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Interact CardioVasc Thorac Surg 2009;8:216-220. doi:10.1510/icvts.2008.186262 © 2009 European Association of Cardio-Thoracic Surgery
Skeletonization with an ultrasonic scalpel is as safe as a non-skeletonized dissection in preserving the endothelial function of the human gastroepiploic artery
a Department of Cardiovascular Surgery, Juntendo University School of Medicine, Tokyo, Japan Received 15 June 2008; received in revised form 15 October 2008; accepted 16 October 2008
*Corresponding author. Department of Physiology, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyo-ku, Tokyo 113-8421, Japan. Tel.: +81-3-5802-1029; fax: +81-3-3813-1609.
The right gastroepiploic artery (GEA) is frequently used as another in situ artery, other than the internal thoracic artery (ITA) in coronary artery bypass grafting (CABG). Skeletonizing the graft with an ultrasonic scalpel is now regarded as a useful technique; however, this technique may damage the endothelial function during harvesting the graft resulting in postoperative graft stenosis or occlusion. In the present study, GEA segments from nine patients were excised in both a skeletonized and non-skeletonized manner with an ultrasonic scalpel, and then were transported to the laboratory. The vessels were trimmed as rings, and were allotted to the group of skeletonized or non-skeletonized, accordingly. The force development in response to 1 µmol/l norepinephrine did not differ between the skeletonized and non-skeletonized groups. Endothelium-dependent relaxation induced by either acetylcholine or bradykinin was not impaired in the skeletonized group in comparison to the non-skeletonized group. No significant difference was observed in endothelium-independent relaxation elicited by sodium nitroprusside. Therefore, the skeletonization of the GEA with an ultrasonic scalpel was thus found to be as safe as a non-skeletonized dissection in preserving the vascular contractile ability or endothelium-dependent and -independent relaxation of the graft.
Key Words: Ultrasonic scalpel; Skeletonization; Endothelial function; Gastroepiploic artery
It has been an unremitting aim to develop a dependable method to mobilize the arterial conduits in myocardial revascularization, because this relates very closely with postoperative long-term patency. Skeletonization has been increasingly used for the dissection of arterial grafts during revascularization procedures, and there are some reports which have shown the advantages of using the ultrasonic scalpel during graft harvesting [1, 2]. The skeletonization of these arterial conduits has been shown to have substantial benefit in clinical practice [3]; it provides a fast and safe procedure, a spasm free graft, and less need for hemostatic clips. However, skeletonizing the graft with an ultrasonic scalpel might also be associated with a risk of endothelial injury, which is likely caused by either thermal or vibratile energy. Endothelial damage can promote a series of detrimental reactions, eventually leading to the short or long-term development of graft stenosis or occlusion [4, 5]. Therefore, the question still arises as to whether skeletonization with this device causes a detrimental effect to the endothelial functions of the grafts. The skeletonization method is routinely employed in coronary artery bypass grafting (CABG) to harvest arterial conduits in our institution. The right gastroepiploic artery (GEA) is another qualified arterial graft in addition to the internal thoracic artery (ITA), and was reported to have satisfactory graft patency [6]. In the present study, we examined the vascular contractile and relaxant responses of an ultrasonically skeletonized GEA and a non-skeletonized one obtained from the same patient to investigate whether skeletonization with an ultrasonic scalpel damages endothelial function by an ex vivo vascular tone experiment.
Nine patients who underwent CABG using GEA from 5 April 2007 to 29 May 2007 in Juntendo University Hospital were included in this study. The candidates consisted of patients who needed surgical revascularization of the right coronary artery. Patients having a calcified aorta, an increased risk for saphenous vein graft disease such as diabetes mellitus, or a small caliber of native coronary artery were more likely to receive GEA as an arterial conduit. The details of the patient characteristics are described in Table 1. This study was approved by our local Human Ethics Committee and written informed consent was obtained from each patient.
