Vertical Displacement of the Beating Heart by the Octopus Tissue Stabilizer: Influence on Coronary Flow
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1 of the Beating Heart by the Octopus Tissue Stabilizer: Influence on Coronary Flow Paul F. Gründeman, MD, PhD, Cornelius Borst, MD, PhD, Joost A. van Herwaarden, MD, Cees W. J. Verlaan, and Erik W. L. Jansen, MD, PhD Department of Cardiology, Heart Lung Institute, Utrecht University Hospital, Utrecht, the Netherlands Background. In beating heart coronary artery bypass graft operations, biventricular pump failure, as observed after exposure of the posterior circumflex branches by sternotomy, may originate from mechanical obstruction to coronary flow. Methods. Regional coronary blood flow was measured in 8 anesthetized, paced, -blocked pigs, and the beating heart was fully retracted. Results. decreased cardiac output from L/min (mean standard deviation) to L/min (p < 0.001), a 42% 6% decrease that resulted in a decrease in mean arterial pressure by 48% 6% (mean standard error of the mean; p < 0.001) and a reduction in coronary blood flow in the left anterior descending coronary artery, the right coronary artery, and the circumflex coronary artery by 34% 6%, 25% 8%, and 50% 10%, respectively (all p < 0.05 versus baseline). Relative circumflex coronary artery flow was 20.1% 8.3% lower than the combined relative value of left anterior descending coronary artery and right coronary artery flows (p 0.046). Subsequent 20 degrees headdown tilt significantly increased ventricular preload pressures and restored cardiac output and mean arterial pressure as well as coronary blood flow. Conclusions. It is inferred that coronary blood flow was not mechanically obstructed during anterior displacement of the porcine beating heart, because augmentation of preloads by the maneuver of Trendelenburg restored coronary flow parallel to the recovery of cardiac output and mean arterial pressure while the heart remained retracted by 90 degrees. (Ann Thorac Surg 1998;65: ) 1998 by The Society of Thoracic Surgeons Coronary artery bypass graft operations on the beating heart without cardiopulmonary bypass has recently gained renewed interest for single and multivessel revascularization [1 7]. For surgical access to circumflex branches through sternotomy, the beating heart needs to be displaced anteriorly. Full exposure of posterior branches for arterial revascularization by a local cardiac wall restraining device (Octopus Tissue Stabilizer; Medtronic Inc, Minneapolis, MN) [8] is feasible in the pig [9, 10]. Arterial pressure, however, tends to decrease considerably during 90 degrees anterior displacement of the heart (apex pointing anteriorly) [9]. Such displacement causes a major drop in stroke volume, in spite of elevation of right ventricular preload and unchanged left ventricular preload [9]. The precise mechanisms that cause deterioration of pump function on lifting the beating heart are not fully understood. It is unknown whether obstruction of coronary blood flow (CBF) by mechanical stress to coronary arteries may contribute to the decreased pump function. The objectives of the study were (1) to monitor regional Accepted for publication Dec 27, Address reprint requests to Dr Gründeman, Experimental Cardiology Laboratory, Heart Lung Institute, Utrecht University Hospital (Rm G02.523), PO Box 85500, 3508 GA Utrecht, the Netherlands ( exp.cardio@hli.azu.nl). CBF during vertical displacement of the beating porcine heart by the Octopus tissue stabilizer; and (2) to assess the modifying effect of the Trendelenburg maneuver (whole-body head-down positioning) on the changes in regional CBF. Material and Methods Eight Dutch Landrace pigs (range, 75 to 85 kg) were used. All animals have received humane care in compliance with the Guide for the Care and Use of Laboratory Animals published by the National Institutes of Health (NIH publication 85-23, revised 1985). The study protocol was approved by the Animal Experimentation Committee of the Utrecht University. Doctors Gründeman, Borst, and Jansen, as coinventors of the Octopus method described in this study and as employees of the Utrecht University or the Utrecht University Hospital, may have a financial interest in the method. Doctor Borst also has a consultancy agreement with Medtronic, Inc (Minneapolis, MN), which holds the patent rights to the Octopus by The Society of Thoracic Surgeons /98/$19.00 Published by Elsevier Science Inc PII S (98)
