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Ann Thorac Surg 1999;68:955-961
© 1999 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Myocardial perfusion during warm antegrade and retrograde cardioplegia: a contrast echo study

^a Division of Cardiovascular Surgery, Toronto General Hospital and the University of Toronto, Toronto, Ontario, Canada
^b Division of Cardiology, Toronto General Hospital and the University of Toronto, Toronto, Ontario, Canada

Address reprint requests to Dr Weisel, Division of Cardiovascular Surgery, Toronto General Hospital, EN 14-215, 200 Elizabeth St, Toronto, ON, Canada M5G 2C4

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. We evaluated distribution of warm antegrade and retrograde cardioplegia in patients undergoing coronary artery bypass grafting (CABG).

Methods. Myocardial perfusion was evaluated pre- and post-CABG using transesophageal echocardiography with injection of sonicated albumin microbubbles (Albunex) during warm antegrade and retrograde cardioplegia. The left ventricle (LV) was evaluated in five segments and the right ventricle (RV) was evaluated in two segments. Segmental contrast enhancement was graded as absent (score = 0), suboptimal or weak (score = 1), optimal or excellent (score = 2), or excessive (score = 3).

Results. Pre-CABG cardioplegic perfusion correlated weakly with severity of coronary artery stenoses (r = -0.331 and 0.276 for antegrade and retrograde cardioplegia, respectively). Antegrade cardioplegia administration resulted in 98% and 96% perfusion to the left ventricle pre- and post-CABG, respectively. Retrograde cardioplegic administration resulted in reduced LV perfusion, with 86% (p = 0.032 from antegrade) and 59% (p < 0.001 from antegrade) pre- and post-CABG, respectively. The average LV perfusion score (mean ± SEM) was greater with antegrade than retrograde cardioplegia both pre-CABG (1.93 ± 0.04 vs 1.53 ± 0.11, p < 0.001) and post-CABG (1.63 ± 0.07 vs 1.19 ± 0.13, p = 0.004). RV perfusion was poor with both techniques pre-CABG, but improved significantly with antegrade cardioplegia post-CABG.

Conclusions. We conclude that warm antegrade cardioplegia results in better left ventricular perfusion than warm retrograde cardioplegia. Right ventricular cardioplegic perfusion was suboptimal, but the best delivery was achieved with antegrade cardioplegia after coronary bypass. We therefore recommend construction of the saphenous vein graft to the right coronary artery early in the operative procedure.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Homogeneous delivery of cardioplegia is an important component of myocardial protection. Poorly protected myocardial segments may have decreased function following ischemia [1]. Animal studies reveal that inhomogeneous cardioplegic delivery results in impaired regional and global left ventricular (LV) systolic function, as well as impaired diastolic function [2].

Antegrade delivery of cardioplegia via the aortic root is a common cardioplegic delivery technique. However, antegrade delivery may result in inhomogeneous perfusion of myocardium in patients with occluded or severely stenotic coronary arteries, decreased coronary perfusion in patients with aortic incompetence, or coronary embolization from patent saphenous vein grafts during redo-coronary artery bypass grafting (CABG). Retrograde cardioplegia via the coronary sinus may provide better protection of myocardium in such patients. However, canine studies have suggested inhomogeneous perfusion of the posterior septum and right ventricle (RV) during retrograde cardioplegia [3]. In humans, anatomic variability in the venous anatomy also raises concerns about the adequacy of LV and RV protection with retrograde cardioplegic techniques.

Myocardial contrast echocardiography (MCE) can be used to assess myocardial perfusion during CABG surgery. Quantitative analyses, such as the rate of contrast washout and area under the intensity-time curve [4, 5], have been correlated with improved perfusion following successful revascularization. Cardioplegic distribution patterns, both antegrade via the aortic root and retrograde via the coronary sinus, using MCE have also been described [1, 6–9]. However, these reports are sparse and tend to focus on cardioplegic distribution in the LV only. The adequacy of RV perfusion, in particular during retrograde cardioplegia, remains controversial.

We performed this study to evaluate the patterns of antegrade and retrograde cardioplegia perfusion in patients undergoing CABG surgery. In particular, we wanted to assess the adequacy of RV perfusion with either technique.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
We evaluated 17 patients undergoing CABG surgery by a single surgeon at Toronto General Hospital. All patients were male. Ages ranged from 48 to 72 years (mean 60 ± 8 years). LV ejection fraction by single plane contrast ventriculography was greater than or equal to 60% in 11 patients, 40% to 59% in 4 patients, and 20% to 39% in 2 patients. All patients had significant triple vessel coronary artery disease. Transesophageal images were inadequate for analysis in 1 patient. Retrograde delivery of cardioplegia was not possible in 2 other patients because of technical difficulties with instrumentation of the coronary sinus. These 3 patients were eliminated from the study group, which consisted of the remaining 14 patients.

The study protocol was approved by the human research ethics committee of the Toronto General Hospital, and all patients gave informed written consent to participate in the study.

Surgical procedure
Standardized anesthetic and surgical techniques were employed as previously described [10]. Cardiopulmonary bypass was instituted via ascending aortic and two-stage right atrial cannulation. A coronary sinus catheter was inserted and positioned as proximal to the mouth of the coronary sinus as possible to perfuse all venous tributaries to the coronary sinus. After occlusion of the ascending aorta, 1,000 mL of cardioplegia was delivered via the aortic root (antegrade) using warm (37°C) 4:1 blood:crystalloid cardioplegia at an aortic root pressure of 70 mm Hg. Following cardioplegic arrest, retrograde (via the coronary sinus) cardioplegia was given at a constant flow rate of 200 mL/min throughout the procedure, unless the cardioplegic pressure exceeded 40 mm Hg in which case the rate was temporarily reduced. The aortic root was decompressed by gravity suction during retrograde cardioplegic delivery. Cardioplegic delivery was interrupted as necessary in order to visualize distal anastomoses. A left internal thoracic artery graft was constructed to the left anterior descending coronary artery as the final bypass graft.

Myocardial perfusion was evaluated using sonicated albumin microbubbles (Albunex, Mallinkrodt Medical Inc, St. Louis, MO). These microbubbles have a mean diameter of 4 µm and a concentration of 450 million microbubbles/mL. Both animal [11] and human [12] studies have shown that intracoronary injection of Albunex has no adverse effects on coronary blood flow, LV function, or systemic hemodynamics. Albunex was administered by injecting 2 mL of the solution into the aortic root catheter for antegrade cardioplegia or into the coronary sinus catheter for retrograde cardioplegia. Antegrade and retrograde injections were performed into the arrested heart while cardioplegia was being administered at 200 mL/min prior to (pre-CABG), and immediately after (post-CABG), the construction of all saphenous vein grafts. (For the remainder of this article, post-CABG refers to the period of time following construction of all distal and proximal saphenous vein graft anastomoses, but prior to implantation of the left internal mammary artery graft and prior to crossclamp removal.) Albunex injections were performed manually at a rate of 2 mL per second by a single operator, followed by an injection of sterile 0.9% saline of a volume equivalent to the dead space of the cardioplegic tubing. Hand delivery of myocardial contrast has been demonstrated to be equally reliable and efficacious when compared to the use of power injectors [13].

Echocardiographic monitoring
After endotracheal intubation, a 5.0 MHZ transducer (Sonos 1500, Hewlett Packard Co, Andover, MI) was placed in the esophagus. Images were obtained using the transgastric short axis view of the right and left ventricle at the level of the papillary muscles, as well as the long axis view of the left ventricle. Images were continuously recorded on 0.5'' videotape starting before the injection of contrast and ending after the disappearance of medium from the myocardium. Imaging planes were kept constant during injections. Gain settings were optimized at the beginning of the study and were not changed for the duration of the study.

Segmental distribution of cardioplegia was evaluated off-line by two independent observers blinded to the method and sequence of cardioplegic delivery. The LV was evaluated in three segments from the short axis view (anteroseptal, posterolateral, and posteroseptal) and two segments from the long axis view (anterior and posterior). The RV was divided into one anterior and one posterior segment from the short axis view.

