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Eur J Cardiothorac Surg 2007;31:659-664. doi:10.1016/j.ejcts.2007.01.014
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Washing of irradiated red blood cells prevents hyperkalaemia during cardiopulmonary bypass in neonates and infants undergoing surgery for complex congenital heart disease

Christine G. Swindell*, Thomas A. Barker, Simon P. McGuirk, Timothy J. Jones, David J. Barron, William J. Brawn, Angela Horsburgh, Robert G. Willetts

Birmingham Children's Hospital, Birmingham, United Kingdom

Received 14 July 2006; received in revised form 19 November 2006; accepted 6 January 2007.

* Corresponding author. Address: Department of Cardiac Perfusion, Birmingham Children's Hospital, Steelhouse Lane, Birmingham, West Midlands B4 6NH, United Kingdom. Tel.: +44 121 3339999; fax: +44 121 3339561. (Email: chris.swindell{at}fsmail.net).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: High concentrations of potassium and lactate in irradiated red cells transfused during cardiopulmonary bypass may have detrimental effects on infants and neonates undergoing cardiac surgery. The effects of receiving washed and unwashed irradiated red cells from the cardiopulmonary circuit on serum potassium and lactate concentrations were compared. Methods: The study population included neonates and infants undergoing heart surgery for complex congenital heart disease. A control group (n = 11) received unwashed irradiated red cells and the study group (n = 11) received irradiated red cells washed in a cell saver (Dideco Electa) using 900 ml of 0.9% saline prior to pump priming. Potassium and lactate concentrations were compared before, during and after bypass. Results: Washing irradiated red cells reduced donor blood [potassium] from > 20 to 0.8 ± 0.1 mmol/l, and [lactate] from 13.7 ± 0.5 to 5.0 ± 0.3 mmol/l (p < 0.001). The resulting prime had significantly lower [potassium] and [lactate] than the unwashed group (potassium 2.6 ± 0.1 vs 8.1 ± 0.4 mmol/l, p < 0.001; lactate 2.6 ± 0.2 vs 4.6 ± 0.3 mmol/l, p < 0.001). Peak [potassium] in the unwashed group occurred 3 minutes after going on bypass (4.9 ± 0.3 mmol/l) and during rewarming (4.9 ± 0.4 mmol/l). These were significantly higher than the washed group (3.1 ± 0.1, p < 0.001 and 3.0 ± 0.1 mmol/l, p < 0.001). The [potassium] was greater than 6.0 mmol/l for 4 out of these 11 unwashed patients compared with none of the washed group. Immediately post-bypass the washed group had significantly lower serum [potassium] (3.2 ± 0.1 vs 4.2 ± 0.2 mmol/l, p = 0.002). There was no significant difference in [lactate] between groups during and after cardiopulmonary bypass. Conclusions: The washing of irradiated red cells reduces potassium and lactate loads and prevents hyperkalaemia during cardiopulmonary bypass. The washing of irradiated red cells should be considered in neonates and infants undergoing cardiac surgery for complex congenital heart disease.

Key Words: Paediatric cardiac surgery • Cardiopulmonary bypass


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Paediatric cardiopulmonary bypass (CPB) involves a high ratio of prime volume to patient blood volume. The transfusion of a clear fluid prime from the circuit would cause haemodilution and induce severe anaemia especially in infants and neonates. Therefore it is considered necessary to add concentrated red cells to the CPB circuit prime to maintain haemoglobin levels and the oxygen carrying capacity of the child's circulatory system.

A number of neonates and infants with complex congenital heart disease have cell-mediated immunodeficiency. This can be associated with conditions such as Di George Syndrome whose symptoms include hypoplasia of the thymus gland and T-cell immunodeficiency. Those patients at risk are prescribed irradiated red cells (IRC) for CPB. The irradiation process inactivates any viable T-lymphocytes in the donor blood preventing the development of transfusion-associated graft versus host disease (TA-GvHD) in the recipient. Irradiation is an important precaution as there is no effective treatment for TA-GvHD and more than 90% of patients developing the condition die [1]. In addition to T-lymphocytes, donor stem cells may also play a role in TA-GvHD.