2 Ann Thorac Surg GRÜNDEMAN ET AL 1998;65: CORONARY FLOW OF DISPLACED BEATING HEART 1349 Anesthesia and Hemodynamic Monitoring The animals were premedicated with 2 mg/kg intramuscular azaperone, 1 mg intravenous atropine, and 1.5 mg/kg intramuscular ketamine, and anesthesia was induced with 2 mg/kg intravenous metomidate. Positivepressure ventilation (Medec Libra; Medec Holland BV, Wormerveer, the Netherlands) was started after endotracheal intubation (oxygen/room air mixture, 1:1; halothane 0.5% to 1%). Pancuronium bromide (0.10 mg/kg intravenously) was given as a muscle relaxant. To maintain anesthesia, midazolam (60 mg/ml, 0.06 mg kg 1 h 1 ) and sufentanil citrate forte (500 g/50 ml, 0.6 g kg 1 h 1 ) were continuously infused by an infusor pump (Becton Dickinson Infusion Systems, Brezins, France). For heart rate and rhythm, an electrocardiogram was recorded (standard lead II or III, Space Labs Medical Inc, Redmond, WA). To reduce the mechanical irritability of the heart, intravenous propranolol (range, 15 to 25 mg) was gradually administered to obtain a heart rate between 50 and 70 beats/min. After midsternotomy, the heart was suspended in a pericardial cradle. Catheter tip micromanometers (Millar Instruments, Houston, TX) were inserted into the ventricles for the measurement of the right and left enddiastolic ventricular pressures. Measurements were taken at the time of end-inspiration of the artificial positive-pressure respiratory cycle. A micromanometer (Millar) was introduced in the carotid artery and advanced close to the aortic valve to record phasic and mean arterial pressure (MAP). A bipolar pacing lead was sutured on the right atrial appendage, after which the heart was paced at a fixed rate of 80 beats/min. The right phrenic nerve was transected to avoid inadvertent diaphragmatic contraction elicited by the pacemaker (Lifepack 9P; Physiocontrol Corp, Redmond, WA). An ultrasound transit time flow probe (Transonic Inc, Ithaca, NY; size 20 or 24 mm) was placed around the aorta for on-line measurement of the cardiac output. Stroke volume (SV) was calculated by dividing cardiac output by heart rate (fixed rate 80/min). Flow probes (Transonic) were placed around the proximal right coronary artery (RCA), the proximal left anterior descending coronary artery (LAD) above the first diagonal branch, and the proximal circumflex artery (Cx). Through the hemiazygos vein, draining in the coronary sinus, a withdrawal catheter was inserted through a small left thoracotomy into the great cardiac vein and advanced 1 cm beyond the ostium of the coronary sinus for the measurement of oxygen saturation of the venous effluent from LAD and Cx territories. In the pig, venous return from the RCA drains directly in the right atrium, or at least distally from the tip of the sampling catheter in the orifice of the coronary sinus. The stump of the hemiazygos vein was snared, and the drainage catheter was secured to ensure exclusive cardiac venous blood sampling. Regional myocardial oxygen consumption (ml 100 g myocardium 1 min 1 ) was calculated from the sum of LAD and Cx flow, and arteriovenous oxygen content differences. Two identical, straight EndoOctopus tentacles [8] (Octopus Tissue Stabilizer; Medtronic Inc) were engaged in a dual holder (Gründeman et al, unpublished data) in a parallel fashion and were connected to a 400-mm Hg vacuum source. The dual holder was attached to a flexible articulating arm, which was fixed to a stable point on the operating table rail. The mounted tentacles were maneuvered single-handedly toward the posterior side of the heart on minimally retracting the heart. After each one was positioned on opposite sides of and parallel to the most distal posterolateral branch of the Cx coronary artery, suction was applied, after which the system firmly took hold of the epicardium. The heart was brought up anteriorly until the apex pointed vertically. Branches of the Cx artery on the backside of the heart became well exposed to operation [9, 10]. The entire displacement procedure, including placement and fixation of the tentacles followed by retraction, took a few seconds. A personal computer-based data acquisition system stored hemodynamic variables, which were simultaneously monitored on an eight-channel recorder (Gould Instrument System Inc, Valley View, OH). Experimental Protocol Baseline cardiovascular values were recorded after at least 15 minutes of pacing (phase 1). Subsequently, values were taken 3 (phases 2 through 5) and 15 minutes (phases 3 and 4) after stabilization after each intervention. After fixation of the stabilizers, the heart was vertically displaced without delay with the Octopus by 90 degrees (phase 2, first displacement) until the apex pointed upward. Subsequently, after stabilization of hemodynamics, the operating table was tilted 20 degrees in the headdown position (Trendelenburg maneuver) without changing the position of the heart relative to the body (phase 3). After 15 minutes of Trendelenburg, the operating table was returned to the horizontal position while the heart remained retracted for 15 min (phase 4, second displacement). Subsequently, the heart was put back in the pericardial cradle and released from the Octopus (phase 5). Three consecutive phases (1 through 3) in the experimental protocol are schematically depicted on the abscissa of Figure 1. Statistical Analysis Data are presented as mean standard deviation (absolute values) or as mean standard error of the means (relative values). Statistical analysis was performed using multivariate analysis of variance to assess the influence of displacement and Student s t test to assess the modifying effect of Trendelenburg compared with protocol control values; p less than 0.05 was considered to indicate a significant change. Relative values of flow in the LAD, RCA, and Cx at 3 minutes displacement were compared using a randomized blocks analysis of variance. Hemodynamic variables in Figure 1 are depicted as mean SEM of the percentage of basal values.
