JTCS Email Content Delivery
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Hikaru Matsuda
Yasuhisa Shimazaki
Susumu Nakano
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sawa, Y.
Right arrow Articles by Nakano, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sawa, Y.
Right arrow Articles by Nakano, S.

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

Yoshiki Sawa, MD, Hikaru Matsuda, MD, Yasuhisa Shimazaki, MD, Mitsunori Kaneko, MD, Motonobu Nishimura, MD, Akira Amemiya, MD, Kei Sakai, MD, Susumu Nakano, MD


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, Go Go 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. Go Go 3-5 The fate of cardiac tissue subjected to temporary ischemia is determined partly by the method of reperfusion, Go Go 6,7 which can be controlled by modification or intervention of reperfusate. Go 7 As an alternative to the controlled reperfusion methods, terminal cardioplegia has been used widely in the clinical situation. Go Go 7-9 However, it still has limitations for severely injured myocardium, Go 10 and further modification of terminal cardioplegia may be required, especially for patients with critically compromised hearts. Go Go Go 3,7,10

Recently, some experimental studies have shown that activated neutrophils cause some aspects of reperfusion injury and the "no-reflow" phenomenon Go Go 11-13; reperfusion with leukocyte-depleted blood has been introduced as a method to prevent such reperfusion injury. Go Go 14-16 However, few attempts have been made to apply this technique clinically during cardiac operations. Go Go 17-19 If this leukocyte-depleted reperfusion is combined with terminal blood cardioplegic solution, the myocardial protective effect may be enhanced. Go 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. Go 20 Recently, lymphocytopheresis was applied in the treatment of the patients with rheumatic arthritis by means of the development of the leukocyte removal filter. Go 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 (GoTable 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 (GoTable II).


View this table:
[in this window]
[in a new window]
  		Table I. Comparison of the basic data among WB, TC, and LDTC groups in patients with elective CABG
 

View this table:
[in this window]
[in a new window]
  		Table II. Comparison of the basic data among WB, TC, and LDTC groups in patients with emergency CABG
 
Myocardial protection.
The basic method of myocardial protection used was with cold potassium crystalloid cardioplegic solution (K+, 18 mEq/L; glucose, 55 gm/L; pH, 7.8; osmolarity; 380 mOsm/ml; temperature, 4° C). Go 5 The initial dose of cardioplegic solution was 10 ml/kg of body weight, and a half dose was reinfused every 30 minutes. Myocardial temperature was monitored at the ventricular septum and maintained below 15° C with topical cooling. Only the patients in the LDTC group received 10 minutes of LDTC before the cessation of aortic crossclamping.

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) Go 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. Go 21 The blood is passed through the polyester fiber at a flow rate of 300 ml/min for 10 minutes (GoTable 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 (GoTable 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.

 

View this table:
[in this window]
[in a new window]
  		Table III. Specifications of leukocyte removal filter (Cellsorba-80P)
 

View this table:
[in this window]
[in a new window]
  		Table IV. Method of leukocyte-depleted terminal cardioplegic solution
 
Measurements.
Leukocyte count and its differential count for neutrophils were obtained from the aortic root at three times: before and during controlled reperfusion and immediately after cardiopulmonary bypass.

Malondialdehyde content in the coronary sinus effluent blood and arterial blood was measured at 30 minutes of reperfusion by high-pressure liquid chromatography Go 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.

 
In emergency CABG cases (Fig. 4), the peak CK-MB level was significantly lower in the LDTC group (27 ± 11 IU/L) than in the TC (56 ± 13 IU/L) and WB (74 ± 18 IU/L, p < 0.05) groups.



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.

 
Regarding the comparison between elective and emergency cases, the LDTC group showed no significant difference between elective and emergency procedures, whereas the TC and WB groups showed significantly higher values of CK-MB in emergency cases than those in elective cases (p < 0.05).

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.

