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Ann Thorac Surg 1996;62:9-15
© 1996 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Salvage of Ischemic Myocardium With Simplified and Even Delayed Coronary Sinus Retroperfusion

Department of Cardiothoracic Surgery, Boston University Medical Center, Boston, Massachusetts

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. Despite the proven efficacy of pressure-controlled intermittent coronary sinus obstruction (PICSO) and synchronized retrograde perfusion (SRP) in salvaging ischemic myocardium, wide application of these coronary sinus (CS) retroperfusion techniques has been limited by concerns about their safety and complexity and in particular the need for repeated occlusion of the CS with a balloon. To address these concerns a simplified retroperfusion technique (SR) was developed that continuously infuses superior vena caval blood at 7 mL/min into the CS catheter without balloon occlusion.

Methods. Thirty pigs underwent 90 minutes of ischemia imposed by snaring the two largest diagonal branches of the left anterior descending artery and were randomized to one of five treatment groups: One group received no retroperfusion (control). Three groups had immediate (Im) institution of PICSO, SRP, or SR. In a final group, an initial 60 minutes of ischemia was followed by 30 minutes of delayed SR with superior vena caval blood. All animals were then placed on cardiopulmonary bypass and, after a 60-minute cardioplegic arrest, the coronary artery obstructions were removed, to simulate surgical revascularization. This was followed by 3 hours of reperfusion. The area of myocardium at risk and the area of infarction were determined by methylene blue and triphenyltetrazolium chloride staining with planimetric quantification.

Results. Results are reported as mean ± standard deviation. The area of the left ventricle at risk for infarction was similar in all the treatment groups and represented 22.3% ± 4.1% of the left ventricular mass. The area of infarction after 3 hours of reperfusion was 48.5% ± 11.0% for the control group, 26.8% ± 7.3% for Im-PICSO, 24.9% ± 4.8% for Im-SRP, 22.4% ± 6.6% for Im-SR, and 27.7% ± 7.2% for delayed SR (p < 0.01 for each group versus control). The mean CS pressure (in mm Hg) during treatment was 6.3 ± 1.7 for the control group, 25.7 ± 4.5 for Im-PICSO, 22.8 ± 3.7 for Im-SRP, 5.0 ± 1.5 for Im-SR, and 6.3 ± 2.1 for delayed SR (p < 0.01 for Im-PICSO and Im-SRP versus control).

Conclusions. The simplified retroperfusion technique is as effective as PICSO and SRP in salvaging ischemic myocardium, but is considerably simpler. The simplified retroperfusion technique is inherently safer because of the lower CS pressures imposed by low flows and the lack of CS balloon obstruction. The efficacy of delayed SR has profound implications on possible mechanisms of ischemic myocardial salvage. Further investigation is warranted.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 15.

In the past four decades, enormous advances in augmenting blood flow to the ischemic myocardium have been made. The use of thrombolytic agents, percutaneous transluminal angioplasty, and coronary artery bypass grafting have become established methods in the treatment of acute coronary artery ischemia. These interventions are directed toward the coronary arterial system where unstable atherosclerotic lesions are found. It should be noted, however, that the initial attempts to treat myocardial ischemia were directed to the coronary venous system [1, 2], which is free of atherosclerotic disease [3].

With the increasing incidence of patients presenting with unstable angina and evolving acute myocardial infarction, the coronary venous system has emerged as an alternative route by which blood can be delivered to the ischemic myocardium. With advances in catheter design and imaging techniques that facilitate access to the coronary sinus (CS) and the development of safer retroperfusion strategies, synchronized retrograde perfusion (SRP) [4– 8] and pressure-controlled intermittent coronary sinus occlusion (PICSO) [7– 10] have emerged as new techniques to redirect blood to the ischemic myocardium beyond a coronary artery occlusion.These techniques have been demonstrated both experimentally and clinically to either delay or reverse ischemic changes, decrease infarct size [6, 10], decrease myocardial hemorrhage and no-reflow phenomenon [6], and improve left ventricular function [11] when coronary blood flow is reinstituted after an acute coronary artery occlusion. The exact mechanisms by which CS retroinfusion salvages ischemic myocardium have not been fully elucidated. However, enhanced washout of toxic reactive oxygen metabolites [12], diminished granulocyte trapping [13], diminished cellular and interstitial edema [14], diminished plugging of the microcirculation, and actual delivery of blood substrate to the ischemic myocardium beyond an acute coronary artery occlusion have all been suggested. Experimental studies using radioactive microspheres and xenon 133 have demonstrated that the restoration of perfusion achieved with SRP only reaches 10% to 60% of normal levels [15, 16], suggesting that nutritive flow achieved by this technique is limited. Because reoxygenation of the ischemic zone is only partial, other mechanisms may be responsible for the observed reduction in infarction.

