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Eur J Cardiothorac Surg 1998;14:596-601
© 1998 Elsevier Science NL

Intermittent antegrade hyperkalaemic warm blood cardioplegia supplemented with magnesium prevents myocardial substrate derangement in patients undergoing coronary artery bypass surgery

M. Caputoa, A.J. Bryana, A.M. Calafioreb, M.-S. Suleimana, G.D. Angelinia

a Bristol Heart Institute, University Of Bristol, Bristol Royal Infirmary, Bristol BS2 8HW, UK
b Department of Cardiac Surgery, Ospedale San Camillo de Lellis, Chieti, Italy

Received 18 May 1998; received in revised form 14 September 1998; accepted 29 September 1998.

Corresponding author. Tel.: +44-117-928-3145; fax: +44-117-929-9737.


   Abstract
Top
 Abstract
Introduction
Methods
Results
 Discussion
References
 
Objective: The influence of the addition of magnesium on myocardial protection with intermittent antegrade warm blood hyperkalaemic cardioplegia in patients undergoing coronary artery surgery was investigated and compared with intermittent antegrade warm blood hyperkalaemic cardioplegia only. Methods: Twenty-three patients undergoing primary elective coronary revascularization were randomized to one of two different techniques of myocardial protection. In the first group, myocardial protection was induced using intermittent antegrade warm blood hyperkalaemic cardioplegia. In the second group, the same technique was used except that magnesium was added to the cardioplegia. Intracellular substrates (ATP, lactate and amino acids) were measured in left ventricular biopsies collected 5 min after institution of cardiopulmonary bypass, after 30 min of ischaemic arrest and 20 min after reperfusion. Results: There were no significant changes in the intracellular concentration of ATP or free amino acid pool in biopsies taken at the end of the period of myocardial ischaemia. However, the addition of magnesium prevented the significant increase in the intracellular concentration of lactate seen with intermittent antegrade warm blood hyperkalaemic cardioplegia. Upon reperfusion there was a significant fall in ATP and amino acid concentration when the technique of intermittent antegrade warm blood hyperkalaemic cardioplegia was used but not when magnesium was added to the cardioplegia. Conclusions: This work shows that intermittent antegrade warm blood hyperkalaemic cardioplegia supplemented with magnesium prevents substrate derangement early after reperfusion.

Key Words: Intermittent antegrade warm blood hyperkalaemic cardioplegia • Magnesium • Coronary surgery • Amino acids • ATP • Lactate


   Introduction
Top
 Abstract
 Introduction
Methods
Results
 Discussion
References
 
Intermittent antegrade warm blood hyperkalaemic cardioplegia (IAWBC) has been recently proposed [1] [2] [3] as an improved method of myocardial protection when compared to intermittent antegrade cold blood cardioplegia during open heart surgery. The reduction in mortality and morbidity associated with the use of IAWBC was attributed to the prevention of myocardial oxidative stress [1] [2].

IAWBC utilizes potassium as the only additive. This arrests the heart by partially depolarizing the cardiac myocyte membrane but at the same time may facilitate opening of the L-type calcium-channels [4]. The direct result of this is calcium loading and therefore potential cellular damage [5] [6]. Magnesium is known to block the L-type calcium-channels and therefore prevent the rise in intracellular calcium during ischaemia [4] [7] [8] and is therefore likely to reduce energy demands and preserve intracellular metabolites. There are therefore strong theoretical reasons to support the addition of magnesium to this cardioprotective strategy.

To investigate whether the addition of magnesium to IAWBC improves myocardial protection, the intracellular concentrations of ATP, amino acids and lactate were monitored in left ventricular biopsies taken from patients undergoing routine coronary artery bypass surgery.


   Methods
Top
 Abstract
 Introduction
Methods
Results
 Discussion
References
 
Twenty-three patients (19 males, mean age±SD: 59.7±9.6 years) with a left ventricular ejection fraction greater than 50%, undergoing primary elective coronary artery bypass surgery were randomized to one of two techniques of myocardial protection: (i) intermittent antegrade warm blood hyperkalaemic cardioplegia (IAWBC) or (ii) intermittent antegrade warm blood hyperkalaemic cardioplegia supplemented with magnesium sulphate (IAWBC+Mg). The study was approved by the hospital ethics committee and patients informed consent obtained.

