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J Thorac Cardiovasc Surg 1994;108:1125-1131
© 1994 Mosby, Inc.

CARDIOPULMONARY BYPASS, MYOCARDIAL MANAGEMENT, AND SUPPORT TECHNIQUES

Evaluation of leukocyte-depleted terminal blood cardioplegic solution in patients undergoing elective and emergency coronary artery bypass grafting

Osaka, Japan

From the First Department of Surgery, Osaka University Medical School, Osaka, Japan.

Received for publication Dec. 17, 1993. Accepted for publication May 31, 1994. Address for reprints: Hikaru Matsuda, MD, Professor, First Department of Surgery, Osaka University Medical School, 2-2, Yamada-oka, Suita, Osaka 565, Japan.

Abstract

Leukocyte depletion at reperfusion may have a role in myocardial protection when combined with terminal cardioplegia. We applied this method in a selected group of 68 patients with coronary artery bypass grafting either for elective surgical procedures (n= 38) or emergency surgical procedures with the use of a preoperative intraaortic balloon pump (n= 30) because of developing acute myocardial infarction. Basic cold potassium crystalloid cardioplegic solution was used. During delivery of leukocyte-depleted terminal cardioplegic solution, warm arterial blood delivered from cardiopulmonary bypass was passed through a leukocyte removal filter, mixed with potassium crystalloid cardioplegic solution, and administered to the aortic root for the first 10 minutes of reperfusion. Patients were randomized into three groups for reperfusion: whole blood, terminal cardioplegic solution, and leukocyte-depleted terminal cardioplegic solution reperfusion groups. In elective coronary artery bypass grafting, no significant difference was found in the clinical data. However, in emergency coronary artery bypass grafting, the leukocyte-depleted terminal cardioplegic solution group (n= 10) showed significantly lower peak creatine kinase MB levels (leukocyte-depleted terminal cardioplegic solution versus terminal cardioplegic solution versus whole blood: 27 ± 11, 56 ± 13, 74 ± 18, respectively; p< 0.05) and maximum dopamine doses required at the weaning of cardiopulmonary bypass (6.3 ± 1.1 versus 11.2 ± 3.3 versus 9.2 ± 2.2; p< 0.05) than did the terminal cardioplegic solution (n= 10) and whole blood groups (n= 10). Moreover, the leukocyte-depleted terminal cardioplegic solution group showed significantly lower difference of malondialdehyde between arterial and coronary sinus blood (0.15 ± 0.09 versus 0.36 ± 0.06 versus 0.66 ± 0.12 nmol/ml, p< 0.05) than did the terminal cardioplegic solution or whole blood groups. These results showed that leukocyte-depleted terminal blood cardioplegic solution may have a role in attenuating reperfusion injury in patients with critical conditions such as preoperative myocardial ischemic injury. (J THORACCARDIOVASCSURG1994;108:1125-31)

In spite of the great advances in myocardial protection during cardiac operations, ^1,2 myocardial injury associated with aortic crossclamping or reperfusion has been one of the major concerns in patients with emergency cases or various indications of compromised hearts, such as severe left ventricular hypertrophy or preoperative ischemic injury. ^3-5 The fate of cardiac tissue subjected to temporary ischemia is determined partly by the method of reperfusion, ^6,7 which can be controlled by modification or intervention of reperfusate. ⁷ As an alternative to the controlled reperfusion methods, terminal cardioplegia has been used widely in the clinical situation. ^7-9 However, it still has limitations for severely injured myocardium, ¹⁰ and further modification of terminal cardioplegia may be required, especially for patients with critically compromised hearts. ^3,7,10

Recently, some experimental studies have shown that activated neutrophils cause some aspects of reperfusion injury and the "no-reflow" phenomenon ^11-13; reperfusion with leukocyte-depleted blood has been introduced as a method to prevent such reperfusion injury. ^14-16 However, few attempts have been made to apply this technique clinically during cardiac operations. ^17-19 If this leukocyte-depleted reperfusion is combined with terminal blood cardioplegic solution, the myocardial protective effect may be enhanced. ¹⁶

Polyester fiber filters have been used during blood transfusion to reduce the leukocytes from stored blood as a preventive measure against side effects because the fine diameter of polyester fiber has a high affinity with the leukocytes. ²⁰ Recently, lymphocytopheresis was applied in the treatment of the patients with rheumatic arthritis by means of the development of the leukocyte removal filter. ²¹ In this randomized clinical study, this newly developed leukocyte removal filter for coronary perfusion with heparinized blood was used, and reperfusion with leukocyte-depleted blood combined with terminal cardioplegic solution was applied to test its efficacy in patients with coronary artery bypass grafting (CABG) for either elective or emergency operations.

PATIENTS AND METHODS

Study groups.
Sixty-eight patients who underwent elective (n = 38) and emergency (n = 30) CABG procedures at Osaka University Hospital during 1991 to 1993 were enrolled in this study. The age at operation ranged from 30 to 78 years (56 ± 16 years, mean ± standard deviation). All patients were revascularized completely. All patients gave their informed consent. Patients were randomized to receive either whole blood (WB), terminal cardioplegic solution (TC) or leukocyte-depleted terminal cardioplegic solution (LDTC) reperfusion. The patients and surgeons were blinded as to which type of reperfusion was used. In patients with elective CABG, 15 patients were in the WB group, 10 were in the TC group, and 13 were in the LDTC group. These three groups showed no significant difference in age, number of grafts, preoperative cardiac index, or aortic crossclamp time (Table I). In the emergency CABG group, all patients were in cardiogenic shock of various degree as a result of left ventricular pump failure caused by developing acute myocardial infarction. These patients showed significantly lower preoperative cardiac index (2.2 ± 0.5 L/min per square meter) than did patients with elective CABG (3.4 ± 0.4, p < 0.05) and were dependent on preoperative intraaortic balloon counterpulsation. They were randomly divided into the WB (n = 10), TC (n = 10), and LDTC (n = 10) groups. Also, no significant difference was found in age, preoperative cardiac index, aortic crossclamp time, or number of grafts among three groups (Table II).

Method of controlled reperfusion.
After the completion of proximal anastomoses during clamping of the aorta, arterial blood for TC and LDTC were separately circulated from the oxygenator reservoir (Fig. 1). In the cases with LDTC only, a newly developed leukocyte removal filter (Cellsorba-80P; Asahi Medical, Tokyo, Japan) ²¹ for coronary perfusion with heparinized blood (Fig. 2) was incorporated just after the oxygenator reservoir to deplete leukocytes. This filter consists of nonwoven fine polyester fiber wound around a porous cylinder. ²¹ The blood is passed through the polyester fiber at a flow rate of 300 ml/min for 10 minutes (Table III). Then, leukocyte-depleted blood was mixed with cold potassium crystalloid cardioplegic solution by double-head coupled roller pumps (Shiley, Inc., Irvine, Calif.); it was infused into the root of the aorta through a cardioplegic cannula at a flow rate of 1 ml/min per gram of left ventricular mass at no more than 200 ml/min with a perfusion pressure of no higher than 60 mm Hg for 10 minutes. It was started to infuse at 30° C and was heated up immediately to 36° C. The hematocrit valve was maintained at approximately 15% to 20% (17% ± 4%), and the level of potassium was maintained from 8 to 10 mEq/L (Table IV). At the end of TC and LDTC reperfusion, the aorta was unclamped, and the heart was reperfused with oxygenated whole blood through the aortic cannula.

View larger version (21K): [in this window] [in a new window]   Fig. 1. Scheme of LDTC. GIK, Glucose-insulin-potassium.

View larger version (151K): [in this window] [in a new window]   Fig. 2. A newly developed leukocyte removal filter (Cellsorba-80P; Asahi Medical, Tokyo, Japan) for coronary perfusion with heparinized blood. A, Arterial side; V, venous side.

Malondialdehyde content in the coronary sinus effluent blood and arterial blood was measured at 30 minutes of reperfusion by high-pressure liquid chromatography ²² and expressed in nanomoles per milliliter. The differences of malondialdehyde between coronary sinus effluent and arterial blood were compared among the three groups.

Serum creatine kinase (CK-MB) value was measured every 6 hours and compared with its peak level during the first postoperative 24 hours.

The maximum dose of dopamine required at the weaning of cardiopulmonary bypass (expressed in micrograms per kilogram per minute) to maintain the arterial pressure more than 80 mm Hg was compared; no other drugs, including catecholamines and vasodilators, were used during these periods.

Statistical analysis.
Results were expressed as mean ± standard deviation. The Newman-Keul test for multiple comparison was used to compare the data. A p value of less than 0.05 was considered statistically significant.