In cardiac surgery, the role of retrograde CS cardioplegia to supplement antegrade cardioplegia delivery to the myocardium in the presence of coronary artery occlusion has been firmly established and liberally applied [17, 20]. Despite numerous experimental and clinical demonstrations of the efficacy of SRP and PICSO in salvaging acutely ischemic myocardium, wide application of these CS retroperfusion techniques has been limited by concerns over their safety and complexity and in particular the need for repeated occlusion of the CS with a balloon. Both techniques depend on complex gating mechnisms to pneumatically inflate and deflate an occlusive balloon in the CS and either passively redirect CS blood (PICSO) or actively pump arterial blood during diastole (SRP) to the ischemic myocardium at risk. High CS pressures (PICSO and SRP) and CS flow (SRP) could result in myocardial edema, hematoma and damage, and CS perforation with tamponade [7].

To address these concerns, we developed a simplified CS retroperfusion technique (termed simplified retroperfusion [SR]) that continuously infuses superior vena caval blood into the CS catheter without balloon occlusion at 7 mL/min. We hypothesized that because full nutritive flow could never be established with any CS retroperfusion techniques, the mechanism of ischemic myocardial salvage could be accomplished as effectively with SR as with SRP or PICSO. We further suggested that the amount of retroperfusate required to modify the resultant infarction after restoration of antegrade myocardial flow may be quite small, and the the timing of the CS retroperfusion intervention could be further delayed and still result in effective ischemic myocardial salvage. This experimental study was undertaken to test the hypothesis that SR (both immediate and delayed) is as effective as PICSO and SRP in reducing the infarct size and ischemic injury after an abrupt coronary artery occlusion followed by a simulated surgical revascularization.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
General Preparation
All animals received humane treatment in accordance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide for the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH publication 86-23, revised 1985). Adult pigs (mean weight, 45.5 kg) were premedicated with intramuscular morphine sulfate (2 mg/kg), anesthetized with alpha-chloralose (75 mg/kg), and supported with positive-pressure ventilation. Catheters were placed into the aorta and left femoral vein for monitoring of systemic pressure and administration of fluids. A median sternotomy was performed, the pericardium was incised and suspended, and the animals were systemically anticoagulated with heparin (3 mg/kg intravenously maintaining an activated clotting time > 500 seconds). The two largest diagonal branches (usually the second and third diagonals) were carefully dissected at their origin from the mid-left anterior descending artery and encircled with vascular snares. Intravenous lidocaine (100 mg) was used to pretreat the animals before imposition of acute, anterior wall, coronary artery occlusion. No inotropic or other pharmacologic agents were given. A double-lumen balloon-tipped retrograde coronary sinus cardioplegia catheter (10F; DLP, Inc, Grand Rapids, MI) was inserted from the internal jugular vein into the CS appropriately, deaired, positioned at the the level of the great cardiac vein, and secured in place (Fig 1). The catheter was used to monitor CS pressure and deliver retroperfusion therapy. The same catheter model was used in all treatment groups.

View larger version (37K): [in this window] [in a new window]   Fig 1. . The simplified retroperfusion catheter is directed from the internal jugular vein into the coronary sinus and the tip is positioned near the great cardiac vein (GCV), which parallels the left anterior descending artery.

View larger version (21K): [in this window] [in a new window]   Fig 2. . Experimental design I. Effect of retroperfusion strategy on myocardial salvage. (CA = coronary artery; CPB = cardiopulmonary bypass; Del = delayed; PICSO = pressure-controlled intermittent coronary sinus obstruction; SR = simplified retroperfusion; SRP = synchronized retrograde perfusion; V = venous blood.)