2.1. Operative technique The CABG procedure was performed in a standard fashion with an off-pump CABG technique. After performing a standard median sternotomy followed by extension to the peritoneum, the GEA was harvested in both a skeletonized and non-skeletonized manner with an ultrasonic scalpel (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH) by the quick touch method. Briefly, while gently pulling up the vessel loops, the greater omentum was divided about 1 mm away from the GEA trunk and the tip of the blade was kept at least 1 mm away from the trunk to divide the branches. During skeletonization, care was taken to ensure that the ultrasonic scalpel did not make contact with the GEA for more than 0.2 s. For the non-skeletonized GEA harvesting, the omentum around the terminal 1.2 cm portion of the GEA was incised with the ultrasonic scalpel along both sides approximately 1 cm away from the GEA trunk. Then, a 3 cm-long segment including both the skeletonized and non-skeketonized portions was cut off from the distal end of the GEA. The non-skeletonized harvest was always performed at the most terminal end of the GEA adjacent to skeletonized portion, and there was no apparent difference in the diameters between them. 2.2. Measurement of changes in force in GEA Immediately after dissection, the GEA segments were placed into cold Krebs-HEPES (25 mmol/l) buffer (pH 7.4) and transferred to the laboratory. All samples were investigated on the same day. Each vessel segment was separated from the skeletonized and non-skeletonized portion, cleaned of surrounding connective tissue and fat, and then cut into rings about 3–4 mm in length for the measurement of changes in force. Care was taken not to touch the endothelial surface to preserve the functional endothelium. The techniques used to measure changes in force in oxygenated Krebs bicarbonate buffer (37 °C) were adapted from previously described methods [7]. Briefly, the arterial rings were mounted on wire hooks attached to force displacement transducers (Nihon Kohden, Tokyo) for measurement of the changes in isometric force on a polygraph (Rikadenki, Tokyo). The rings were incubated in individually thermostated (37 °C) 10-ml baths for 120 min at an optimal passive tension of 5 g in Krebs bicarbonate buffer (pH 7.4) containing the following (in mmol/l): 118 NaCl, 4.7 KCl, 1.5 CaCl2, 25 NaHCO3, 1.1 MgSO4, 1.2 KH2PO4, and 5.6 glucose, gassed with 21% O2–5% CO2 (balance N2).The vessels were initially contracted with norepinephrine (NE, 1 µmol/l) and once a steady-state level of contraction was observed, either acetylcholine (ACh, 1 nmol/l to 10 µmol/l) or bradykinin (BK, 0.1 nmol/l to 1 µmol/l) was applied cumulatively to evaluate the endothelium-dependent relaxation. At least two vessel rings from both the skeletonized and non-skeletonized portion were obtained from one isolated GEA segment, and were assigned to either ACh or BK group. At the end of the ACh- or BK-induced relaxation study, the vessels were washed with fresh Krebs bicarbonate buffer and then allowed to reequilibrate for 30 min. In the next series of experiments, the vessels were precontracted with 1 µmol/l NE again and the endothelium-independent relaxation elicited by a cumulative dose of sodium nitroprusside (SNP, 0.1 nmol/l to 10 µmol/l) was examined. Relaxation was expressed by the percentage change of the steady-state level of the NE-induced contraction. The results are expressed as the means±S.E.M., with n equal to the number of vessels examined. Comparisons between groups were made using Student's unpaired t-test or two-way ANOVA with Bonferroni's correction. A P<0.05 was considered to indicate statistical significance.
The maximum force development evoked by 1 µmol/l NE did not differ significantly between the non-skeketonized and skeletonized groups either in the ACh- or BK-relaxed groups (Fig. 1); 8.2±1.0 g in the non-skeketonized, ACh group (n=11) vs. 7.4±0.7 g in the skeletonized, ACh group (n=11, P=0.5131), and, 6.6±0.8 g in the non-skeketonized, BK group (n=9) vs. 7.2±0.7 g in the skeletonized, BK group (n=10, P=0.5666).
Fig. 2 shows the endothelium-dependent vascular relaxation elicited by either ACh or BK. There was no significant difference between the non-skeketonized (n=14) and skeletonized (n=12) groups in ACh relaxation (P=0.8597), or between non-skeketonized (n=9) and skeletonized (n=10) groups in BK relaxation (P=0.9556).
The subsequent endothelium-independent relaxation caused by SNP in either the ACh group or BK group are shown in Fig. 3. There was no significant difference between the non-skeketonized (n=14) and skeletonized (n=14) groups in ACh group (P=0.1027) or non-skeketonized (n=8) and skeletonized (n=8) groups in BK group (P=0.7271).