 
DISCUSSION

Although remarkable advances in myocardial protection in cardiac surgery exist, difficulties in preventing myocardial injuries resulting in postoperative low cardiac output still remain. Go Go 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. Go Go Go 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. Go 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), Go 7 has been introduced to attenuate ischemic myocardial damage with cardioplegic arrest with acceleration of myocardial metabolic recovery and preservation of high energy phosphate. Go Go 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. Go 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. Go Go 13-16 It has been reported that removal of neutrophils at the time of reperfusion improved functional recovery. Go Go Go 14,15,25 Conversely, other studies have shown that neutrophil content in stunned myocardium is not increased Go 26 and that interventions to remove neutrophils have not improved function. Go Go 27,28 It seems reasonable that the role of neutrophils in reperfusion injury may depend on the degree of myocardial damage Go 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. Go 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 Go Go 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. Go 30 Conversely, incomplete depletion of leukocytes provided no other attenuation in the clinical outcome. Go 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. Go Go 6,7 In this period, major morphologic changes of subcellular levels are detected Go 6 and neutrophils start to adhere to endothelial cells on which adhesion molecules have already been expressed. Go 31 Intracellular neutrophil hydrogen peroxide begins to increase as early as 15 minutes. Go 32 Breda and associates Go 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

  1. Flameng W, Van der Vusse GJ, De Meyere R, et al. Intermittent aortic cross-clamping versus St. Thomas' Hospital cardioplegia in extensive aorta-coronary bypass grafting. J THORAC CARDIOVASC SURG 1984;88:164-73.[Abstract]
  2. Conti RV, Bertranou EG, Blackstone EH, Kirklin JW, Digerness SB. Cold cardioplegia versus hypothermia for myocardial protection. J THORAC CARDIOVASC SURG 1978;76:577-89.[Abstract]
  3. Wechsler AS. Deficiencies of cardioplegia: the hypertrophied ventricle. In: Engelman RM, Levitsky S, eds. A textbook of clinical cardioplegia. New York: Futura, 1982:381-90.
  4. Mundth ED, Goel IP, Morgan RJ. Effect of potassium cardioplegia and hypothermia on left ventricular function in hypertrophied and non-hypertrophied heart. Surg Forum 1975;7:550.
  5. Matsuda H, Maeda S, Hirose H, et al. Optimum dose of cold potassium cardioplegia for patients with chronic aortic valve disease: determination by left ventricular mass. Ann Thorac Surg 1986;41:22-6.[Abstract]
  6. Schaper J, Schaper W. Reperfusion of ischemic myocardium: ultrastructural and histochemical aspects. J Am Coll Cardiol 1983;1:1037-46.[Abstract]
  7. Buckberg GD. Studies of controlled reperfusion after ischemia. I. When is cardiac muscle damaged irreversibly? J THORAC CARDIOVASC SURG 1986;92:483-7.
  8. Follete DM, Fey K, Buckberg GD, et al. Reducing post-ischemic damage by temporary modification of reperfusate calcium potassium pH and osmolarity. J THORAC CARDIOVASC SURG 1981;82:221-38.[Abstract]
  9. Teoh KH, Christakis GT, Weisel RD, et al. Accelerated myocardial metabolic recovery with terminal warm blood cardioplegia. J THORAC CARDIOVASC SURG 1986;91:888-95.[Abstract]
  10. Lazar HL, Buckberg GD, Manganaro AM, Becker H. Myocardial energy replenishment and reversal of ischemic damage by substrate enhancement of secondary blood cardioplegia with amino acids during reperfusion. J THORAC CARDIOVASC SURG 1980;80:350-9.[Medline]
  11. Engler RL, Schmid-Schoenbein GW, Pavelec RS. Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog. Am J Pathol 1983;111:98-111.[Abstract]
  12. Forman MB, Puett DW, Virmani R. Endothelial and myocardial injury during ischemia and reperfusion: pathogenesis and therapeutic implications. J Am Coll Cardiol 1989;11:1309-16.
  13. Sawa Y, Nakano S, Shimazaki Y, Nishimura M, Kuratani T, Matsuda H. Myocardial protective effect and its mechanism of leukocyte depleted reperfusion in neonatal rabbit hearts. Ann Thorac Surg (In press).
