Continuous Warm Blood Cardioplegia Research Articles

Myocardial Protection Era: From Valve Surgery to Heart Transplantation

Myocardial Protection Era: From Valve Surgery to Heart Transplantation

Myocardial energy metabolism and functional recovery in coronary bypass surgery: A comparative study between continuous retrograde warm and mild hypothermic blood cardioplegia

The optimal temperature for delivery of continuous retrograde blood cardioplegia is not known. Twenty-two patients admitted to the hospital for elective coronary artery bypass grafting were randomized into the warm (37°) and mild hypothermic (28°C) cardioplegia groups. Changes in myocardial energy metabolism during cardiopulmonary bypass, postoperative efflux of the creatine kinase MB isoform (CK-MB), functional hemodynamic recovery, and postoperative complications were followed. During aortic cross-clamp, the average oxygen consumption was higher in the warm than in the mild hypothermic group (3.4±0.4 vs 2.4±0.3 ml/minute,p=0.06), as was the average transcardiac (outflow-inflow) pCO2-difference (1.1±0.1 vs 0.7±0.1 kPa,p=0.02). The average transcardiac pH-difference during aortic cross-clamp was lower in the warm group (−0.08±0.01 vs −0.06±0.01 U,p=0.02), reflecting more profound tissue acidosis. In accordance with this, warm hearts produced more lactate, especially towards the end of the aortic cross-clamp period (p=0.001). The net efflux of adenosine and its degradation products was more prominent during warm than during mild hypothermic cardioplegia (p=0.016), indicating less degradation of high energy adenylates in the hypothermic group. The functional hemodynamic recovery during the first postoperative day was similar in both patient groups, although the myocardial injury estimated as postoperative leakage of CK-MB was less extensive in the hypothermic group (p=0.011). There were no major differences in the postoperative complications between the study groups. We conclude that continuous retrograde mild hypothermic blood cardioplegia offers better myocardial protection during coronary bypass surgery than does continuous retrograde warm cardioplegia. The clinical significance of this should be tested in a larger series of patients, especially those with recent myocardial infarction, unstable angina, or severely depressed left ventricular function.

Continuous warm blood cardioplegia: A randomized prospective clinical comparison

Seventy-eight patients undergoing isolated coronary artery bypass grafting (CABG) were randomized to receive one of two myocardial preservation techniques. Control patients (C) (n=38) had myocardial protection by moderate systemic hypothermia, topical cold saline, and myocardial arrest with antegrade dilute blood/cold potassium cardioplegia with subsequent intermittent retrograde solution every 10–15 minutes during the period of aortic cross-clamping. The experimental group (warm blood, WB) (n=40) had myocardial protection at systemic normothermia, myocardial arrest with antegrade high potassium, and warm blood cardioplegia with subsequent continuous retrograde low potassium warm blood cardioplegia throughout aortic cross-clamping. The two groups were similar preoperatively. After aortic declamping, all WB patients developed a spontaneous rhythm. Only three (7.5%) required intraoperative defibrillation compared with 23 (61%) C patients,p<0.0001. The cross-clamp time per graft was greater with WB,p=0.003. The postoperative need for inotropes, cardiac pacing, incidence of ventricular dysrhythmia, chest tube drainage, and hospital stay did not differ between groups. Perioperative myocardial infarction occurred in 2 WB and 0 C patients (p=0.25). Mortality was not different between groups (WB=1, C=2,p=0.89). It is possible to perform CABG with continuous warm blood cardioplegia with low morbidity and mortality. However, no clear advantage was demonstrated over standard techniques that allow the technical ease of a bloodless field. The metabolic and physiologic significance of spontaneous resumption of sinus rhythm upon aortic declamping remains to be elucidated.

Cold Agglutinins in Cardiac Surgery: Management of Myocardial Protection and Cardiopulmonary Bypass

Cold agglutinins are of unique relevance in cardiac surgery because of the use of hypothermic cardiopulmonary bypass (CPB). Immunoglobulin M autoantibodies to red blood cells, which activate at varying levels of hypothermia, can cause catastrophic hemagglutination, microvascular thrombosis, or hemolysis. Management of CPB and myocardial protection requires individualized planning. We describe a case of aortic valve replacement in a patient with high titre cold agglutinins and a high thermal amplitude for antibody activation. Normothermic CPB and continuous warm blood cardioplegia were successfully used.

754. Different Regulation of Myocardial Atrial and Ventricular Calcium Pump Activity (Ca-ATP-ase) during Cardiac Arrest

Ca++-ATP-ase activity is a sensitive marker of myocardial metabolic integrity and ischemia. We hypothetized that changes occur in atria (A) and ventricle (V) Ca++ATP-ase mRNA expression of this gene during cardiac arrest protected by continuous warm blood cardioplegia (CWBCP).

Efficacy and safety of on-pump beating heart surgery for valvular disease

Background. This study was conducted to assess the efficacy and applicability of on-pump beating heart valvular operations using retrograde coronary sinus perfusion. Methods. A prospective, randomized study was conducted. A total of 50 patients participated in this study after having been allocated to one of two groups. On-pump beating heart valvular operations using retrograde coronary sinus perfusion as myocardial protection were performed in 25 patients (beating heart procedure group: aortic = 8 patients, mitral = 15 patients, double = 2 patients). Twenty-five patients underwent conventional valvular operation using retrograde continuous warm blood cardioplegia (conventional procedure group: aortic = 9 patients; mitral = 13 patients; double = 3 patients). The remaining operative variables and early outcomes of these procedures were compared. In the beating heart procedure group, myocardial tissue oxygen was measured by near infrared spectroscopy, and partial oxygen pressure of coronary sinus perfusion was also measured. Results. The visual field of the on-pump beating heart was equal to that of conventional valvular operation, and technical accuracy was not compromised. In the beating heart procedure group, tissue oxygen saturation was maintained at 79% ± 2%, and partial oxygen pressure of coronary sinus perfusion blood and returned blood were maintained at 383 ± 29 mm Hg and 38 ± 2 mm Hg, respectively. Postoperative peak creatine kinase-MB (measured every 3 hours postoperatively) and peak troponin T concentrations were significantly lower than those of conventional procedures (17.5 ± 7.8 vs 32.1 ± 9.3 IU/L and 0.12 ± 0.04 vs 0.21 ± 0.06 ng/mL, respectively; p < 0.05). There was no operative mortality and no major complications. Conclusions. On-pump beating heart valvular operation is a good surgical option, and has advantages because conditions for the heart are more physiologic with beating tonus than with cardioplegia.

Both Glucose-Insulin-Potassium and Glutamine in Warm Blood Cardioplegia Increase the Rates of Myocardial Glucose and Free Fatty Acid Oxidation

Objective -- We wanted to assess the effect of glucose-insulin-potassium (GIK) and glutamine on the oxidative metabolism during and after prolonged warm continuous blood cardioplegia (WB). Design -- WB was given to 21 pigs divided into three equally sized groups: WB (control), WB and GIK, or WB and glutamine. Oxidation rates of radiolabeled glucose ( 14 C) and free fatty acid (FFA) ( 3 H) were assessed before, during, and at 30 and 60 min after 3 h of cardiac arrest with WB. Results -- During standstill the substrate oxidation dropped markedly (<60%), glucose oxidation was highest in the WB + GIK group ( p < 0.05) and FFA oxidation highest in the WB + glutamine group (NS). During recovery the GIK group had an elevated glucose oxidation (47 and 40% vs WB at 30 and 60 min recovery, respectively - p < 0.05). Following 30 min recovery the addition of GIK suppressed FFA oxidation some 60%. Glutamine increased the oxidation of both glucose (30%) and FFA (150%) following 60 min recovery ( p < 0.05). During the whole recovery phase the relative FFA oxidation was significantly lowered in the GIK group. There were no differences between the groups regarding arterial levels or uptake of substrates, except for a higher myocardial oxygen consumption (MVO 2 ) during cardioplegia in the glutamine group. All the hearts performed similarly. Conclusion -- Addition of GIK or glutamine to the well-perfused and oxygenated heart during WB led to a postcardioplegic increase in oxidative metabolism and MVO 2 . GIK resulted in a significant metabolic shift from FFA to glucose.

Even a Root Canal Has its Advantages: Dental Syringe as a Mist Blower

In coronary artery surgery, especially during off-pump procedures and when continuous retrograde warm blood cardioplegia is used, a gentle but effective system is required to improve visualization without desiccating tissues. A simple, efficient, reusable, and very cost-effective device is described.