IMMEDIATE PRESSURE-CONTROLLED INTERMITTENT CORONARY SINUS OCCLUSION.
Six pigs received immediate (Im) PICSO therapy after imposition of coronary artery occlusion for 90 minutes. The previously placed CS catheter was connected to a CS pressure feedback control box (Meditech Labs, Charlestown, MA), which automatically inflated and deflated the CS balloon according to a previously preset cycle. The control box consisted of a pneumatic pump that inflated the CS balloon to a preset pressure. During the infation period, when the CS was occluded, there was a slow increase in the CS pressure until a peak pressure was maintained for three to four heart beats. When that pressure was reached, the balloon was automatically deflated, resulting in an abrupt decrease in the CS pressure. When the CS pressure reached baseline levels, the balloon was automatically reinflated and the PICSO cycle was repeated. Previous studies in our laboratory have shown that PICSO is most effective when the inflation-deflation cycle is set for 10 seconds of inflation and 4 seconds of deflation [21].

IMMEDIATE SYNCHRONIZED RETROGRADE PERFUSION.
Six pigs received Im-SRP therapy after imposition of coronary artery occlusion (Mansfield Scientific, Boston, MA) for 90 minutes. Arterial blood was shunted from the femoral artery into the great cardiac vein by a gated pump mechanism through the previously placed CS catheter. The CS balloon was infated during diastole by electrocardiographic triggering using a pneumatic pump and arterial blood was actively pumped into the great cardiac vein using a second, servo-controlled infusion pump also gated to the R wave of the electrocardiographic signal. During diastole, the CS was occluded with a balloon and arterial blood was actively reinfused into the great cardiac vein. During systole, active infusion of arterial blood ceased and the CS balloon was deflated. The SRP cycle was repeated with each cardiac beat. Synchronized retrograde perfusion was initiated at a flow rate of 10 mL/min and rapidly increased until peak CS pressures reached 40 to 50 mm Hg, giving flows between 50 and 200 mL/min [6].

IMMEDIATE SIMPLIFIED RETROPERFUSION.
Six pigs received Im-SR for 90 minutes. Superior vena caval blood was continuously withdrawn into a reservoir through a Cordis introducer (Baxter, Irvine, CA) using a volumetric infusion pump (Baxter Flow-Gard 6201, Deerfield, IL), and a level of 50 mL of blood was maintained in the reservoir. Using another Harvard infusion pump the blood was administered through the previously placed CS catheter at 7 mL/min, without CS occlusion.

DELAYED SIMPLIFIED RETROPERFUSION.
In 6 pigs, after an initial ischemic period of 60 minutes during which no intervention was performed, continuous infusion of superior vena caval blood was initiated through a previously placed CS catheter at 7 mL/min, without CS occlusion, and continued for 30 minutes. Thus, in this experimental group, CS retroinfusion was delayed by 60 minutes and delivered for only 30 minutes during the 90 minutes of acute coronary artery occlusion.

To assess the effect of the CS retroperfusate composition on ischemic myocardial salvage, 12 animals were further randomly assigned to two final treatment groups (Fig 3):

View larger version (26K): [in this window] [in a new window]   Fig 3. . Experimental design II. Effect of simplified retroperfusion (SR) retroperfusate composition on myocardial salvage. (Abbreviations are as in Figure 2.)

IMMEDIATE SIMPLIFIED RETROPERFUSION WITH CRYSTALLOID.
Six pigs received Im-SR for 90 minutes. Plasmalyte (Baxter, Deerfield, IL) was continuously infused through a previously placed catheter at 7 mL/min, without CS occlusion.

At the end of the 90 minutes of acute anterior ischemia, all animals were placed on total cardiopulmonary bypass and cooled to 32°C. An antegrade cardioplegic arrest was achieved with 800 mL of cold blood cardioplegia (4°C), supplemented with 400 mL of retrograde CS cardioplegia and topic hypothermia. Antegrade and retrograde cardioplegia were readministered every 20 minutes (400 mL via each route). At the end of 60 minutes of total cardiopulmonary bypass, the cross-clamp was removed and the occlusive coronary artery snares were released, simulating a successful coronary revascularization. The animals were warmed to 37°C, and the hearts were reperfused for 3 hours.

Measurements and Data Analysis
Electrocardiographic leads were used to monitor heart rate and electrical activity during ischemia and cardiac arrest. Left ventricular end-diastolic pressure was recorded with piezoelectric Mikro-Tip catheter pressure transducer (Millar Instruments, Inc, Houston, TX) inserted via a stab wound in the left ventricular apex.