3 1350 GRÜNDEMAN ET AL Ann Thorac Surg CORONARY FLOW OF DISPLACED BEATING HEART 1998;65: % of baseline (p 0.001) (Table 1; Fig 1, phase 2). As a result, MAP decreased to 52% 6% of baseline (p 0.001). Right ventricular end-diastolic pressure increased to 176% 16% (p versus baseline). In contrast, no significant change in left ventricular end-diastolic pressure was observed (120% 13%, p 0.12). Coronary blood flow in LAD, RCA, and Cx decreased by 34% 6%, 25% 8%, and 50% 10%, respectively (p 0.001, p 0.024, and p versus baseline, respectively). The relative coronary flow in the LAD was not significantly different from that in the RCA (mean difference 8.5% 4.6%, p 0.11). The relative coronary flow in the Cx was significantly less than the average percentage change of LAD and RCA (mean difference 20.1% 8.3%, p 0.046). Myocardial oxygen consumption decreased by 36% 7% (p compared with baseline). Fig 1. Relative changes in hemodynamic parameters during vertical displacement of the beating porcine heart by the Medtronic Octopus Tissue Stabilizer and the effect of head-down tilt. (BASE pericardial control position; Cx circumflex coronary artery; DIS displacement of the heart by the Octopus, DIS TREND Trendelenburg maneuver [20 degrees head-down tilt] while the heart remained 90 degrees retracted; LAD left anterior descending coronary artery; RCA right coronary artery; mean arterial pressure; Statistical comparison with control values: *p 0.05, **p 0.01, # p 0.001, ˆp versus combined relative value of LAD and RCA flows.) Results All animals survived the entire procedure without the need to defibrillate or administer inotropic drugs. The paced heart remained in a regular rate of 80 beats/min throughout the experiment. Table 1 and Figure 1 summarize the absolute and relative hemodynamic variables and flow data, respectively, measured in the subsequent phases of the protocol. of the Beating Heart The heart was retracted by 90 degrees in a straightforward manner within a few seconds without inadvertent detachment. The right ventricle was folded against the right border of the pericardial sac by the left ventricle. of the beating heart decreased SV to 58% Whole-Body Head-Down 20-Degree Tilt (Trendelenburg) At 3 minutes of Trendelenburg, SV had increased to 87% 6% of baseline (p 0.05) and MAP had just normalized (Table 1; Fig 1, phase 3). Right ventricular end-diastolic pressure had further elevated to 272% 10% (p compared with baseline) and left ventricular end-diastolic pressure had now increased to 171% 7% (p compared with basal values). Coronary blood flow of LAD, RCA, and Cx recovered to 114% 8% (not significant), 115% 8% (not significant), and 84% 9% (p 0.086), respectively. Myocardial oxygen consumption recovered to 92% 4% of baseline (not significant compared with baseline values). At 15 minutes of Trendelenburg, Cx flow decreased again to 75% 6% of baseline whereas other values showed minor changes. Return of Operating Table to Horizontal Position After returning the operation table to the horizontal position, most values returned to pre-trendelenburg levels (Table 1; phase 4). At 15 minutes, preloads further increased and SV did not change. Freely Beating Heart in Anatomic Position After repositioning the heart into its cradle and releasing it from the Octopus, central hemodynamic status improved rapidly and the coronary flows returned to baseline values (Table 1, phase 5). We observed that the right ventricle tended to dilate shortly after the maneuver. Comment The principal findings of the study were, first, in the supine animal vertical displacement of the paced beating heart resulted in a major reduction in SV, MAP, and coronary flows. The latter ranged from 25% in the RCA to 50% in the Cx. Second, the borderline circulatory status during displacement was markedly improved to almost baseline status by blood volume redistribution (Trendelenburg maneuver). At the same time, CBF returned to baseline values.