Transfusion of non-irradiated red cells during CPB does not result in systemic hyperkalaemia [2]. However, when blood is irradiated the red cell membranes are weakened allowing K+ to leach into the extracellular space increasing plasma K+ concentration compared to non-irradiated cells [3]. In addition, by the time the red cells are irradiated they may have been stored for up to 2 weeks allowing lactate levels to increase due to anaerobic energy metabolism in the erythrocytes [4]. Several studies have reported extremely high levels of K+ along with increased lactate concentrations in units of IRC [1,3,5,6]. This has the potential to lead to complications during and after transfusion.

Transfusion of IRC that contain high levels of K+ and lactate increases the potential for serious adverse effects, especially if it takes place over a short time period. Establishment of CPB produces a rapid blood transfusion which can increase [K+] by an average of 3.1 mmol/l in neonates [7]. Deaths have been reported in neonates from arrhythmias and cardiac arrest almost immediately following transfusion of red cells containing high potassium concentrations [8,9]. Consequently the immediate effects of rapid transfusion of hyperkalaemic red cells appear to pose a significant risk to the patient.

Hyperlactaemia is strongly correlated with postoperative morbidity and mortality for patients undergoing complex open-heart surgery, especially children and infants [10,11]. The lactate is a marker of poor tissue perfusion and low cardiac output and can lead to metabolic acidosis. Additional lactate load in the circulation may further influence acid-base status and pre-load the lactate metabolism.

Pre-washing the donor IRC in a cell saver with saline is a method of reducing K+ and lactate concentrations. A number of studies have used similar devices for the removal of K+ and saline washing has been shown to produce an effective K+ reduction in all cases [1,12,13]. Modern cell saver devices such as the Dideco Electa (Sorin Group, Italy) used in this study have been designed to minimise haemolysis. Previous research has found no evidence of significant red blood cell haemolysis, a condition associated with hyperkalaemia, in cell washed blood or in the systemic blood after transfusion of washed red cells [12].

This study aimed to identify whether cell saver washing of IRC prior to transfusion reduced K+ and lactate levels in the donor blood. Furthermore, we aimed to identify whether transfusion of washed cells prevented hyperkalaemia and hyperlactaemia in the serum of neonates and infants undergoing open-heart surgery.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 Appendix A
 References
 
This study was approved by the Research and Development Department at Birmingham Children's Hospital and the North Birmingham Local Research Ethics Committee. Written consent was obtained from parents of all participants in the study. A prospective randomised control study was carried out on 22 infants and neonates undergoing CPB for complex congenital heart surgery between January 2005 and May 2006. Infants were identified as babies under 1-year-old.

All patients included in the study received IRC as they had, or were suspected to have had, a syndrome associated with immunodeficiency as stated in the transfusion guidelines for our institution. If there was any doubt about immunocompetence based on clinical or laboratory features, IRC were used until an immunodeficiency had been excluded. The donor blood was gamma irradiated using a dose of 25 Gy within 14 days of donation. Patients received the IRC within 14 days of irradiation. The storage solution used for the donor red cell in this study was citrate-phosphate-dextrose-adenine-1 (CPDA-1).

The characteristics of patients included in this study are shown in Table 1 . Group A (control group, n = 11) received 1 unit of unwashed IRC in the CPB circuit prime. Group B (experimental group, n = 11) received the processed volume from 2 units of IRC pre-washed in a cell saver before addition to the CPB circuit prime. Group B received 2 units to compensate for the volume loss during processing. Therefore, group A received a second unit of unwashed irradiated red cells as required during CPB.


