Ann Thorac Surg 2002;73:809-812
© 2002 The Society of Thoracic Surgeons
Original article: cardiovascular
Epicardial ultrasound in off-pump coronary artery bypass grafting: potential aid in intraoperative coronary diagnostics
Patrick Klein, MSca,
Rudy Meijera,
Jan H. R. Eikelaar, MDa,
Paul F. Gründeman, MD, PhDa,
Cornelius Borst, MD, PhD*a
a Department of Cardiology, Heart Lung Center, Utrecht University Medical Center, Utrecht, The Netherlands
Accepted for publication November 26, 2001.
* Address reprint requests to Dr Borst, Utrecht University Medical Center (G02.523), PO Box 85500, 3508 GA Utrecht, The Netherlands
e-mail: c.borst{at}hli.azu.nl
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Abstract
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Background. In off-pump coronary artery bypass surgery (OPCAB), epicardial ultrasound may aid in several intraoperative dilemmas. The aim of this study was to test a new mini-transducer for intraoperative coronary diagnostics.
Methods. A 10 MHz mini-transducer (15 x 6 x 9 mm) was applied epicardially in eight open chest and two closed chest porcine OPCAB procedures (using robotics) and on four postmortem human hearts. The transducer fitted in between the suction pods of the cardiac stabilizer and passed an 11-mm port.
Results. In the open chest cases the internal mammary arteries (including the side branches) could be visualized totally (n = 12). The left anterior descending coronary artery could be located over its entire course. Vascular anatomy, side branches, and septal perforators (diameter 0.2 mm) could easily be discerned. In the closed chest cases the left anterior descending coronary artery, its side branches, and septal perforators could be visualized in both cases. In the postmortem human hearts the left anterior descending coronary artery could be visualized totally under the thick epicardial fibro-fatty layer and pathologic conditions could be identified.
Conclusions. The 10 MHz ultrasound mini-transducer showed promise as a diagnostic tool in both open and closed chest coronary procedures on the beating heart.
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Introduction
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In off-pump coronary artery bypass (OPCAB) surgery [1], epicardial ultrasound may aid in five intraoperative dilemmas. First, localization of the coronary artery under the epicardial fat and determination of its course and side branches. Second, determination of an anastomotic site with little coronary pathology. Third, isolation of a coronary segment without a major (septal perforating) sidebranch to prevent profuse retrograde bleeding from the arteriotomy. Fourth, visualization of the course of the internal mammary artery (IMA) and its sidebranches. Fifth, assessment of the quality of the anastomosis before chest closure. Using various ultrasound probes, the potential value of intraoperative use of high frequency epicardial ultrasound has been demonstrated by Hiratzka and colleagues, McPerson and associates, and others [28] in the 1980s and 1990s. At that time, however, technical limitations of the equipment such as imaging performance, size of the transducer, and cardiac motion prevented routine clinical application.
The introduction of beating heart coronary surgery using a stabilizer has opened a renewed interest in epicardial ultrasound. The aim of this study was to explore the value of a recently developed mini-transducer in the localization of coronary arteries, evaluation of arterial anatomy and determination of optimal anastomotic target site. The mini-transducer was applied in porcine open and closed chest OPCAB procedures and on postmortem human hearts.
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Material and methods
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Animals
This study was performed in eight Dutch Landrace pigs weighing 80 to 120 kg. It was carried out in compliance with the "Guide For the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources. All procedures performed in this study were approved by the Animal Experimentation Committee of the Utrecht University.
Anesthesia and surgical procedure
The animals were sedated using azaperone (2.0 mg/kg) and ketamine (1.5 mg/kg), administered by intramuscular injection. An intravenous line was established, and metomidate (2.0 mg/kg) and atropine (1.0 mg) were administered. The animals were intubated and mechanically ventilated. Anesthesia was maintained by an intravenous infusion of midazolam (0.06 mg · kg-1 · h-1) and by supplying a mixture of oxygen and air (1:1 v/v), with 1% of halothane added. Analgesia was obtained by intravenous infusion of sufentanil-citrate (0.6 ug · kg-1 · h-1). The heart was exposed through a median sternotomy. By means of the Octopus-2 stabilizer (Medtronic, Minneapolis, MN) segments of the left anterior descending coronary artery (LAD) were stabilized [9].
Ultrasound equipment
The Aloka SSD 5000 Pro-sound ultrasound system and UST-5531 linear array mini-transducer were used with a 10.0-MHz transmission frequency and a field of view 10.0 mm in width. The transducer is 15 mm in length, 6 mm in width, 9 mm in height. It was connected to the ultrasound system by a thin flexible cable. Manipulation was done using a specialized scalpel-shaped connecting grip. The mini-probe fitted in all directions between the suction pods of the Octopus-2.
OPCAB study protocol
Six animals were used in an OPCAB-setting. First, the IMAs were scanned in situ. The location of large side branches (
1.0 mm) was noted together with their diameters. Second, the course of the LAD was identified. Third, from beginning to end, the LAD was divided into five segments and scanned transversally in B-mode to visualize vascular anatomy and locate side branches. Fourth, the different segments were scanned longitudinally in B-mode to visualize and locate septal perforators. Finally, a longitudinal-sweep in color Doppler-flow mode in the different segments was performed to verify the findings in B-mode.
Endoscopic OPCAB study protocol
Two animals were used in a totally endoscopic OPCAB setting. Four ports with a diameter between 10 and 12 mm were placed for introduction of the robotic endoscopic master-slave surgery equipment (Da Vinci, Intuitive Surgical, Mountain View, CA), Octopus-1 stabilizer (separate suction pods [10]), camera, and ultrasound transducer.