Anaesthetic technique was standardized for all patients. Thiopentone (1–3 mg/kg) was used for induction with 3–5 mg/kg fentanyl, and volatile agents were delivered in 50% air–O2 mixture for maintenance. Propofol (3 mg/kg per h) was given as an infusion during cardiopulmonary bypass and neuromuscular blockade was achieved by 0.1–0.15 mg/kg pancuronium bromide. Alpha stat acid–base management was adopted. Initial anticoagulation was accomplished with 3 mg/kg body weight of heparin and was supplemented as required in order to maintain an active clotting time of 480 s or above. All operations were performed using cardiopulmonary bypass with ascending aortic cannulation and two-stage venous cannulation. Target systemic temperatures were between 34° and 37°C.

The cardioplegic solution was delivered and prepared as described by Calafiore et al. [1] [2]. Blood was taken directly from the oxygenator via a 1/4-inch tubing and was infused at 34–37°C into the aortic root by means of a roller pump. A syringe pump containing 50 ml KCl (2 mmol/ml) (IAWBC) or KCl+MgSO4 (40 ml of 2 mmol/ml KCl+10 ml of 2 mmol/ml MgSO4) (IAWBC+Mg) was connected to the 1/4-inch tubing to deliver the cardioplegic solution. Following induction of ischaemic arrest with dose 1, subsequent dosages (2, 3 etc.) were administered on completion of each distal coronary anastomosis (Table 1). All the distal coronary anastomoses were completed during a single period of aortic cross-clamping. Proximal anastomosis were completed on a beating heart using an aortic partial occlusion clamp.


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  		Table 1. Delivery protocol of warm intermittent antegrade blood cardioplegia

 
Collection of ventricular biopsies
Three myocardial biopsy specimens (4–14 mg wet wt.) were taken from the apex of the left ventricle using a 14 gauge TWX 11.4 cm Cannula `Trucut' needle (Baxter Healthcare, Deerfield, IL). The first biopsy was taken 5 min after institution of cardiopulmonary bypass. The second biopsy was taken after 30 min of ischaemic time, and the third after 20 min of reperfusion. Each specimen was immediately frozen (in the operating theatre) in liquid nitrogen until processing for amino acid, ATP and lactate analysis. All biochemical analyses were performed by an investigator blind to the technique used.

Amino acids, ATP and lactate
The procedure followed to extract free amino acids, ATP and lactate was similar to that described previously [9]. In brief, frozen biopsy specimens were crushed under liquid nitrogen and the resultant powder (taken as wet wt.) was extracted with perchloric acid. The extracts were centrifuged at 1500xg for 10 min at 4°C. The supernatant was neutralized and the ATP content measured using a bioluminescent assay [10]. Lactate was measured using a serum lactate determination kit from Sigma Diagnostics (Sigma, Poole, UK). As the kit was designed for measuring a much higher concentration of lactate compared to the biopsy specimen, only percentage change in lactate is shown in the results section (all samples were paired).

Amino acids in the extracts from both groups were determined according to the Waters Pico–Tag method as reported previously [9]. Essentially, 100 µl of the extract was dried using vacuum centrifugation (Savant SV160, Farmingdale NY). Free amino acids were derivatized using phenylisothiocyanate. The phenylisothiocarbamyl derivatized amino acids were separated by HPLC using a 30 cm Pico–Tag column (Millipore, Milford, MA) with two Waters delivery pumps (A and B) at a constant flow of 1 ml/min with the following gradient: 100% A for 13.5min, 97% A for 10.5 min, 94% A for 6 min, 91% A for 20 min, 66% A for 12.5 min and 0% A for 4 min. The solvents used were for A: 132 mM sodium acetate, 470 ml/l triethylamine (pH 6.4), and 6% acetonitrile. Solvent B was 60% acetonitrile. Derivatized amino acids were detected at 254 nm (46°C) using a Waters 486 detector. Quantitative and qualitative analysis was carried out using amino acid standards (Sigma, Dorset, UK) and the acquired data was processed using the Millennium 2000 software supplied by Waters Millipore (Watford, UK). Chemicals needed to derivatize amino acids and separate them were obtained from Waters Millipore (Watford, UK).

Data collection and analysis
Values are expressed as mean±standard error of mean (SEM) unless otherwise stated. Statistical analysis was carried out using repeated measures ANOVA and Bonferroni multiple comparisons test (intragroup analysis) and Mann–Whitney test (intergroup analysis) using InStat and statview packages provided on a Macintosh PC. The correlation matrix was calculated and the significance determined using Fisher's r to z. The level of statistical significance was taken as 5%.


   Results
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 Abstract
 Introduction
Methods
Results
Discussion
References
 
Clinical outcome
There were no deaths in the series. The clinical information is presented in Table 2. The two groups were similar with respect to sex, age, preoperative ventricular function, extent of coronary disease, ischaemic and cardiopulmonary bypass time, ITU and hospital stay.


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  		Table 2. Patient characteristics

 
Changes in cellular metabolites during ischaemia and reperfusion
Following ischaemic arrest using either IAWBC or IAWBC+Mg, there was a modest decline in the intracellular concentration of ATP (12% and 16% respectively) ( Fig. 1 ). After 20 min reperfusion the ATP levels decreased markedly and significantly in the IAWBC group but not in the IAWBC+Mg group (48% and 20%, respectively, Fig. 1).



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  		Fig. 1. Tissue ATP levels measured in ventricular biopsies taken from patients undergoing coronary artery bypass surgery using IAWBC (n=11) or IAWBC+Mg (n=12). Biopsy 1 was collected 5 min after institution of cardiopulmonary bypass (ob), biopsy 2 after 30 min ischaemic arrest (cb) and biopsy 3 after 20 min of reperfusion (hb). P-values using repeated measures ANOVA (Bonferroni multiple comparison) test are also shown. A comparison between IAWBC and IAWBC+Mg (Mann–Whitney test) showed no significant difference between ATP levels in control, ischaemia or reperfusion biopsies.

 
In contrast to the changes in ATP, there was a rise in tissue lactate levels after ischaemic arrest when using IAWBC or IAWBC+Mg. However this was statistically significant for the IAWBC group only. On reperfusion there was a trend for lactate to decrease but remained relatively higher in the IAWBC group ( Fig. 2 ).



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  		Fig. 2. Percentage change in tissue lactate levels measured in ventricular biopsies taken from patients undergoing coronary artery bypass surgery using IAWBC (n=11) or IAWBC+Mg (n=12). Biopsy 1 was collected 5 min after institution of cardiopulmonary bypass (ob), biopsy 2 after 30 min of ischaemic arrest (cb) and biopsy 3 after 20 min of reperfusion (hb). P-values using repeated measures ANOVA (Bonferroni multiple comparison) test are also shown.

 
Following the period of ischaemia prior to reperfusion, there was no change in the intracellular concentration of the total free intracellular amino acid pool compared to the control biopsy: 36.1±2.2 to 35.0±1.9 µmol/g wet weight, respectively, for the IAWBC group and 34.2±1.8 to 34.8±1.9 µmol/g wet weight, respectively, for the IAWBC+Mg group ( Fig. 3 ). The intracellular free amino acid pool is largely made up of the principal free amino acids, glutamine, glutamate, taurine, aspartate, alanine and asparagine, which constitute more than 90% of the pool. Although there was no overall change in the amino acid pool, individual variations were observed (Table 3Table 4). A significant increase in the intracellular concentration of alanine was seen in both groups. In the IAWBC group, the increase in alanine was associated with a significant fall in glutamate. A small non-significant fall in glutamate was also seen in the IAWBC+Mg group.



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  		Fig. 3. Intracellular concentration of the amino acids pool measured in ventricular biopsies taken from patients undergoing coronary artery bypass surgery using IAWBC (n=11) or IAWBC+Mg (n=12). Biopsy 1 was collected 5 min after institution of cardiopulmonary bypass (ob), biopsy 2 after 30 min ischaemic arrest (cb) and biopsy 3 after 20 min of reperfusion (hb). P-values using repeated measures ANOVA (Bonferroni multiple comparison) test are also shown. A comparison between IAWBC and IAWBC+Mg (Mann–Whitney test) showed a significant difference (P<0.05) only between reperfusion biopsies.

 

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  		Table 3. Changes in the intracellular concentrations of amino acids (mmol/g wet wt.) in ventricular biopsies collected from patients undergoing coronary artery bypass surgery using IAWBC in the absence of magnesium (n=11). The P-values using repeated measures analysis of variance (Bonferroni multiple comparisons test) are shown

 

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  		Table 4. Changes in the intracellular concentrations of amino acids (µmol/g wet wt.) in ventricular biopsies collected from patients undergoing coronary artery bypass surgery using IAWBC in the presence of magnesium (n=12). The P-values using repeated measures analysis of variance (Bonferroni multiple comparisons test) are shown

 
In contrast to ischaemic arrest, after 20 min reperfusion, there was a marked and significant fall in the intracellular concentration of the amino acids pool in the IAWBC group ( Fig. 3). This was due to a fall in glutamine, glutamate, taurine, aspartate and asparagine (Table 3). When IAWBC+Mg was used there was no significant change in the intracellular free amino acids pool ( Fig. 3). The increase in the intracellular concentration of alanine seen after ischaemia in both groups was significantly reversed after 20 min reperfusion.

Tissue alanine/glutamate ratio has been used as a marker of ischaemic stress and during anaerobic metabolism, there is a fall in tissue glutamate with a corresponding rise in alanine [9] [11] [12] [13]. Fig. 4 shows that a significant increase in the alanine/glutamate ratio occurred as a result of ischaemic arrest using IAWBC or IAWBC+Mg, although the increase was lower in the later. On reperfusion the increase in the alanine/glutamate ratio was maintained in the IAWBC group but tended to fall in the IAWBC+Mg group ( Fig. 4). If this ratio is indeed a true measure of metabolic stress, then the alanine/glutamate ratios should correlate with ATP or lactate levels. This indeed was the case as there was a negative correlation between ATP and the alanine/glutamate ratio (P<0.005, Fisher's r to z), but the correlation was positive between lactate and alanine/glutamate ratio (P<0.05).



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  		Fig. 4. Alanine/glutamate ratio calculated for biopsies taken from patients undergoing coronary artery bypass surgery using IAWBC (n=11) or IAWBC+Mg (n=12). Biopsy 1 was collected 5 min after institution of cardiopulmonary bypass (ob), biopsy 2 after ischaemic arrest (cb) and biopsy 3 after 20 min of reperfusion (hb). The ratio was first calculated for individual patients and then the mean±SEM was used in the figure. P-values using repeated measures ANOVA (Bonferroni multiple comparison) test are also shown.

 
A comparison between the two groups (unpaired analysis using Mann–Whitney test) did not show any differences in the concentration of metabolites in the first biopsy (control). After 30 min of ischaemia the concentration of aspartate was significantly lower (P<0.05) in the IAWBC group. On reperfusion the concentration of aspartate, glutamate, asparagine, glutamine and amino acid pool was significantly lower in the IAWBC group compared to the IAWBC+Mg group.


   Discussion
Top
 Abstract
 Introduction
Methods
Results
 Discussion
References
 
In this work we documented the changes in the intracellular concentrations of ATP, intracellular amino acid pool and lactate in the ischaemic-reperfused myocardium of patients undergoing coronary artery surgery using the technique of IAWBC, with or without the addition of magnesium.

The finding that normothermic arrest using IAWBC was associated with a modest fall in tissue ATP and in the total free intracellular amino acid pool ( Fig. 1), supports an early suggestion that this technique is associated with mild ischaemia [1] [2]. However, during this period there was a significant rise in tissue lactate which is consistent with anaerobic metabolism. This is further supported by the fall in the amino acid glutamate, known to be utilized for energy production by the ischaemic myocardium [11] [12] [14]. Evidence for glutamate utilization for energy production is provided by the finding that alanine accumulated, resulting in an increase in alanine/glutamate ratio ( Fig. 4). The addition of magnesium prevented a significant rise in lactate. However, alanine rose significantly resulting in an increase in the alanine/glutamate ratio. These observations suggest that the inclusion of magnesium in the cardioplegic solution results in relatively lower anaerobic metabolic activity during ischaemic arrest.

The relatively minor changes seen during ischaemia were markedly accentuated after 20 min of reperfusion with a significant fall in ATP and the free intracellular amino acid pool seen only in the IAWBC group. Amino acids are important for normal cellular function [9] [15] and can be utilized for energy production and therefore help the heart during ischaemia/reperfusion. A preservation in these amino acids, as seen in the IAWBC+Mg group, may facilitate recovery following cardiac surgery. Consistent with improved myocardial preservation in IAWBC+Mg group is the finding that ATP and individual amino acids (with the exception of glutamate) were significantly preserved.

A comparison between the two groups further supports the suggestion that the inclusion of magnesium in the IAWBC prevents substrates derangement. With the exception of ATP and taurine, the rest of the substrates were significantly higher in the IAWBC+Mg group after reperfusion.

The data suggest that IAWBC+Mg prevents metabolic derangement on reperfusion. The cardioprotective effect of magnesium is likely to be due to effects on calcium transport. Ataka et al. [4] have found that hyperkalaemic cardioplegia without magnesium does not prevent the rise in intracellular calcium during ischaemia. Hyperkalaemic cardioplegic solutions partially depolarize the membrane and may open the L-type calcium-channels. Elevated intracellular calcium levels will activate a variety of cellular enzymes and transport systems as well as influencing mitochondrial function [5] [6] [16]. This will lead to increased cellular energy demands, some of which can be met by using amino acids like glutamate (which can also be produced from glutamine) and aspartate [4] [9] [15]. Magnesium, by reducing calcium loading during ischaemia and reperfusion [4] [7] [8], will also reduce energy demands and preserve intracellular metabolites.