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  		Table 1 Patient characteristics
 
The priming solution for both groups consisted: Plasmalyte 148–30 ml/kg, 1 unit of fresh frozen plasma, heparin – 2500 units, methylprednisolone – 20 mg/kg, calcium chloride – 2.5 mmol (0.5 mmol/ml), sodium bicarbonate 8.4%–10 ml, mannitol – 0.5 g/kg, irradiated red cells (stored at 4 °C in citrate-phosphate-dextrose-adenine-1 [CPDA-1] solution) – washed or unwashed depending on patient group.

The Dideco Electa cell saver was used to wash the IRC for group B patients. The cell saver was operated in automatic mode with a 125 ml centrifuge bowl. During each wash cycle the red cells were washed with 900 ml of 0.9% sodium chloride solution at a speed of 400 ml/min.

The CPB machine used in the study was a Sarns 8000 nonpulsatile roller occlusive pump (Terumo, Belgium). The same CPB circuit set-up was used for all patients. This consisted of a closed system with a soft shell reservoir and a Hilite 1000 oxygenator (Medos, Germany), which is used for flows up to 1 l/min. Patients received cold crystalloid cardioplegia (St Thomas’ Solution with a K+ concentration of 20 mmol/l) administered by the anaesthetist at a dose of 30 ml/kg after cross clamping, which then passed through the pump. All patients received one dose of cardioplegia except for four patients undergoing cavo-pulmonary shunts that did not receive any.

The sampling protocol is shown in Fig. 1 . The CPB circuit samples were drawn from the arterial line within the circuit. Samples were taken for immediate analysis, using the alpha stat technique with the GEM Premier 3000 blood gas analyzer (Instrumentation Laboratory, UK). The primary outcomes of interest were K+ and lactate both in the IRC and in-patient samples. The analyser has a detection level of up to 20 mmol/l for K+ and 15 mmol/l for lactate concentrations. Consequently, readings above the upper limit were given as 20 and 15 mmol/l, respectively. Sodium (Na+) concentrations were also recorded as secondary outcomes. Normal physiological ranges of analytes in the samples were considered to be; K+: 3.2–4.6 mmol/l, lactate: < 2 mmol/l, Na+: 133–148 mmol/l.


Figure 1
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  		Fig. 1. Flow diagram showing the sampling protocol.

 
Statistical analysis was performed using SPSS for windows (version 12 SPSS Inc., Chicago, IL, USA). Power calculations were carried out based on the data reported by Keidan et al. [14]. This showed that a sample size of 11 in each group would give our study an 80% power. Results were expressed as a mean ± standard error of the mean (SEM). To make comparative analyses between the two experimental groups a t-test was used. A p-value ≤ 0.05 was considered statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Baseline
There were no differences in the initial IRC concentrations of K+, lactate and Na+ between groups A and B. All [K+] were above the upper limit on the GEM Premier 3000 blood gas analyser and were reported as 20 mmol/l. Also mean [lactate] and [Na+] in sample 1 (the pre-washed/pre-transfused sample) were not significantly different between groups: lactate (A) 14.6 ± 0.2 versus (B) 13.7 ± 0.5 mmol/l (p = 0.13), and [Na+] (A) 118.1 ± 4.4 versus (B) 126 ± 2.1 mmol/l (p = 0.13). There were no differences between the mean patient pre-bypass serum concentrations of the three analytes; [K+] (A) 4.0 ± 0.3 versus (B) 3.5 ± 0.2 mmol/l (p = 0.24); [lactate] (A) 1.3 ± 0.2 mmol/l versus (B) 1.5 ± 0.2 (p = 0.54); [Na+] A 133.3 ± 1.1 versus 135 ± 1.2 mmol/l (p = 0.31).

3.2 Effect of cell washing
Washing the IRC in the cell saver caused reductions in [K+]; Pre-washed > 20.0 versus washed 0.8 ± 0.5 mmol/l. [Lactate] were also reduced; Pre-washed 13.7 ± 1.7 versus washed 5.0 ± 1.0. In contrast washing increased [Na+]; Pre-washed 126 ± 7.0 versus washed 147.6 ± 1.4. The [Na+] for the washed group were, however, within normal limits for our institution (133–148 mmol/l) (Fig. 2 ).


Figure 2
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  		Fig. 2. Comparison of IRC [K+], [lactate] and [Na+] before and after cell washing.

 
CPB prime [K+] prior to bypass were significantly lower in group B primes (2.6 ± 0.1 mmol/l) compared to group A (8.1 ± 0.4 mmol/l), p < 0.001. In addition group B lactate concentrations (2.6 ± 0.2 mmol/l) were significantly lower than in group A (4.6 ± 0.3 mmol/l), p < 0.001. Prime [Na+] were significantly higher in group B (151.5 ± 1.0 mmol/l) compared to group A (147.5 ± 1.2 mmol/l), p = 0.02 (Fig. 3 ).


Figure 3
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  		Fig. 3. Comparison of potassium, lactate and sodium prime concentrations before CPB between groups A and B. *Significantly lower than group A. {dagger}Significantly higher than group A (p < 0.05).

 
3.3 Potassium concentrations during cardiopulmonary bypass
Potassium concentrations in group A were significantly higher than group B, throughout CPB, sampling points 5–8, p < 0.05 (Fig. 4 ). In the unwashed group A, peak [K+] occurred at both the start of bypass (sample 5) and during rewarming at 28 °C (sample 7), 4.9 ± 0.3 mmol/l and 4.9 ± 0.4 mmol/l, respectively. These were above the normal physiological range of 3.2–4.6 mmol/l. Group A [K+] then decreased to within the normal range immediately post-bypass (Sample 9: 4.2 ± 0.2, p = 0.003). In comparison, group B mean [K+] were below the normal range from the start of bypass until rewarming to 28 °C. The lowest [K+] being Sample 7 (3.0 ± 0.1 mmol/l) and the highest at Sample 8, 3.8 ± 0.3 mmol/l (Fig. 4).


Figure 4
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  		Fig. 4. Patient potassium concentrations throughout the study (Sample 4: patient pre-bypass; sample 5: CPB sample 3mins on bypass; sample 6: CPB sample 28 °C cooling; sample 7: CPB sample 28 °C rewarming; sample 8: CPB sample 36 °C rewarming; sample 9: sample from patient immediately post-bypass). *Significant difference between groups, p < 0.05.

 
The [K+] was greater than 6.0 mmol/l during CPB for 4 out of the 11 unwashed group A patients compared with none of the washed group B. Two of group A had ventricular fibrillation (VF) in the presence of hyperkalaemia ([K+] 6.1 and 6.4) within 5 min of institution of CPB compared to none of group B. The VF was successfully cardioverted with a single DC shock in one case and spontaneously resolved in the other. Immediately post-bypass the washed group had significantly lower serum [K+] than the unwashed group (3.2 ± 0.1 vs 4.2 ± 0.2, p = 0.003). Post-bypass values were, however, within normal ranges for both groups. In addition, there was no difference in [K+] in patients not receiving cardioplegia.

3.4 Lactate concentrations during cardiopulmonary bypass
Group A [lactate] were not significantly higher than group B during bypass apart from at sample 7 (28 °C rewarming), (A) 6.3 ± 0.5 mmol/l and (B) 4.9 ± 0.3 mmol/l, p = 0.03. This coincided with a further transfusion of unwashed blood for 5 of 11 group A patients. Throughout CPB the [lactate] for both groups were increased. This hyperlactaemia was exaggerated following the arrest period, during rewarming. Peak [lactate] occurred in group A at sample 9 (post-bypass), 6.9 ± 0.8 mmol/l and in group B at sample 8 (36 °C rewarming), 5.1 ± 0.5 mmol/l (Fig. 5 ).


Figure 5
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  		Fig. 5. Patient lactate concentrations throughout the study. *Significant difference between groups, p < 0.05.