This is the first study that directly compared the endothelial function of ultrasonically skeltonized GEA with that of a non-skeketonized one by use of the same vessel segment obtained from the same patient. We showed equal vascular contractility and equal endothelium-dependent and -independent vasorelaxant responses. The ultrasonic scalpel was introduced into clinical surgical use in 1987 and has been increasingly applied, because it provides an easy, safe, and efficient procedure in the dissection of arterial conduits in CABG [8]. Since Gagliardotto et al. first documented skeletonization of the GEA in myocardial revascularization [9], this useful technique was certified with many proven advantages over the pedicled methods [10, 11]. Despite the advantages, the complex surgical manipulation in skeletonization of the graft may jeopardize the functional integrity of the conduit. Vessel damage by either thermal or vibratile energy of the ultrasonic scalpel is a major reason cited for not employing the skeletonized method in harvesting the grafts. Rukosujew et al. reported that skeletonization with an ultrasonic scalpel was more harmful to the endothelial integrity of the conduits in comparison to the conventional pedicled method [12]. As the endothelium plays a vital protective role by releasing endothelium-derived relaxing factor (EDRF), a potent vasodilator and inhibitor of platelet aggregation, endothelial damage can promote the atherosclerotic process, leading to the early or late failure of the graft [4, 5]. There have been many concerns expressed in regard to the possible detrimental effect of skeletonization on the endothelial integrity and function [13]. Fukata et al. reported that the thermal degeneration was limited to the surrounding connective tissue and that the media or intima of the vessel wall was not affected by the ultrasonic scalpel [14]. They showed that the ultrasonic scalpel-induced vessel damage is avoidable by setting it at an appropriate level of energy and by using a quick touch method. Because most of these studies have focused on the endothelial integrity of the ITA, we investigated the endothelial function of ultrasonically skeletonized human GEA by an ex vivo vascular tone experiment. Acetylcholine-induced vascular relaxation is one of the established methods in the detection of functional endothelial damage [15]. In the present study, we also used BK, another endothelium-dependent vasorelaxant, to evaluate endothelial function. We did not find any difference in the ACh- or BK-induced relaxation either in the skeletonized or non-skeketonized groups, which indicates that the endothelial function of the ultrasonically skeletonized human GEA was well-preserved. Matsumoto et al. reported that the endothelial function of the ultrasonically skeletonized vessels was evidently reduced in comparison to the pedicled one via an ex vivo vascular tone experiment [13]. They found that the rings from pedicled grafts showed greater relaxation responses to ACh than did the rings from the skeletonized grafts. This discrepancy between our results might be explained by differences in the sample group or by the differences in the graft harvesting process. One tough point in investigating the endothelial function in patients with coronary heart disease is that they are multiform groups with various factors, for example, diabetes mellitus, dyslipidemia, hypertension, smoking, etc. These factors may affect the endothelial function and make it difficult to pair the baseline among the different groups, thus resulting in the need for a very large number of samples to show statistical significance in this kind of study. In the present study, each paired skeletonized and non-skeletonized rings was taken from the same patient, which we believe eliminated the possible discrepancy from different individuals and gave the samples a consistent baseline. All arteries were taken meticulously by the same experienced surgeon who used the standard harvesting technique skillfully, which may diminish the surgical discrepancy. The number of specimens in our study was only nine, however, the small S.E.M. of our results enabled us to end our work at this point. An implicit limitation of this study is that we examined the endothelial function of only the distal portion of the graft. Therefore, in order to definitively conclude that skeletonization along the entire graft is similar to non-skeletonization with respect to endothelial function, further studies which address other parameters that may be affected by the graft harvesting technique, such as the in vivo graft flow and graft length, are needed. We concluded that skeletonization with an ultrasonic scalpel is as safe as a non-skeletonized dissection in preserving the contractile properties or endothelium-dependent and -independent relaxations of the GEA, while marked surgical damage when dissecting the grafts could thus be avoided by using this device in a careful manner. We therefore advocate the application of this convenient technique for harvesting the GEA graft in CABG, however, careful consideration should be made when selecting this modality in clinical practice, because this study is an ex vivo experiment and is not a concomitant in situ assessment of the vascular function.
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Abstract
1. Introduction