From the data presented above, it would seem that the addition of magnesium to the protocol of IAWBC is justified, since it preserves intracellular metabolites and reduces metabolic stress in hearts of patients undergoing coronary surgery. Further work is needed to establish whether these changes are translated into better clinical outcome.


   Acknowledgments
 
This work was supported by the British Heart Foundation and the Garfield Weston Trust. We would like to acknowledge Anne Moffatt for her excellent technical assistance and the clinical staff in Cardiac Surgery for their assistance.


   References
Top
 Abstract
 Introduction
Methods
Results
 Discussion
References
 

  1. Calafiore A.M., Teodori G., Mezzetti A., Bosco G., Verna A.M., DiGiammarco G., Lapenna D. Intermittent antegrade warm blood cardioplegia. Ann Thorac Surg 1995;59:398-402.[Abstract/Free Full Text]
  2. Mezzetti A., Calafiore A.M., Lapenna D., Deslauries R., Tian G., Salerno T.A., Verna A.M., Bosco G., Pierdomenico S.D., Caccurullo F. Intermittent antegrade warm blood cardioplegia reduces oxidative stress and improves metabolism in the ischemic-reperfused human myocardium. J Thorac Cardiovasc Surg 1995;109:787-795.[Abstract/Free Full Text]
  3. Menasché P. Blood cardioplegia: do we still need to dilute?. Ann Thorac Surg 1996;62:957-960.[Free Full Text]
  4. Ataka K., Chen D., McCully J., Levitsky S., Feinberg H. Magnesium cardioplegia prevents accumulation of cytosolic calcium in the ischemic myocardium. J Mol Cell Cardiol 1993;25:1387-1390.[Medline]
  5. Tani M. Mechanisms of Ca2+ overload in reperfused ischemic myocardium. Annu Rev Physiol 1990;52:543-559.[Medline]
  6. Jennings R.B., Reimer K.A. The cell biology of acute myocardial ischemia. Annu Rev Med 1991;42:225-246.[Medline]
  7. Dichtl A., Vierling W. Inhibition by magnesium of calcium inward current in heart ventricular muscle. Eur J Pharmacol 1991;204:243-248.[Medline]
  8. Trosper T.L., Philipson K.D. Effects of divalent and trivalent cations on Na-Ca exchange in cardiac sarcolemmal vesicles. Biochim Biophys Acta 1983;731:63-68.[Medline]
  9. Suleiman M.-S., Dihmis W.C., Caputo M., Angelini G.D., Bryan A.J. Changes in myocardial concentration of glutamate and aspartate during coronary artery surgery. Am J Physiol 1997;272:H1063-H1069.[Abstract/Free Full Text]
  10. Spielman H., Jacob-Miller V., Schulz P. Simple assay of 0.1–1.0 pmol of ATP, ADP and AMP in single somatic cells using purified luciferin lucifrase. Anal Biochem 1981;113:172-176.[Medline]
  11. de Villalobos D.H., Taegtmeyer H. Metabolic support for postischaemic heart. Lancet 1995;345:1552-1555.[Medline]
  12. Mudge G.H., Mills R.M., Taegtmeyer T., Gorlin R., Lesch M. Alterations of myocardial amino acid metabolism in chronic ischemic disease. J Clin Invest 1976;58:1185-1192.[Medline]
  13. Conger K.A., Garcia J.H., Lossinsky A.S., Kauffman F.C. Effect of aldehyde fixation on selected substrates for energy metabolism and amino acids in mouse brain. Histochem Cytochem 1978;26:423-433.[Abstract]
  14. Rosenkranz E.R. Substrate enhancement of cardioplegic solution: experimental studies and clinical evaluation. Ann Thorac Surg 1995;60:797-800.[Abstract/Free Full Text]
  15. Suleiman M.-S., Moffatt A., Dihmis W.C., Caputo M., Angelini G.D., Hutter J.A., Bryan A.J. Effect of ischaemia and reperfusion on the intracellular concentration of taurine and glutamine in the hearts of patients undergoing coronary artery surgery. Biochim Biophys Acta 1997;1324:223-231.[Medline]
  16. Minezaki K.K., Suleiman M.-S., Chapman R.A. Changes in mitochondrial-function induced in isolated guinea-pig ventricular myocytes by calcium overload. J Physiol (Lond) 1994;476:459-471.[Abstract/Free Full Text]



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