The presence or absence of contrast was graded according to the scale developed by Aronson and coworkers [1] as follows: 0 = no contrast enhancement; 1 = contrast enhancement suboptimal or weak, but definitely present; 2 = optimal or excellent contrast enhancement; and 3 = attenuation of ultrasound image because of excessive contrast enhancement. The grades given by observers for each injection and segment were averaged.

A myocardial score index was generated to reflect overall ventricular perfusion and was calculated by summing the scores for each segment and dividing the total by the number of segments visualized for each patient.

Statistical analyses
All statistical analyses were performed with Statistical Analysis Systems software (SAS Institute, Cary, NC). Comparisons between groups were performed using Fisher’s exact test and the Wilcoxon rank sums test wherever appropriate. A two-way analysis of variance was employed to evaluate echocardiographic scores. Statistical significance was assumed at a probability level of less than 0.05.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
There were no deaths, myocardial infarctions, or other major complications in this small group of coronary bypass patients.

Contrast enhancement and severity of coronary artery stenosis
Table 1 displays severity of coronary artery stenoses for each patient, as well as number of visualized left and right ventricular segments which were enhanced by contrast (score = 1, 2, or 3) or not enhanced (score = 0) before and after CABG with warm antegrade or retrograde cardioplegia administration. A weak negative trend existed between regional contrast enhancement during antegrade perfusion and increasing severity of corresponding coronary artery disease (r = -0.331, p = 0.098); a weak positive trend was observed between retrograde enhancement and coronary stenoses (r = 0.276, p = 0.128). That is, more severe coronary artery disease correlated with decreased antegrade perfusion and increased retrograde perfusion, but this was not statistically significant.

View larger version (23K): [in this window] [in a new window]   Fig 1. Segmental perfusion of the left ventricle (LV) during antegrade (Ante) and retrograde (Retro) cardioplegia before and after coronary artery bypass grafting (CABG). Stacked bars show the percentage of visualized segments in which contrast enhancement was weak (score = 1), optimal (score = 2), or excessive (score = 3). Antegrade cardioplegic delivery resulted in better perfusion both pre- and post-CABG.

View larger version (19K): [in this window] [in a new window]   Fig 2. Left ventricular perfusion scores (mean ± SEM) during antegrade and retrograde cardioplegia before and after CABG. Antegrade cardioplegic delivery resulted in better mean perfusion scores both pre- and post-CABG.

View larger version (19K): [in this window] [in a new window]   Fig 3. Segmental perfusion of the right ventricle (RV) during antegrade and retrograde cardioplegia before and after CABG. RV perfusion was poor with both techniques pre-CABG, but was better with antegrade delivery post-CABG.

View larger version (126K): [in this window] [in a new window]   Fig 4. Long axis epicardial echocardiographic view of the left ventricle during retrograde cardioplegic administration. Injection of sonicated albumin contrast identified the presence of direct vascular communications (arrows) to the ventricular cavity in all patients. These channels may represent Thebesian veins.

Figure 3 demonstrates that perfusion of the RV with antegrade cardioplegia was better than retrograde cardioplegia post-CABG (62% versus 24% respectively, p = 0.010). RV perfusion for both techniques improved from pre- to post-CABG (p = 0.014).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
The echo intensity of myocardium receiving normal perfusion increases after injections of echocardiographic contrast agents. Conversely, myocardial contrast echocardiography (MCE) has been used to assess underperfused myocardium after myocardial infarction. The "area at risk" or size of infarction as determined by MCE has been shown to correlate with traditional methods of infarction assessment in animal models [14] and in clinical research [15].

In this study, MCE was used to assess myocardial perfusion patterns and the adequacy of perfusion using different cardioplegic techniques in patients undergoing CABG. In particular, we attempted to evaluate both LV and RV perfusion during warm antegrade and retrograde cardioplegia.