4 Ann Thorac Surg GRÜNDEMAN ET AL 1998;65: CORONARY FLOW OF DISPLACED BEATING HEART 1351 Table 1. Changes in Hemodynamic Parameters With Various Maneuvers a Parameter Basal Values (phase 1) (phase 2) Trendelenburg 20 Degrees Head-Down (phase 3) Trendelenburg 20 Degrees Head-Down (phase 3 at 15 min) (phase 4) (phase 4 at 15 min) Freely Beating (phase 5) Stroke volume (ml) e c Heart rate (beats/min) Cardiac output (L/min) e c Mean arterial pressure e Right ventricular enddiastolic d 9 3 e pressure Left ventricular enddiastolic e pressure Right coronary artery c blood flow (ml/min) Left anterior descending e coronary artery blood flow (ml/min) Circumflex coronary artery d,f blood flow (ml/min) Regional myocardial oxygen consumption b (ml 100 g 1 min 1 ) d a Values are shown as mean standard deviation (n 8). b Calculated from the sum of left anterior descending coronary artery and circumflex coronary artery flows. When compared with protocol control values where appropriate, p 0.05 was considered significant. c p d p e p f Comparison with combined relative value of the left and right coronary artery flows (p 0.046). of the Beating Heart Fixation of the EndoOctopus tentacles by suction to the posterior wall of the heart without displacement did not change CBF in the Cx (not shown). The deteriorated circulation during displacement was characterized by a 42% reduction in SV and by an elevated right ventricular preload without concomittantly elevated left ventricular preload. This is in full accordance with our previous observations [9]. In the current study, pacing the heart at 80 beats/min prevented the baroreceptor reflex-mediated increase in heart rate as observed earlier [9]. Surprisingly, MAP decreased as much as cardiac output. Apparently, total peripheral resistance did not increase to mitigate the arterial pressure drop. Concomittant with the major drop in arterial pressure, CBF decreased in all coronary arteries, albeit not to the same degree in the three major arteries. The pathophysiology of CBF on displacement is complex. The decrease in CBF is likely to reflect through autoregulation the decrease in myocardial work, as wall tension is supposed to be reduced when afterload is decreased. The assumption that cardiac work was decreased on displacement by the resulting drop in arterial pressure is supported by the observation that left ventricular myocardial oxygen consumption diminished. During various maneuvers, propranolol may have had a negative effect on cardiac performance. The observed changes in left ventricular myocardial oxygen consumption reflect the combined alterations in regional oxygen uptake irrespective of the direction of change within the territories of LAD and Cx. Theoretically, by retracting the heart anteriorly and rightward at the same time, the coronary artery system, including epicardially running arteries and intramyocardial microvasculature, may be subjected to mechanical stress. The observation that the drop in CBF on displacement was somewhat more pronounced in the Cx is hard to explain. Care was taken to avoid placement of the stabilizing paddles across visible Cx branches. It is conceivable, however, that the underlying myocardium was subjected to (shear) stress on retraction, thus somehow limiting flow in the microvasculature. From changes in mean flow through the Cx artery no inferences can be made on subendocardial hypoperfusion. It is conceivable, however, that retraction may cause focal myocardial ischemia. A study with microsphere injections is needed to monitor changes in perfusion of deeper layers of the myocardium on vertical displacement. Effect of 20-Degree Trendelenburg Positioning Twenty degrees of Trendelenburg elevated SV from 58% to 87% of its baseline value. The incomplete recovery of the cardiac output (also from 58% to 87% of baseline) contrasts with our earlier findings [7], but is explained by the inability of the heart to increase its rate in the paced animal (80 beats/min). With the normalization of mean arterial perfusion pressure in the presence of increased preloads, CBF normalized in the LAD and RCA whereas Cx flow recovered to nearly 85% of baseline. Coronary blood flow recovered within 3 minutes without signs of reactive hyperemia. If CBF reduction on displacement had been caused by mechanical obstruction of the coronary arteries (flow-