Two-dimensional echocardiographic recordings were obtained with a hand-held 3.5-MHz ultrasound transducer (ALT, Temple, AZ). An echocardiographic short-axis image was obtained at the level of the papillary muscles. Serial measurements were imaged to assess changes in regional wall motion. The ventricle was arbitrarily divided into eight anatomic areas and the wall motion analyzed qualitatively by a double-blinded experienced echocardiographer using a numeric score (4 = normal, 3 = mild hypokinesia, 2 = moderate hypokinesia, 1 = severe hypokinesia, 0 = akinesia, and -1 = dyskinesia) averaged over 20 heart beats. To standardize loading conditions between animals, echocardiographic scores were obtained at a constant preload (left ventricular end-diastolic pressure of 15 mm Hg) by using partial right heart bypass and loading technique at a constant afterload (mean arterial pressure, 65 mm Hg).

The area at risk and the area of necrosis were determined by histochemical staining, as previously described [22]. After a 3-hour reperfusion period, the second and third diagonal branches were reoccluded, the ascending aorta was cross-clamped, and the area at risk was determined by injecting 60 mL of phthalo-blue dye (Harshaw-Filtrol, Cleveland, OH) into the aortic root through the antegrade cardioplegia catheter. The heart was then removed and the left ventricle was systematically divided into 5- to 10-mm cross-sectional slices. The infarct area was determined by incubating the slices in triphenyltetrazolium chloride (Sigma Chemical Co, St Louis, MO) for 30 minutes and then placing them in formaldehyde overnight. The next morning, the stained slices were placed under a glass plate and traced on a clear plastic sheet. With reperfusion of the ischemic myocardium, there is a washout from the nonviable cells of dehydrogenases necessary to reduce nitro blue tetrazolium, and these areas remain pale [22]. The areas of risk and infarct are then measured with planimetry and quantified for each slice to obtain (1) the area of risk compared with the left ventricular mass and (2) the area of infarct in the area at risk.

Numeric Methods
All data are presented as the mean ± standard deviation. Statistical evaluation between treatment groups was performed by repeated measures analysis of variance and a Newman-Keuls a posteriori test of significance. Differences were considered significant at a p value less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The mean blood pressure was similar (no significant differences) in all treatment groups throughout the experiment (Table 1). The left ventricular end-diastolic pressure was also similar (no significant differences) among treatment groups, with an initial left ventricular end-diastolic pressure of 4.0 ± 0.9 mm Hg before the imposition of acute anterior wall ischemia, 8.2 ± 3.5 mm Hg after 90 minutes of ischemia, and 13.2 ± 4.2 mm Hg after 3 hours of reperfusion. The area of the left ventricle at risk for infarction measured as a percentage of the left ventricular mass was also similar in all treatment groups (Fig 4). The area of necrosis after a 3-hour reperfusion, represented as a ratio to the area of the left ventricle at risk for infarction, was significantly lower in the Im-PICSO, Im-SRP, Im-SR-venous and delayed SR-venous groups compared with the control group (p < 0.01) (Fig 5), with a reduction of 43% to 54%. The mean CS pressures during treatment were significantly higher in the Im-PICSO and Im-SRP treatment groups (p < 0.05) (Fig 6). The effect of SR retroperfusate composition on ischemic myocardial salvage was evaluated. Again, there were no differences in the area of the left ventricle at risk for infarction between the treatment groups (Fig 7). There were no significant differences in the ratio of area of necrosis to the area at risk between the Im-SR-arterial, Im-SR-venous, and Im-SR-crystalloid groups (Fig 8). There were no differences in echocardiographic scores between treatment groups before ischemia, after 90 minutes of ischemia, and after 3 hours of reperfusion. After 90 minutes of ischemia, the echocardiographic left anterior wall function was severely depressed in all treatment groups, with a mean score of 0.8 ± 0.2 (p < 0.0001 compared with preischemic value). After a 3-hour reperfusion period the echocardiographic anterial wall motion improved to 1.7 ± 0.2 (p < 0.0002 versus 90 minutes of ischemia) but remained depressed when compared with the preischemic value (p < 0.0001) (Fig 9).

View larger version (17K): [in this window] [in a new window]   Fig 4. . Comparison of the left ventricular area at risk (presented as a percent of the left ventricular mass). (Abbreviations are as in Figure 2.)

View larger version (16K): [in this window] [in a new window]   Fig 5. . Comparison of the area of necrosis (presented as a ratio of the area at risk). (*p < 0.01.) (Abbreviations are as in Figure 2.)

View larger version (11K): [in this window] [in a new window]   Fig 6. . Coronary sinus (CS) pressure (in mm Hg) during treatment. (*p < 0.05.) (Abbreviations are as in Figure 2.)