 
3.5 Sodium concentrations during cardiopulmonary bypass
There was no significant difference in [Na+] between groups during CPB apart from at sample 8 (36 °C rewarming), A) 138.9 ± 0.8 mmol/l and B) 142 ± 1.1 mmol/l p = 0.03. Immediately after bypass (Sample 9), group B [Na+] were also significantly higher (145.5 ± 1.3 mmol/l) than group A (141.5 ± 0.6 mmol/l), p = 0.008, but both values remained within the normal physiological range during and post-bypass (Fig. 6 ).


Figure 6
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  		Fig. 6. Patient sodium concentrations throughout the study. {dagger}Significant difference between groups, p < 0.05.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
Appendix A
 References
 
We found that cell saver washing consistently reduced [K+] and [lactate] in donor units of IRC. This led to the prime solution having lower [K+] and [lactate] resulting in reduced levels throughout CPB. In contrast to the [K+] and [lactate], [Na+] were significantly higher in washed blood although levels were within the normal physiological range. We showed that cell saver washing of IRC produces a more physiological prime and prevents hyperkalaemia during CPB in neonates and infants undergoing cardiac surgery for complex congenital heart disease.

All the donor IRC units used in this study had [K+] above 20 mmol/l, which was considerably higher than previously reported concentrations of 9.2–15 mmol/l [14]. This difference may be a result of differing IRC processing protocols between hospitals. Cell saver removal rates for [K+] found in the literature of 97.3% [13] are comparable with our study. The higher [K+] observed at our institution further supports the investigation of the benefits of cell saver washing in order to reduce the potential effects of IRC transfusions.

In patients who received unwashed blood, [K+] were highest, and above the normal range, at the start of CPB and again during rewarming. This was likely due to the high K+ load in the prime for the first peak. The second peak coincided with a further unwashed IRC transfusion occurring in nearly half the patients during rewarming, again generating a high K+ load.

Potassium concentrations above 5 mmol/l have previously been shown to cause distinct changes in the electrocardiogram indicating hyperkalaemia; and cardiac arrhythmias have been associated with concentrations over 7.5 mmol/l [8]. Of note in our study is that 4 of the 11 patients receiving unwashed IRC had a [K+] above 6.0 mmol/l. Of these, two sustained ventricular fibrillation associated with the hyperkalaemia at the start of CPB ([K+] > 6.0 mmol/l). Due to numbers in the study this did not reach statistical significance and further investigation would be required to confirm whether cell saver washing does reduce the incidence of arrhythmias.

Following CPB the [K+] returned to within the normal range in the unwashed group indicating that K+ was able to redistribute back into the intracellular space after rapid transfusion had ceased. Washing IRC resulted in more patients becoming hypokalaemic with four requiring K+ supplementation during rewarming compared with none in the unwashed group. Despite this, [K+] was within the normal range immediately post CPB. Red cell washing has previously been shown to produce hypokalaemia in previously normokalaemic infants and this was associated with cardiac dysrhythmias [15]. There were no visible ECG changes consistent with hypokalaemia during or after CPB in our study patients receiving washed IRC. We conclude that this iatrogenic reduction of [K+] by IRC washing is not detrimental and is easier to manage than the hyperkalaemia seen in patients receiving unwashed IRC.

Previously cell saver washing has been shown to lower [lactate] by 54% [16]. Despite washed IRC having a 64% reduction in our study this did not reduce hyperlactaemia during CPB. All patients experienced an increase in [lactate] as CPB progressed which was exaggerated by the DCHA causing increased production of lactate from anaerobic glycolysis. The only significant difference in [lactate] between groups was observed during rewarming (at 28 °C). As with the second peak of [K+] during CPB, this can be explained by the further transfusion of unwashed IRC at this point. The effect on [lactate] by transfusing unwashed IRC is therefore not as exaggerated as its effect on [K+] as it took the transfusion of two unwashed units to demonstrate a difference compared with just for one unit for [K+]. We therefore think that the potential benefits of cell saver washing are due to its ability to reduce patients K+ rather than lactate levels.

Sodium concentrations, a secondary outcome of this study, were found to be significantly increased in IRC by cell saver washing which has previously been reported [16]. This resulted in the prime solutions, and patient samples throughout CPB also containing higher [Na+]. This was due to the wash solution consisting of 0.9% sodium chloride. We feel that this does not have any detrimental effects as serum [Na+] during and after CPB were, in general, within the normal physiological range (133–148 mmol/l).

Despite the benefits of red cell washing, this process may have the potential to further damage IRC which could shorten their survival time after transfusion. Although this was not the main focus of our study, we would recommend using the correct volume of wash solution combined with low pump processing speeds in the cell saver. This should improve the quality of the wash and minimise further haemolysis during processing. Further investigation into IRC haemolysis during washing and red cell survival time post transfusion would be useful in order to discover any adverse effects.

In conclusion, cell saver washing of IRC helps to prevent hyperkalaemia during CPB but does not prevent hyperlactaemia in neonates and infants undergoing cardiac surgery for complex congenital heart disease. Therefore the washing of IRC should be considered for these patients. Further studies are required to confirm whether IRC washing reduces arrhythmia rates. In addition, investigation into the longer term sequelae of the benefits of this technique would also be helpful.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
References
 
Conference discussion

Dr M. Danton (Glasgow, United Kingdom): Was there any tendency to increased hemolysis in the patients that had washed red cells?

Dr Swindell: We didn’t look into hemolysis due to the fact that once the cells are washed, they actually pass through the bypass pump anyway. However the Dideco Electa is designed to minimize hemolysis. Also in the literature, previous studies have shown that there was no significant increase in hemolysis from cell-saver washing.

Dr S. Sano (Okayama, Japan): This technique has been used for many years in Japan. We call this a preoperative ultrafiltration. The reason of this technique is not only to control all the potassium or other electrolyte in normal level but also to decrease cytokines preoperatively. This technique prevents initial pressure drop soon after the cardiopulmonary bypass. My question is that did you check cytokine level and hemodynamic parameters pre-, peri- and post-CPB in this study?

Dr Swindell: No we didn’t measure any other parameters because this study was specifically focusing on potassium and lactate and whether we could reduce those. It would be a good idea to look into that in the future.

Dr Sano: I think this technique is very much useful, especially in the neonate, to prevent the perioperative shock and postoperative management.

Dr R. Jonas (Washington, D.C., USA): Can you help me to understand just how important it is to irradiate blood. I have to admit that I have sometimes been lax in asking for irradiation in settings, for example, where the thymus is not present. And yet I don’t personally recall a single letter from a cardiologist saying ‘I’m sorry, but your patient has developed some graft-versus-host neoplastic problem’.

We are working in an era where most of us use white cell free blood, so please help me to understand, is irradiation something that I should be doing more aggressively and what problem will I be preventing?

Dr Swindell: I think there is some controversy over it. Our blood is ordered on the ward, so as perfusionists we don’t really have anything to do with ordering irradiated blood. But it is prescribed in our institution for those with DiGeorge syndrome or those that haven’t had their chromosome tests back yet, the neonates in particular, and those with an absent thymus.

But there may be a lack of communication, because sometimes we receive irradiated red cells from the blood bank when the patient has aortic arch anomalies but then we find that the patient has got a thymus gland. So I think really some of the blood doesn’t actually need to be irradiated when it is and I think we need to address that issue as well within our institution. I don’t know the protocol at other institutions, but I think that is part of the problem.


   Footnotes
 
\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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B. Ji and J. Liu
Is there any difference in lactate level between washed and unwashed donor blood during pediatric cardiopulmonary bypass?
Eur. J. Cardiothorac. Surg., August 1, 2007; 32(2): 401 - 402.
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