Cardioplegia and ischemia in the canine heart evaluated by 31P magnetic resonance spectroscopy

Background. Warm continuous blood cardioplegia provides excellent protection, but must be interrupted by ischemic intervals to aid visualization. We hypothesized that (1) as ischemia is prolonged, the reduced metabolic rate offered by cooling gives the advantage to hypothermic cardioplegia; and (2) prior cardioplegia mitigates the deleterious effects of normothermic ischemia. Methods. Isolated cross-perfused canine hearts underwent cardioplegic arrest followed by 45 minutes of global ischemia at 10°C or 37°C, or 45 minutes of normothermic ischemia without prior cardioplegia. Left ventricular function was measured at baseline and during 2 hours of recovery. Metabolism was continuously evaluated by phosphorus-31 magnetic resonance spectroscopy. Results. Adenosine triphosphate was 71% ± 4%, 71% ± 7%, and 38% ± 5% of baseline at 30 minutes, and 71% ± 4%, 48% ± 5%, and 39% ± 6% at 42 minutes of ischemia in the cold ischemia, warm ischemia, and normothermic ischemia without prior cardioplegia groups, respectively. Left ventricular systolic function, left ventricular relaxation, and high-energy phosphate levels recovered fully after cold cardioplegia and ischemia. Prior cardioplegia delayed the decline in intracellular pH during normothermic ischemia initially by 9 minutes, and better preserved left ventricular relaxation during recovery, but did not ameliorate the severe postischemic impairment of left ventricular systolic function, marked adenosine triphosphate depletion, and creatine phosphate increase. Left ventricular distensibility decreased in all groups. Conclusions. When cardioplegia is followed by prolonged ischemia, better protection is provided by hypothermia than by normothermia. Prior cardioplegia confers little advantage on recovery after prolonged normothermic ischemia but delays initial ischemic metabolic deterioration, which would contribute to the safety of brief interruptions of warm cardioplegia.

Myocardial metabolism and efficiency after warm continuous blood cardioplegia

Background. Warm continuous blood cardioplegia (WCBCP) has been recommended during prolonged cardiac arrest to minimize functional deterioration. Myocardial metabolism and efficiency after this cardioplegic modality are not well described. Methods. Substrate oxidation, blood flow, and myocardial function were measured before, during, and after 3 hours of WCBCP in 7 pigs. Results. Free fatty acid and glucose oxidation decreased by 60% ± 3.8% and 94% ± 1.2%, respectively, during cardioplegia (both p < 0.05) and increased to 62% ± 28% and 122% ± 62% of baseline during the early recovery phase ( p < 0.05 for glucose). One hour after WCBCP oxidation rates were similar to baseline. The transient postcardioplegic increase in substrate oxidation was associated with a 43% ± 23% elevation of oxygen consumption (MVO 2) compared with baseline and a 62% ± 18% increase in myocardial blood flow. Cardiac output and mean arterial pressure did not change significantly after WCBCP, although myocardial function (stroke work, left ventricular end-systolic pressure, end-diastolic pressure, contractility, and efficiency) was depressed ( p < 0.05). End-diastolic pressure and contractility improved from early to late phase of recovery, whereas the other indicators of ventricular function remained depressed. Conclusions. Myocardial substrate oxidation was preserved after 3 hours of WCBCP, although ventricular function was moderately impaired. Thus, WCBCP with a seemingly normal substrate and oxygen supply was associated with a reduced cardiac efficiency.

Warm or cold continuous blood cardioplegia provides similar myocardial protection

Background. This study was performed to investigate the effect of temperature of blood cardioplegia on the recovery of postischemic cardiac function. Methods. Pigs on cardiopulmonary bypass were subjected to global ischemia (30 minutes), followed by cold (n = 10) or warm (n = 11) continuous antegrade blood cardioplegia (45 minutes) delivered at 55–60 mm Hg. Results. Global left ventricular function, evaluated by preload recruitable stroke work, decreased with cold cardioplegia from 91 (85–103) [mean (quartile interval)], at baseline, to 73 (55–87) erg × 10 3/mL postbypass ( p = 0.03), but was unchanged after warm cardioplegia; 110 (80–132) to 109 (71–175) erg × 10 3/mL ( p > 0.5). However, the difference between treatment effects was not significant ( p = 0.25). Diastolic function, evaluated by end-diastolic pressure-volume relation, deteriorated without any difference between groups. Mean cardioplegic flow was similar between groups. Coronary vascular resistance increased at constant rate during warm cardioplegic delivery, but remained unchanged with cold cardioplegia ( p = 0.001 between regression coefficients). Conclusions. No significant difference was found in postischemic functional recovery comparing cold and warm continuous blood cardioplegia. Cold cardioplegia is therefore preferred due to added safety of hypothermia.