View larger version (13K): [in this window] [in a new window]   Fig 7. . Comparison of the left ventricular area at risk (presented as a percent of the left ventricular mass). (A = arterial; c = crystalloid; IM = immediate; SR = simplified retroperfusion; V = venous.)

View larger version (12K): [in this window] [in a new window]   Fig 8. . Comparison of the area of necrosis (presented as a ratio of the area at risk). (Abbreviations are as in Figure 7.)

View larger version (13K): [in this window] [in a new window]   Fig 9. . Comparison of anterior left ventricular echocardiographic function. (*p < 0.0001 versus preischemia; •p < 0.0002 versus preischemia and versus 90 minutes of ischemia.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Immediate SR with superior vena caval blood was as effective as Im-PICSO and Im-SRP in salvaging acutely ischemic myocardium (see Fig 5). Previous studies have demonstrated that SRP can only restore 10% to 60% [15, 16] of antegrade nutritive flow. We did not specifically study the differences in regional blood delivery to the ischemic area beyond the acute coronary artery occlusion but assume that the flow delivered by SRP (with mean CS catheter flow of 50 mL/min and maximal CS flows exceeding 200 mL/min) is greater than the passive CS flow imposed by PICSO with CS occlusion or imposed actively without CS occlusion by SR (7 mL/min). Despite these differences, the degree of myocardial salvage was not statistically different among retroperfusion strategies. Because Im-PICSO, which is thought to passively displace the very desaturated CS blood into the ischemic myocardial bed, accomplished myocardial salvage similar to that of Im-SRP, we can infer that neither the absolute amount of retroperfusate flow nor the degree of oxygenation or oxygen delivery is critical in salvaging ischemic myocardium. We are not surprised, therefore, that the composition of retroperfusate (arterial blood, venous blood, or crystalloid solution) did not influence the efficacy of SR in salvaging ischemic myocardium.

Finally, despite a delay in CS retroperfusion by 60 minutes and a shorter duration of therapy (30 minutes), the delayed SR with venous blood was equally effective as immediate CS intervention strategies in salvaging ischemic myocardium (see Fig 5). Our results demonstrate that the beneficial effects of reperfusion could be obtained from a brief and even delayed CS intervention, with minimal retroperfusate reaching the ischemic muscle. Although we did not specifically study the mechanism by which CS retroperfusion accomplishes myocardial salvage, these results imply that of the various proposed mechanisms of how CS retroinfusion accomplishes myocardial salvage, rather than providing adequate nutritive flow, myocardial salvage is perhaps accomplished by decreasing the reperfusion injury that results when antegrade coronary blood flow is restored after a prolonged period of ischemia. Others have suggested that this attenuation of the reperfusion injury may be mediated by a decrease in granulocyte trapping or enhanced preservation of endothelial integrity or function [6, 12–14].

Because CS interventions can rarely be initiated at the onset of an acute ischemic event, the efficacy of delayed SR widens the window for therapeutic intervention and offers this strategy as a practical clinical option. We did not study the effect of longer delays in initiation of therapy (greater than 60 minutes) on attempted salvage of acutely ischemic myocardium. However, Allen and associates [23] successfully demonstrated salvage of ischemic myocardium hours after an acute imposition of coronary artery occlusion when conditions of reperfusion and the composition of the retroperfusate were carefully controlled. More recently Wakida and colleagues [6] also demonstrated similar results with delayed SRP after 3 hours of acute ischemia.

In conclusion, a simplified CS retroperfusion strategy was developed that continously infuses blood into the CS without balloon occlusion and effectively salvages acutely ischemic myocardium. The SR technique is inherently safer and simpler than PICSO and SRP because it does not require repeated CS occlusions, does not impose high CS flows and pressures, and does not require complicated gating mechanisms. The efficacy of delayed SR provides an opportunity for continued research into the possible mechanisms responsible for ischemic myocardial salvage and has important implications on clinical utility. Simplified retroperfusion should be considered for further experimental and clinical investigation before its clinical use is broadened.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.

Address reprints requests to Dr Aldea, Department of Cardiothoracic Surgery, Boston University Medical Center, 88 E Newton St, Boston, MA 02118-2393.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Gabriel S. Aldea Richard J. Shemin Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Aldea, G. S. Articles by Shemin, R. J. Search for Related Content PubMed PubMed Citation Articles by Aldea, G. S. Articles by Shemin, R. J. Related Collections Related Article