In vitro study protocol
Four postmortem human hearts (patient age at time of death 70+ years, cause of death unknown) were pressure-perfused (80 mm Hg) with normal saline. The LAD was scanned with emphasis on the visualization of coronary pathology. Data are presented as mean ± standard deviation (SD).
First, the LAD was located on the heart under the epicardial fat layer in a transversal-sweep using B-mode. Second, when the course of the vessel was noted, the LAD was divided into five segments and scanned transversally in B-mode; vascular anatomy, pathology (arteriosclerotic plaque formation, stenosis, occlusion, and calcification) and side branches were visualized in this way. Third, the different segments were scanned longitudinally in B-mode to visualize septal perforators. The location of the pathology, side branches, and septal perforators were drawn on a standardized vascular map. The mean diameter of the LAD in the different segments and the mean diameter of the septal perforators were noted. The scanning time of a single transversal sweep in B-mode of the entire LAD was also recorded.
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Results
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OPCAB study
IMA localization
Both IMAs could be visualized over their entire length (n = 12). In the thoracic cavity their internal diameter measured proximally 2.5 ± 0.4 mm, medially 1.7 ± 0.4 mm, and distally 1.4 ± 0.1 mm. The location of all large side branches (
1.0 mm) corresponded to the finding during subsequent routine harvesting procedure.
LAD localization
In 6 of 6 animals the LAD could easily be identified under the epicardium and its entire course followed from beginning at the main stem to the apex. Scanning in transverse B-mode required 2 ± 1 minute (±SD). Its vascular anatomy and side branches could be easily identified. Making a longitudinal sweep between the two suction pods of the Octopus-2 (Fig 1A),
septal perforators with a diameter of 0.2 mm or more could be discerned in all animals (Fig 1B). In all cases color Doppler-flow mode recordings (Fig 1C) were concordant with the B-mode findings. The results are summarized in Table 1.
Totally endoscopic OPCAB study
The mini-transducer could be inserted through an 11-mm port and the LAD and its side branches and septal perforators visualized. In contrast to the open chest procedure, in the endoscopic approach the stabilizer could not properly reach the extremes of the LAD. Scanning required 7 and 5 minutes, respectively in the two animals.
In vitro study
In all four postmortem human hearts, the LAD could be located under the thick epicardial fibro-fatty layer and its entire course followed from beginning at the main stem to the apex. Coronary anatomy and pathology (arteriosclerotic plaque, stenosis, occlusion, and calcification) (Fig 2)
and side branches were identified in all hearts. Septal perforators 0.4 mm or more were present in all four hearts. The results are summarized in Table 2.

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Fig 2. A 10-MHz B-mode image of atherosclerotic changes in human left anterior descending coronary artery in vitro. Arrows: (1) perforating side branch, (2) atheroma in near wall, (3) calcified plaque in near wall.
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Comment
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Ultrasound transducer developments have led to a commercially available mini-probe that passes through an 11-mm port. In addition, the probe fits in between the suction pods of the Octopus stabilizer allowing easy scanning of the coronary artery. Without stabilization, porcine coronary vessels could be located quite easily with color-Doppler mode being helpful. To evaluate the anatomy and pathology of the vessel closely, on the other hand, adequate stabilization is required to obtain good images. The probes image quality at least matched the performance of much larger transducers that were used more than a decade ago to establish the potential diagnostic value of epicardial ultrasound. The present findings confirm the pioneering work from the 1980s and 1990s [28, 1113] and report the added value of color Doppler in localizing septal perforators and IMA side branches. The development of this miniprobe has created a new intraoperative diagnostic modality during beating-heart coronary surgery that will aid in determining the intramyocardial course of the coronary artery, its side branches and septal perforators, its pathologic characteristics (plaque, calcifications, and distal outflow stenosis), as well as the quality of the anastomosis intraoperatively. The present study focused on the LAD, but satisfactory images were also obtained when we scanned the right coronary and circumflex vessels in two open chest animals and in two postmortem human hearts.
In three respects, epicardial ultrasound deserves renewed attention. First, in beating heart coronary surgery, epicardial ultrasound was capable of detecting septal perforators as small as 0.4 mm in diameter. Avoiding septal perforators in the vicinity of the arteriotomy will reduce the risk of profuse retrograde bleeding, which obscures the view on the arteriotomy edges. Second, the more challenging task of anastomosis construction on the beating heart has revived the need for intraoperative assessment of anastomosis quality before chest closure. The potential of 20 MHz ultrasound to visualize an anastomosis accurately and to detect technical defects [2] is illustrated in Figure 3. Third, in endoscopic coronary surgery on the beating heart, tactile feedback is absent. Epicardial ultrasound will aid in finding the proper anastomotic site, with little coronary pathology, and without septal perforator nearby. In these procedures in particular, torrents of blood from the arteriotomy will create an obstacle to meticulous anastomosis suturing. Guiding the endoscopic choice of arteriotomy site by ultrasound is likely to aid in avoiding this obstacle.

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Fig 3. A 20-MHz annular array B-mode image of an optimal left internal mammary artery (lima) left anterior descending coronary artery (lad) anastomosis in the pig.
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In summary, a newly developed 10-MHz ultrasound mini-transducer that fitted in between the suction pods of a cardiac stabilizer and passed an 11-mm port showed promise as a diagnostic tool in both open and closed chest coronary procedures on the beating heart.
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Acknowledgments
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The authors acknowledge the contribution of John Dries and colleagues of the Utrecht University Central Animal Facilities. The ultrasound equipment was kindly provided by Biomedic B.V., The Netherlands. We thank the Department of Functional Anatomy of the Utrecht University Medical Center and Rik Mansvelt Beck for their contributions to this study.
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