The end of the cold era: from intermittent cold to intermittent warm blood cardioplegia.

A major reduction in the energy demand of the myocardium results from the electromechanical arrest, and cooling contributes to a lesser degree to this reduction. It is from this assumption that strategies of myocardial protection, utilizing warm blood cardioplegic induction, followed by cold cardioplegia with terminal warm reperfusion before removal of the aortic cross clamp, became established as optimal myocardial protection. Continuous normothermic perfusion 'closed the loop' by avoiding myocardial ischemia and linking warm induction and terminal reperfusion. A series of laboratory and clinical data confirmed the benefits of warm heart surgery on myocardial function and metabolism. The disadvantages of continuous warm blood cardioplegia including disturbance of the operative field, led surgeons to administer warm hyperkalaemic blood intermittently as a new cardioplegic strategy. This review examines the laboratory and clinical data with reference to the intermittent warm blood cardioplegia, to establish its experimental basis and place in clinical practice. Experimental observation and clinical application have established intermittent warm blood cardioplegia as a practical, effective and cheap myocardial protection technique, particularly with reference to coronary artery surgery.

Intermittent warm blood cardioplegia--an experimental study

The influence of intermittent warm blood cardioplegia (WBCP) on myocardial function and metabolism was studied. Fourty-two adult mongrel dogs were used. The isolated heart of one dog was perfused by the cross circulation method with another support dog. The dogs then were divided into three groups. In group I (n = 6), the empty beating heart was perfused with warm blood (WB) kept at 36 degrees C for 100 minutes. In group II (n = 7), the arrested heart was perfused with continuous WBCP using modified Fremes solution for 100 minutes. In group III (n = 8), the arrested heart was perfused with WBCP for 10 minutes following a 15-minute non-perfusion period. This perfusion method was repeated four times. The E max, LV developed pressure, +/- LV dp/dt and LVEDP were all measured to evaluated the myocardial function. In addition, the coronary venous blood pH, myocardial oxygen consumption, myocardial lactate extraction, coronary blood flow, myocardial high energy phosphate content and myocardial water content were also studied in order to elucidate the myocardial metabolism. Regarding the myocardial function, no significant difference was observed between the three groups. The results of chemical studies on the myocardial metabolism were as follows: (1) the coronary venous blood pH in group III decreased at the end of the no perfusion period of WBCP. But it thereafter gradually returned to the normal physiological range; (2) the myocardial oxygen consumption in group III increased just after each interruption, but then gradually decreased toward following intermittent WBCP; (3) the myocardial lactate extraction decreased at the end of the non-perfusion period. However, it gradually returned to the control value by the end of each period of WBCP perfusion; (4) after 60 minutes of reperfusion, the coronary venous blood pH, myocardial oxygen consumption and myocardial lactate extraction showed no significant differences between the groups; (5) the coronary blood flow in group III increased significantly after 1 minute of reperfusion; (6) the ATP value in group III decreased significantly after 60 minutes of reperfusion. The ADP and AMP values demonstrated no significant difference between the groups during the same period; and (7) no significant difference was seen in the myocardial water content between the groups after 60 minutes of reperfusion. It is thus concluded that 10 minutes of intermittent WBCP followed by a 15-minute interruption appeared to have no deleterious effect on the myocardial function and metabolism.

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Comparative Effects of Continuous Warm Blood and Intermittent Cold Blood Cardioplegia on Coronary Reactivity

Cardioplegia is known to affect coronary vascular reactivity. We examined the effects of intermittent cold and continuous warm blood cardioplegia on beta-adrenoceptor-mediated, adenosine triphosphate-sensitive K+ (K+ATP)-channel-mediated, and endothelium-dependent relaxation and on the myogenic tone of coronary arterioles. Pigs were placed on cardiopulmonary bypass. Hearts were arrested for 1 hour with a cold blood cardioplegic solution administered intermittently (n = 12; iCB-CP) or with a warm blood cardioplegic solution delivered continuously (n = 12; cWB-CP). Selected hearts (n = 6 in each group) were then reperfused for 1 hour. In vitro relaxation responses of precontracted microvessels (50 to 160 microns) were studied in a pressurized no-flow state. Relaxation in response to isoproterenol (beta-adrenergic agonist) was similar after iCB-CP and cWB-CP, whereas forskolin (adenylate cyclase activator)-induced relaxation was impaired more after iCB-CP than after cWB-CP. After reperfusion the respective responses were similar. Both iCB-CP and cWB-CP preserved receptor-mediated, endothelium-dependent relaxation in response to adenosine, 5'-diphosphate; non-receptor-mediated endothelium-dependent relaxation in response to A23187; endothelium-independent cyclic guanosine monophosphate-mediated relaxation in response to sodium nitroprusside, and K+ATP-channel-mediated relaxation. Relaxations in response to 8-bromo-cyclic guanosine monophosphate (a cyclic guanosine monophosphate-dependent protein kinase activator) and to 8-bromo-cyclic adenosine monophosphate (a cyclic adenosine monophosphate-dependent protein kinase activator) were impaired after iCB-CP alone and after reperfusion, whereas the respective responses were not affected after cWB-CP. Myogenic tone was decreased similarly after iCB-CP and cWB-CP but was not further altered after reperfusion. Cardiac function was similar after iCB-CP and cWB-CP. These results suggest that cWB-CP is similar to iCB-CP in its ability to preserve endothelium-dependent relaxation and K+ATP-channel function. The superior preservation of beta-adrenergic-cyclic adenosine monophosphate-mediated coronary responses after cWB-CP is brief and associated with minimal improvement of myocardial function and myogenic tone.

How to Protect Hypertrophied Myocardium? A Prospective Clinical Trial of three Preservation Techniques

Protection of the hypertrophied myocardium during heart surgery is still a controversial matter. We prospectively studied 3 currently available preservation techniques in 60 patients operated on for isolated aortic stenosis. Patients were randomly assigned to one of the following groups: CWB: continuous warm blood cardioplegia ICB: intermittent cold blood with warm blood controlled reperfusion Cryst: intermittent cold crystalloid cardioplegia (SLF11, Biosédra Laboratory, Vernon, France). All groups were matched for age, ejection fraction, NYHA class, aortic valve surface, and operative risk score. There were no deaths. No statistically significant difference was found among the groups in terms of ventilatory support time, ICU stay time, hospitalization or atrial fibrillation occurrence. Blood gases in the coronary sinus at the time of clamp release showed deep acidosis with crystalloid cardioplegia (pH = 7.11 vs 7.39 for CWB and 7.38 for UCB, p < 0.0001) associated with a higher lactate production than in the other groups (1.3 mmol vs 0.5 for CWB and 0.58 for ICB, p < 0.0001). Acidosis was corrected at the end of bypass with no significant differences among groups. CK-MB samples were taken on arrival in ICU, then 6 and 24 hours later. These samples showed much higher levels with cold blood (H6: 70 mcg/l vs 33 for CWB and 45 for Cryst, p = 0.0019). Although the 3 types of cardioplegia may be safely used for isolated aortic stenosis surgery, continuous warm blood cardioplegia appears to be the best choice.

Preconditioning during warm blood cardioplegia.

Preconditioning describes the cardioprotective effects of multiple brief episodes of warm ischemia. The purpose of the study was to determine whether warm ischemia, during the intermittent delivery of warm blood cardioplegia, would induce preconditioning during cardioplegia arrest. Dogs, 15, were randomized to a preconditioning protocol or to serve as controls. The control group received 60 min of continuous warm blood cardioplegia (WBC) followed by 30 min of warm arrested ischemia. The preconditioned group were arrested with WBC and then underwent three consecutive cycles consisting of 10 min of warm ischemia followed by 10 min of reperfusion. Reperfusion was provided by a continuous infusion of WBC. The preconditioning protocol was followed by 30 min of warm arrested ischemia. Myocardial functional recovery was assessed before cardiopulmonary bypass and cardioplegia arrest and again 30, 60 and 90 min after the arrest. Pressure-volume loops were used to measure the maximum elastance of the left ventricle (Emax), diastolic compliance, and used to calculate preload recruitable stroke work area. Myocardial functional recovery was better preserved after 30 min of warm arrested ischemia in those animals that had been preconditioned. Preconditioning may be induced when warm blood cardioplegia is delivered intermittently during cardioplegia arrest.