  14. Engler RL, Dahlgren MD, Peterson MA, Dobbs A, SchmidSchoenbein GW. Accumulation of polymorphonuclear leukocytes during 3-h experimental myocardial ischemia. Am J Physiol 1986;251:H93-100.[Abstract/Free Full Text]
  15. O'Neill PG, Charlat ML, Michael LH, Roberts R, Bolli R. Influence of neutrophil depletion on myocardial function and flow after reversible ischemia. Am J Physiol 1989;256:H341-51.[Abstract/Free Full Text]
  16. Breda MA, Drinkwater DC, Laks H, et al. Prevention of reperfusion injury in the neonatal heart with leukocyte depleted blood. J THORAC CARDIOVASC SURG 1989;97:654-65.[Abstract]
  17. Pearl EM, Drinkwater DC, Laks H, Stein DG, Capouya ER, Bhuta S. Leukocyte-depleted reperfusion of transplanted human hearts prevents ultrastructural evidence of reperfusion injury. J Surg Res 1992;52:298-308.[Medline]
  18. Pearl JM, Drinkwater DC, Laks H, Capouya ER, Gates RN. Leukocyte depleted reperfusion of transplanted human hearts: a randomized, double-blind clinical trial. J Heart Lung Transplant 1992;11:1082-92.[Medline]
  19. Paianzo DA, Manley NJ, Montesano RM, Yeisley GL, Gordon D. Clinical evaluation of the LeukoGuard (LG-6) arterial line filter for routine open heart surgery. Perfusion 1993;8:489-96.
  20. Sirchia G, Rebulla P, Parravicini A, Carnelli V, Gianotti GA, Bertolini F. Leukocyte depletion of red blood cell units at the bedside by transfusion through a new filter. Transfusion 1987;27:402-5.[Medline]
  21. Kondoh T, Hidaka Y, Katho H, Inoue N, Saito S. Evaluation of a filtration lymphocytapheresis device for use in the treatment of patients with rheumatoid arthritis. Artif Organs 1991;15:180-1.[Medline]
  22. Bull AW, Marnett LJ. Determination of malondialdehyde by ion-pairing high-performance liquid chromatography. Analyt Biochem 1985;149:284-90.
  23. Rosenkrantz ER, Vinten-Johansen J, Buckberg GD, Okamoto F, Edwards H, Bugyi H. Benefits of normothermic induction of blood cardioplegia in energy depleted hearts with maintenance of arrest by multidose cold blood cardioplegic infusions. J THORAC CARDIOVASC SURG 1982;84:667-77.[Abstract]
  24. Roberts AJ, Woodhall DD, Knauf DG, Alexander JA. Coronary artery bypass graft surgery: clinical comparison of cold blood potassium cardioplegia, warm cardioplegic induction, and secondary cardioplegia. Ann Thorac Surg 1985;40:483-7.[Abstract]
  25. Engler RL, Covell JW. Granulocytes cause reperfusion ventricular dysfunction after 15-minutes ischemia in the dog. Circ Res 1987;61:20-8.[Abstract/Free Full Text]
  26. Go Lo, Murry CE, Richard VJ, Weischedel GR, Jennings RB, Reimer KA. Myocardial neutrophil accumulation during reperfusion after reversible and irreversible ischemic injury. Am J Physiol 1988;255:H1188-98.[Abstract/Free Full Text]
  27. Jeremy RW, Becker LC. Neutrophil depletion does not prevent myocardial dysfunction after brief coronary occlusion. J Am Coll Cardiol 1989;13:1155-63.[Abstract]
  28. Carlson RE, Schott RJ, Buda AJ. Neutrophil depletion fails to modify myocardial no reflow and functional recovery after coronary reperfusion. J Am Coll Cardiol; 14:1803-13.
  29. Reimer KA, Murry CE, Richard VJ. The role of neutrophils and free radicals in the ischemic reperfused heart: Why the confusion and controversy. J Mol Cell Cardiol; 21:1225-39.
  30. Bando K, Pillai R, Cameron DE, et al. Leukocyte depletion ameliorates free radical mediated lung injury after cardiopulmonary bypass. J THORAC CARDIOVASC SURG 1990;99:873-7.[Abstract]
  31. Entman ML, Michael LH, Rossen RD, et al. Inflammation in the course of early myocardial ischemia. FASEB J 1991;5:2529-37.[Abstract]
  32. Ko W, Hawes AS, Lazenby WD, et al. Myocardial reperfusion injury: platelet-activating factor stimulates polymorphonuclear leukocyte hydrogen peroxide production during myocardial reperfusion. J THORAC CARDIOVASC SURG 1991;102:297-308.[Abstract]




This Article
Right arrow Abstract Freely available
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Hikaru Matsuda
Yasuhisa Shimazaki
Susumu Nakano
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sawa, Y.
Right arrow Articles by Nakano, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sawa, Y.
Right arrow Articles by Nakano, S.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS