme immunoassay with two different anti-HH-FABP monoclonal antibodies [16].

Plasma creatine kinase-MB concentrations were measured every 6 hours by immunoinhibition assay, and compared with the peak concentration during the first 24 postoperative hours [17].

The maximum dose of catecholamine, dopamine plus dobutamine, required at the time of weaning from CPB and during the postoperative course was compared between groups (expressed in micrograms per kilogram of body weight per minute).

Scanning electron microscopy
We examined the used leukocyte removal filter with a scanning electron microscope to evaluate the effect of leukocyte depletion after several BCP administrations.

Statistical analysis
All data are expressed as the mean ± standard deviation. One-way analysis of variance was used to test the time-dependent changes in the leukocyte depletion ratio. Student’s t test was used to compare the data between groups. A p value of less than 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Clinical outcome
All patients in this study tolerated the surgical procedures. No significant complications related to BCP or LDBCP were observed.

Efficiency of leukocyte and neutrophil depletion
In the LDBCP group, leukocyte depletion was performed for every administration of BCP, the leukocyte and neutrophil depletion ratio remained at a relatively high level even after several administrations of cardioplegia solution (leukocyte depletion ratio: 1st, 97.5% ± 1.1%; 2nd, 96.3% ± 1.7%; 3rd, 94.5% ± 2.0%; 4th, 96.6% ± 2.4%; 5th, 94.0% ± 2.6%; 6th, 93.2% ± 3.0%; 7th, 89.7% ± 3.5%; neutrophil depletion ratio: 1st, 96.7% ± 1.3%; 2nd, 95.6% ± 1.9%; 3rd, 94.8% ± 2.3%; 4th, 92.6% ± 2.7%; 5th, 94.5% ± 2.5%; 6th, 93.4% ± 3.1%; 7th, 92.3% ± 3.2%; Fig 2).



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  		Fig 2. Change in the depletion ratios of leukocytes. The depletion ratio with the leukocyte removal filter remained at a relatively high level even after several administrations of cardioplegia (CP solution).

 
Myocardial protective effect
The coronary sinus effluent blood to arterial blood difference in MDA concentrations just after myocardial reperfusion in the LDBCP group was significantly lower than that in the BCP group. The LDBCP group showed significantly lower concentrations of HH-FABP and maximum creatine kinase-MB than did the BCP group. The maximum dose of catecholamine was significantly smaller in the LDBCP group (Fig 3; Table 4).



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  		Fig 3. Comparison of myocardial protective effects between the blood cardioplegia solution (BCP) and the leukocyte-depleted blood cardioplegia solution (LDBCP) groups. (CS-Ao MDA = difference in plasma concentration of malondialdehyde between coronary sinus effluent blood and arterial blood; HH-FABP = human heart fatty acid-binding protein in the plasma obtained 50 minutes after reperfusion; max CK-MB = the peak concentration of plasma creatine kinase-MB during the first 24 hours postoperatively; catecholamine = the maximum dose of catecholamine, dopamine plus dobutamine, required at the time of weaning from cardiopulmonary bypass and during the postoperative course.)

 

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  		Table 4. Comparison of Malondialdehyde, Human Heart Fatty Acid-Binding Protein, Creatine Kinase-MB, and Catecholamine Between Cardioplegia Solution Groups

 
Scanning electron microscopy
Scanning electron microscopy revealed a large number of blood cells in the fibers of the used leukocyte removal filter. These cells were regarded as white blood cells, judging from their size and shape; this removal filter successfully removed circulating leukocytes from the cardioplegia solution (Fig 4).



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  		Fig 4. Representative electron micrographs of the fibers of the leukocyte removal filter. A large number of blood cells, which were regarded as white blood cells, were captured on the fibers of the leukocyte removal filter. (A, x500; B, x1,500; C, x5,000.)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
We evaluated the myocardial protective effect of LDBCP for open heart operation. In the LDBCP group, the coronary sinus effluent blood to arterial blood difference in MDA concentrations just after reperfusion, the HH-FABP concentration obtained at 50 minutes after aortic unclamping, the peak value of creatine kinase-MB for the first 24 hours postoperatively, and the maximum dose of catecholamine at the time of weaning from CPB and during the postoperative course were lower than corresponding values in the BCP group. A quantitative functional-morphologic evaluation was not performed in this study because of the study design, but such experimental and clinical evaluation would be of interest for future study.

It is still unclear whether BCP solution containing leukocytes and platelets has a cytotoxic effect on the myocardium during periods of ischemia. CPB-induced blood activation [18] may enhance capillary plugging and release cytotoxic chemical mediators before cardioplegic cardiac arrest and during aortic cross-clamping. Nakanishi and coworkers [19] demonstrated that 45 minutes of normothermic ischemia plus intermittent BCP without reperfusion resulted in no significant coronary endothelial dysfunction related to nitric oxide in adult mongrel dogs. Schmidt and associates [20] reported a protective effect on endothelial function by leukocyte depletion in both extracorporeal circuits and cardioplegia circuits using continuous BCP under moderate hypothermia in a canine model of regional myocardial ischemia and reperfusion. However, the possible cytotoxicity of BCP as a risk for myocardial reperfusion injury has not been clearly demonstrated, even under conditions of cold BCP administered to hypothermic myocardium during cardioplegic arrest. Our results suggest the superiority of LDBCP for myocardial protection during open heart operation with respect to MDA, HH-FABP, maximum creatine kinase-MB, and catecholamine dosage, even though the study group comprised infants, in whom the myocardial scavenging systems for CPB-induced chemotactic mediators are immature in comparison with adult myocardium [2, 21, 22].

Although we have demonstrated the clinical myocardial protective effect of LDBCP, two disadvantages of the LDBCP system prevent us from using it unquestioningly. In pediatric open heart surgical procedures, the dose of BCP is smaller than that in adult operations, and it seems possible to frequently repeat the leukocyte depletion. In cases requiring many administrations of BCP, however, repeated LDBCP administration lessens the ability of the filter to deplete the leukocytes; it is affected by the total BCP administered. Because the mechanism of possible cytotoxicity of BCP remains unclear, we are not willing to make the best use of LDBCP in such cases, and our first choice is to use leukocyte-depleted terminal cardioplegia solution, which we use in adult open heart operations [12, 13]. Another disadvantage is the priming volume required for the LDBCP system. The leukocyte removal filter requires as much as 205 mL for priming, and this amount is large in comparison to the total volume used for priming the pediatric CPB circuit. The increased priming volume for CPB circuits enhances hemodilution and may prevent cardiac operations without blood components, especially in pediatric patients. Even though frequent leukocyte depletion can be used in pediatric open heart operations, we have to use conventional BCP administration without leukocyte depletion in cases in which perioperative blood transfusion should be avoided. Our hope is that an improved system will be developed that will allow for frequent leukocyte depletion along with a smaller priming volume.

In summary, initial and intermittent administrations of LDBCP seem superior to administrations of BCP without leukocyte depletion in terms of myocardial protection for ischemia-reperfusion injury. Although the cytologic mechanism of CPB-induced leukocyte activation during cardioplegic arrest remains unclear, the LDBCP modification may provide a cytoprotective effect as an adjunct to BCP.


   Acknowledgments
 
We thank the Pall Filter Company for kindly providing BC-1, the newly developed leukocyte removal filter.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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Accepted for publication December 23, 1999.




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