Cardioplegia retrógrada atrial: estudo clínico

This study presents the results in a group of fifteen patients submitted to cardiac surgery, using continuous atrial retrograde warm blood cardioplegia for myocardial protection. Eleven patients were submitted to myocardial revascularization and four were submitted to valvular transplantation. There was no need for inotropic drugs or intraaortic balloon pump support during or after the procedure, and no myocardial infarction was detected in this group. When the heart was arrested, the cardioplegia line was switched to the atrial cannula. The aortic root was vented throughout the cross-clamp period, and retrograde perfusion was assured by noting the engorged exygenated cardiac veins as well as the return of dark blood through the vent in the aortic root. The patients presented good clinical and laboratory course. No right ventricular dysfunction was detected. Two patients were in atrial fibrillation before the surgery, one of them returned to this cardiac rhythm three days after the procedure.

Myocardial Energy Metabolism and Functional Recovery in Coronary Bypass Surgery: A Comparative Study Between Continuous Retrograde Warm and Mild Hypothermic Blood Cardioplegia

The optimal temperature for delivery of continuous retrograde blood cardioplegia is not known. Twenty-two patients admitted to the hospital for elective coronary artery bypass grafting were randomized into the warm (37°) and mild hypothermic (28°C) cardioplegia groups. Changes in myocardial energy metabolism during cardiopulmonary bypass, postoperative efflux of the creatine kinase MB isoform (CK-MB), functional hemodynamic recovery, and postoperative complications were followed. During aortic cross-clamp, the average oxygen consumption was higher in the warm than in the mild hypothermic group (3.4 ± 0.4 vs 2.4 ± 0.3 ml/minute, p = 0.06), as was the average transcardiac (outflow-inflow) pCO2-difference (1.1 ± 0.1 vs 0.7 ± 0.1 kPa, p = 0.02). The average transcardiac pH-difference during aortic cross-clamp was lower in the warm group (−0.08 ± 0.01 vs −0.06 ± 0.01 U, p = 0.02), reflecting more profound tissue acidosis. In accordance with this, warm hearts produced more lactate, especially towards the end of the aortic cross-clamp period (p = 0.001). The net efflux of adenosine and its degradation products was more prominent during warm than during mild hypothermic cardioplegia (p = 0.016), indicating less degradation of high energy adenylates in the hypothermic group. The functional hemodynamic recovery during the first postoperative day was similar in both patient groups, although the myocardial injury estimated as postoperative leakage of CK-MB was less extensive in the hypothermic group (p = 0.011). There were no major differences in the postoperative complications between the study groups. We conclude that continuous retrograde mild hypothermic blood cardioplegia offers better myocardial protection during coronary bypass surgery than does continuous retrograde warm cardioplegia. The clinical significance of this should be tested in a larger series of patients, especially those with recent myocardial infarction, unstable angina, or severely depressed left ventricular function.

術後急性期の心機能におけるＣｏｎｔｉｎｕｏｕｓ ｗａｒｍ ｂｌｏｏｄ ｃａｒｄｉｏｐｌｅｇｉａの優位性

Continuous warm blood cardioplegia (CWBC) の術後急性期の心機能における優位性を cold crystalloid cardioplegia (CCC) を対照して比較検討した. CABG症例をCWBC群 (21例) とCCC群 (15例) に分け, ICU入室時, 1POD, 2PODの心機能, CK, CKMB値と, ICU入室時, 入室後6h, 12h, 18h, 24hのカテコールアミン使用量を測定し比較検討した. 自己心拍再開率はCWBC群が高率だった. 各時点のCIはCWBC群のほうが高値であった. ICU入室時のLVSWI, LVWIもCWBC群で高値であった. RVSWI, RVWIは各時点で両群間に差がなかった. Dopamine, dobutamine 使用量はCWBC群のほうが少なかった. CK, CKMB値はCWBC群のほうが低値であった. これより離脱後心機能や心筋逸脱酵素においてCWBC群のほうがCCC群より優れた結果を示していた.