RESULTS

Clinical results.
With regard to operative death and survival, all patients tolerated the surgical procedures and survived without significant complications related to TC or LDTC.

Leukocyte count.
Before controlled reperfusion, no significant differences were found in the number of leukocytes (counts per cubic millimeter) or differential counts for neutrophils (%) among the WB (7900 ± 800 counts/mm ³,66% ± 13%), TC (8200 ± 700, 63% ± 16%), and LDTC groups (7600 ± 800, 67% ± 23%) with elective and emergency CABG. However, during controlled reperfusion, the LDTC group showed significantly lower numbers of leukocytes and differential count for neutrophils in the aortic root (200 ± 100, 10% ± 5%) than were shown in the TC (6600 ± 600, 68% ± 19%) and WB (8200 ± 1100, 67% ± 12%, p < 0.01) groups. No significant difference was found in the number of leukocytes and differential counts for neutrophils immediately after cardiopulmonary bypass among the WB (8800 ± 900, 68% ± 13%), LDTC (7800 ± 1600, 65% ± 18%), and TC (8200 ± 900, 62% ± 16%) groups.

CK-MB.
In elective CABG cases (Fig. 3), no significant differences were found in peak value of CK-MB for 24 hours postoperative among the WB (38 ± 16 IU/L), TC (35 ± 18 IU/L), and LDTC (33 ± 19 IU/L) groups.

View larger version (35K): [in this window] [in a new window]   Fig. 3. Comparison of CK-MB and dopamine dose at the time of weaning from cardiopulmonary bypass among WB, TC, and LDTC cases in patients with elective CABG. N.S., Not significant.

View larger version (41K): [in this window] [in a new window]   Fig. 4. Comparison of CK-MB and dopamine dose at the time of weaning from cardiopulmonary bypass among WB, TC, and LDTC cases in patients with emergency CABG.

Maximum dopamine dose required at the weaning of cardiopulmonary bypass.
In elective CABG cases (Fig. 3), no significant difference was found in the maximum dopamine dose required at the weaning of cardiopulmonary bypass among the WB (5.8 ± 4.2 IU/L), TC (6.9 ± 5.1 IU/L) and LDTC (5.0 ± 4.1 IU/L) groups.

In emergency CABG cases (Fig. 4), the LDTC group (6.1 ± 0.9 IU/L) showed significantly lower doses of dopamine required at the weaning of cardiopulmonary bypass than did the WB (10.0 ± 3.0 IU/L) and TC (7.9 ± 3.2 IU/L, p < 0.05) groups.

Malondialdehyde level in coronary sinus blood.
The LDTC group (0.1 ± 0.08 nmol/ml, p < 0.05) showed a significantly lower coronary sinus–arterial difference of malondialdehyde than did the TC (0.32 ± 0.05) nmol/ ml) and WB (0.57 ± 0.11 nmol/ml groups) (Fig. 5).

View larger version (36K): [in this window] [in a new window]   Fig. 5. Comparison of coronary sinus-arterial blood difference of malondialdehyde among WB, TC, and LDTC groups.

Although remarkable advances in myocardial protection in cardiac surgery exist, difficulties in preventing myocardial injuries resulting in postoperative low cardiac output still remain. ^1,2 Such situations include valvular operations for patients with severely hypertrophied left ventricle from aortic or mitral regurgitation, as well as coronary revascularization for patients with preoperative acute myocardial infarction. In this clinical study, as one of the strategies for improving cardioplegic protection, LDTC with a new leukocyte removal filter developed for the coronary circulation with heparinized blood was applied to test its efficacy compared with whole blood simple reperfusion, as well as TC. These results showed that LDTC provided decreased myocardial damage with regard to oxygen free radical productions and CK-MB release and our routine use of dopamine to wean patients from bypass compared with WB and TC in a selected group of patients with emergency CABG. Namely, this technique was significant when used in patients with developing acute myocardial infarction requiring intraaortic balloon pumping.