5 1352 GRÜNDEMAN ET AL Ann Thorac Surg CORONARY FLOW OF DISPLACED BEATING HEART 1998;65: limiting stenosis), normalization of CBF as observed in the LAD and RCA by the Trendelenburg maneuver (augmentation of preloads with concomitant recovery of SV and MAP) would not be expected because the position of the displaced heart relative to the body remained unchanged during tilting. Furthermore, coronary flow must have been largely unrestricted because left ventricular myocardial oxygen uptake suggested normalization after head-down tilt, parallel to the increase in SV and afterload. The somewhat incomplete recovery of Cx CBF to 85% of baseline remains to be understood. An argument against the existence of significant valvular incompetence on retraction is that Trendelenburg improves SV markedly whereas the position of the heart relative to the body does not change. By inspection, we observed distention of the right ventricle on quickly replacing the heart into its anatomic position. The dilatation disappeared within several minutes while the central hemodynamic status improved. Apparently, the right ventricle needs to adjust to physiologic filling pressure after more than 30 minutes of deformation and increased preload. Limitations of the Study In contrast to healthy pigs, displacement of the beating heart in patients with ischemic heart disease and critically impaired left ventricular function may not be tolerated. Extrapolation of these results to clinical practice must be carefully considered although off-pump revascularization of the posterior wall in patients with a beating heart is feasible with the Octopus stabilizer (Jansen EWL, personal communication). Conclusion We infer that coronary blood flow in the major coronary arteries was not mechanically obstructed during abrupt anterior displacement of the beating porcine heart, because augmentation of preloads by the maneuver of Trendelenburg restored coronary flow parallel to the recovery of MAP and myocardial oxygen consumption while the heart remained retracted by 90 degrees. We acknowledge the technical contributions of Hans P. van der Brugge, Hans W. G. Vosmeer, and colleagues. We appreciate the comments on the manuscript by Drs Johan J. Bredée and Jaap R. Lahpor. For assistance in statistical analysis, we thank Ingeborg van der Tweel, Center of Biostatistics, University of Utrecht. References 1. Calafiore AM, Di Giammarco G, Teodori G, et al. Left anterior descending coronary artery grafting via left anterior small thoracotomy without cardiopulmonary bypass. Ann Thorac Surg 1996;61: Robinson MC, Gross DR, Zeman W, et al. Minimally invasive coronary artery bypass grafting: a new method using anterior mediastinotomy. J Card Surg 1995;10: Subramanian VA, Sani G, Benetti FJ, Calafiore AM. Minimally invasive coronary bypass surgery: a multi-center report of preliminary clinical experience [Abstract]. Circulation 1995;92:I Boonstra PW, Grandjean JG, Mariani MA. Improved method for direct coronary grafting without CPB via anterolateral small thoracotomy. Ann Thorac Surg 1997;63: Jansen EWL, Gründeman PF, Borst C, et al. Less invasive off-pump CABG using a suction device for immobilization: the Octopus method. Eur J Cardiothorac Surg 1997;12: Buffolo E, Silva De Andrade JC, Branco JNR, Teles CA, Aguiar LF, Gomes WJ. Coronary bypass grafting without cardiopulmonary bypass. Ann Thorac Surg 1996;61: Jansen EWL, Gründeman PF, Borst C, et al. Less invasive coronary artery bypass grafting on the beating heart: initial clinical experience with the Utrecht Octopus method for regional cardiac wall immobilization [Abstract]. Circulation 1996;94:I Borst C, Jansen EWL, Tulleken CAF, et al. Coronary artery bypass grafting without cardiopulmonary bypass and without interruption of native coronary flow using a novel anastomosis site restraining device ( Octopus ). J Am Coll Cardiol 1996;27: Gründeman PF, Borst C, van Herwaarden JA, Mansvelt Beck HJ, Jansen EWL. Hemodynamic changes during displacement of the beating heart by the Utrecht Octopus Method. Ann Thorac Surg 1997;63:S Jansen EWL, Gründeman PF, Mansvelt Beck HJ, Heijmen RH, Borst C. Experimental off-pump grafting of a circumflex branch via sternotomy using a suction device. Ann Thorac Surg 1997;63:S93 6.
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