We found very good left ventricular perfusion pre-CABG during antegrade cardioplegia. Evidence from animal models would suggest that antegrade cardioplegia should result in decreased perfusion to those areas subtended by occluded or severely stenotic coronary arteries, and that regional perfusion should improve with retrograde delivery [16]. However, these studies tend to be performed in models of acute coronary occlusion, as opposed to the progressive stenoses commonly encountered in human atherosclerosis. Adequate antegrade enhancement in our study population suggests that these patients had significant collateral flow, since 50% of patients had a previous myocardial infarction and 57% had at least one occluded coronary artery. Analysis of those patients who had coronary angiography performed at our institution revealed that all of these patient had angiographic evidence of good collateral circulation to the left ventricle. (Good collateralization of the right ventricle, however, was seen in only 5 of 9 patients with occlusive coronary disease.) The presence of collateral circulation, as well as the relatively small number of patients examined, may explain our inability to demonstrate a statistically significant relation between perfusion and severity of coronary artery stenoses.

Left ventrical perfusion—antegrade versus retrograde cardioplegia
We found significantly improved left ventricular perfusion during antegrade cardioplegia in this study, a finding which agrees with our previous studies [10, 17] and other investigators’ works [18, 19]. We previously compared antegrade and retrograde cardioplegia in a randomized trial of 107 coronary bypass patients [17]. Retrograde cardioplegia resulted in increased myocardial lactate production and creatine kinase MB isoenzyme (CKMB) release, as well as lower adenosine triphosphate (ATP) levels. In another trial, we randomized 75 CABG patients to antegrade, retrograde, or combination cardioplegia (continuous retrograde delivery plus antegrade via completed saphenous vein grafts) [10]. Warm retrograde cardioplegia resulted in increased myocardial lactate and acid release, as well as increased levels of ATP degradation products, when compared to the other two techniques. These two studies led us to conclude that retrograde cardioplegia resulted in suboptimal myocardial protection when compared to antegrade delivery.

There are a number of possible explanations for decreased LV perfusion with retrograde cardioplegia. First, even in experienced hands, the coronary sinus catheter may be placed too distally resulting in the occlusion of the orifices of veins which drain into the terminal coronary sinus, especially the middle and small cardiac veins [20]. Second, the tributaries of the great, small, middle, and posterior veins of the ventricles may have fairly well developed uni- or bi-cuspid valves at their orifices [20], which may subsequently obstruct retrograde flow. Finally, retrograde delivery may be limited by the presence of widespread venovenous anastomoses, which have been described at all levels of the cardiac venous circulation. Previous studies have suggested that up to 60% of the retroperfusate may shunt into the RV via venous and Thebesian channels [3, 18], and therefore significant amounts may never reach the capillary network to act as "nutrient flow." Shunting of retrograde perfusion into both RV and LV cavities via Thebesian channels could be visualized in all of our patients (see Fig 4).

Our finding of increased LV perfusion with antegrade cardioplegia differs somewhat from the results of two previous contrast echo studies. Quintillo and colleagues [8] found significantly improved myocardial opacification during retrograde cardioplegia in patients with poor collaterals. As mentioned above, post-hoc analysis revealed evidence of good LV collateralization in all patients with coronary occlusions in our study. The extent of this collateralization may explain the discordant results with Quintillo and coworkers. A study by Caretta and colleagues [9] also found improved LV perfusion with retrograde delivery. Once again, however, a significant proportion of their patients had occlusive coronary disease with poor collateralization, in contrast to our patient population. In addition, these investigators used twice the dose of sonicated albumin for retrograde delivery (4 mL versus 2 mL for antegrade delivery), which may have confounded their results because of the known linear relationship between dose of sonicated albumin and peak myocardial intensity [21].

Right ventrical perfusion
Assessment of RV perfusion was difficult since the RV was adequately visualized in only 64% of the patients. In a study similar to ours, Aronson and colleagues [1] were able to analyze the RV in only 21% of their patients. The RV is difficult to visualize in cardiac surgical studies because it is thin-walled and anteriorly located, and it is frequently shadowed by microbubbles.