Regarding the indication used for emergency cases in this study, we have chosen the patients with acute myocardial infarction supported with intraaortic balloon pumping. In such situations, additional myocardial ischemia and reperfusion at the time of operation may increase the risk of the development of extension of myocardial injuries and hemorrhagic infarction in severe cases. ^1,2,7 Patients who need an emergency operation with cardiogenic shock may be characterized biochemically as having depleted myocardial energy stores, which decreases tolerance to aortic crossclamping even under cardioplegic arrest. ²³ In spite of the significantly lower preoperative index, LDTC reperfusion attenuated CK-MB leakage in emergency cases to the same degree as in elective cases, whereas WB and even TC reperfusion failed to attenuate these cytosol enzyme leakages. This finding means that LDTC prevents the sarcolemmal damage caused mainly by free radicals from neutrophils in the compromised hearts.

TC, particularly with warm blood (hot shot), ⁷ has been introduced to attenuate ischemic myocardial damage with cardioplegic arrest with acceleration of myocardial metabolic recovery and preservation of high energy phosphate. ^8,9 Although, this technique has been widely applied in clinical situations, the efficacy of TC alone is not well determined, particularly in a standard elective operation. ²⁴ In this study, TC contributed less to attenuation of myocardial injury, as well as in compromised hearts. This finding may suggest that TC alone has little difference in its myocardial protective effect compared with conventional uncontrolled reperfusion in noncompromised hearts. However, the combination of TC and leukocyte depletion improved the efficacy of TC reperfusion, which may suggest the different contribution of both TC and LDTC methods in attenuation of reperfusion injury.

Leukocyte-depleted reperfusion has been introduced in cardiac catheterization laboratory and cardiac operations as a strategy to attenuate the reperfusion injury in the hearts damaged by ischemia. ^13-16 It has been reported that removal of neutrophils at the time of reperfusion improved functional recovery. ^14,15,25 Conversely, other studies have shown that neutrophil content in stunned myocardium is not increased ²⁶ and that interventions to remove neutrophils have not improved function. ^27,28 It seems reasonable that the role of neutrophils in reperfusion injury may depend on the degree of myocardial damage ²⁹ and that leukocyte depletion alone may have a limiting effect in vulnerable myocardium to attenuate reperfusion injury. In this study, we combined leukocyte depletion and terminal cardioplegia: leukocyte depletion augmented the myocardial protective effect of TC in the emergency cases of CABG with intraaortic balloon pumping, whereas leukocyte depletion had no significant augmentation of the effect of TC in the elective cases of CABG. This result is consistent with the suggestion that the specific contribution of neutrophils to mild or moderate myocardial damage seems less effective in contrast to the severely damaged myocardium. ²⁹

With respect to the clinical application of reperfusion with leukocyte-depleted blood, the direct insertion of the leukocyte removal filter into the circuit of the extracorporeal circulation ^19,30 is easy compared with our method. In that case, it remains to be determined whether completeness of leukocyte depletion in the systemic circulation would lead to clinical problems and whether the simultaneous depletion of platelets produced by filters might be concerned. ³⁰ Conversely, incomplete depletion of leukocytes provided no other attenuation in the clinical outcome. ¹⁹ In our LDTC reperfusion system, TC was applied for selective perfusion with leukocyte-depleted blood only through the coronary circulation and only during the early phase of reperfusion. Consequently, neither serious infections nor serious bleeding occurred in the postoperative period in any patients of the LDTC group in spite of more than 95% depletion of leukocytes in the coronary circulation during reperfusion only.

In this study, LDTC was applied in the first 10 minutes of reperfusion. There are a few explanations for this choice: the first 10 minutes of reperfusion is the critical period for myocardial protection against reperfusion injury. ^6,7 In this period, major morphologic changes of subcellular levels are detected ⁶ and neutrophils start to adhere to endothelial cells on which adhesion molecules have already been expressed. ³¹ Intracellular neutrophil hydrogen peroxide begins to increase as early as 15 minutes. ³² Breda and associates ¹⁶ reported that a 10-minute period of leukocyte depletion appeared to be adequate to prevent reperfusion injury in an isolated heart. Further estimation of the propriety of the duration of LDTC reperfusion should be sought in experimental and clinical studies to obtain the optimal duration of LDTC reperfusion to attenuate the neutrophil-induced reperfusion injury.

In summary, LDTC reperfusion as an adjunct to TC was applied in patients with CABG. Leukocyte depletion augmented TC with attenuation of reperfusion injury in patients with critical conditions involving preoperative myocardial infarction; therefore, this modification may have a role as an adjunct to cardioplegia when conventional myocardial protection is not sufficient to prevent ischemia-reperfusion injury.

References

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