When RV analysis was possible, we found poor perfusion during both antegrade and retrograde cardioplegia pre-CABG. Poor antegrade perfusion was not surprising since 8 of the 9 patients had an occluded or severely stenotic right coronary artery, with angiography revealing poor RV collateral circulation in 5 of these patients. Poor retrograde RV perfusion has been demonstrated by other investigators in animal models [18] as well as in cardiac surgery patients [7]. Inadequate RV perfusion may be explained by the finding that anterior cardiac veins, which drain the free wall of the RV, usually empty into the right atrium directly [20]. Similar to our findings, Allen and colleagues [7] found that retrograde cardioplegia provided poor RV perfusion by contrast echo, with almost four times greater perfusion seen in the LV free wall compared to the RV. These investigators also demonstrated that right ventricular oxygen extraction increased fourfold following retrograde infusion. Aronson and coworkers [6] also demonstrated poor RV perfusion during antegrade and retrograde cardioplegia pre-coronary bypass.

We found that visualization and perfusion of the RV significantly improved with antegrade delivery post-CABG. We feel this is due to implantation of the right coronary artery (RCA) saphenous vein bypass graft in those patients with critical RCA stenoses and poor RV collateral circulation. Since both antegrade and retrograde cardioplegia resulted in suboptimal perfusion of the RV pre-CABG in this study, early implantation of the RCA graft followed by antegrade delivery into the graft may impart the best early protection to the RV.

LV and RV perfusion post-CABG
In the current study, retrograde cardioplegia resulted in decreased myocardial perfusion compared with antegrade delivery post-CABG. The decrease in LV perfusion that we observed from pre- to post-CABG for both cardioplegic techniques (Figs 1 and 2) is an interesting phenomenon. This finding may be related to the fact that despite optimum cardioplegic delivery, there is a degree of myocardial ischemia during crossclamp application and the resultant acidemia or lactate production may result in vasospasm post-CABG. Alternatively, the decrease in myocardial contrast from pre- to post-CABG may be the result of post-bypass myocardial edema, a consequence of cardiopulmonary bypass [22]. Further studies will be required in order to elucidate the mechanism of this finding.

Limitations
A potential limitation of our study is that our cardioplegic flow rates (200 mL/min) during contrast injection was insufficient, particularly during retrograde cardioplegia. We have previously demonstrated, however, that retrograde delivery above 200 mL/min does not increase myocardial oxygen consumption or decrease myocardial lactate or acid production [23]. Flow rates above 200 mL/min result in increased venovenous shunts rather than increased nutritive flow.

Another possible limitation of this study is that we did not perform a quantitative densitometric analysis of myocardial contrast enhancement. To evaluate the presence or absence of perfusion, however, densitometry is unnecessary. In addition, Thebesian flow with retrograde cardioplegia results in non-uniform distribution of contrast, and we found that selecting areas of interest for densitometric analysis was difficult. Therefore we believe that a quantitative analysis is inaccurate and misleading during retrograde cardioplegia because of the inhomogenous distribution of cardioplegia.

Finally, it should be noted that not all myocardial segments could be analyzed for all sonicated albumin injections. Our decision to assess the RV and LV simultaneously in the short axis view may have resulted in decreased visualization of the RV. In addition, shadowing from contrast in other myocardial segments or in ventricular cavities at times obscured the anterior walls of the left and right ventricles. However, we did not find a difference in the number of segments available for analysis between antegrade and retrograde cardioplegia, and therefore we feel our conclusions on the efficacy of these two techniques are valid.

In conclusion, we found that antegrade cardioplegia resulted in better myocardial perfusion than retrograde cardioplegia in our population of elective coronary bypass patients. Retrograde cardioplegia resulted in shunting of this retroperfusate through Thebesian veins directly into the ventricular cavities, bypassing the nutrient capillary network and decreasing segmental perfusion. These observations support our previous studies which suggested that the use of retrograde cardioplegic delivery alone provides inadequate myocardial protection during cardiac surgery.

The right ventricle was not well perfused by either retrograde or antegrade techniques prior to coronary bypass. Cardioplegic perfusion of the right coronary bypass graft early after cardioplegic arrest may improve RV protection.

	Acknowledgments

 
This research was supported in part by the Heart and Stroke Foundation of Ontario, grant NA 3767.

	References

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This Article Abstract Full Text (PDF) 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): Michael A. Borger Richard D. Weisel John S. Ikonomidis Vivek Rao Gideon Cohen Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Borger, M. A. Articles by Rakowski, H. Search for Related Content PubMed PubMed Citation Articles by Borger, M. A. Articles by Rakowski, H.