Skeletonized and Pedicled Internal Thoracic Artery Grafts: Effect on Free Flow During Bypass
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1 Skeletonized and Pedicled Internal Thoracic Artery Grafts: Effect on Free Flow During Bypass Jong Bum Choi, MD, and Sam Youn Lee, MD Department of Thoracic and Cardiovascular Surgery, Wonkwang University School of Medicine, Iksan, South Korea Background. The skeletonization technique of the internal thoracic artery (ITA) is used as a dissection technique for myocardial revascularization procedures. This study compared free flow between skeletonized ITA grafts and ITA pedicled grafts. Methods. The ITA pedicled grafts were sprayed and wrapped in sponges soaked in dilute papaverine solution in 14 patients and prepared with intraluminal papaverine injection in 18 patients. For 23 other patients, the ITA was skeletonized. We measured the first free flow from the distal ITA early after the start of cardiopulmonary bypass and the second free flow just before the ITA was grafted to the left anterior descending artery. Results. The first flow was greater in the skeletonized ITAs than in the ITA pedicled grafts with topical application of papaverine alone ( versus ml/min; p < 0.001). For the second flow, the pedicle grafts with intraluminal papaverine injection and the skeletonized ITAs showed greater flow rate than the pedicled grafts with topical application of papaverine ( and versus ml/min; p < and p < 0.05, respectively), but there was no significant difference between the former two groups (p = 0.53). Conclusions. Skeletonization of the ITA is as efficient a strategy to increase the flow as intraluminal papaverine injection for the ITA pedicled graft. When the ITA is harvested in a skeletonized fashion, arterial spasm and reduced early flow can be avoided, even without intraluminal injection of papaverine. (Ann Thorac Surg 1996;61:909-13) he use of an internal thoracic artery (ITA) graft to the T left anterior descending coronary artery (LAD) is associated with superior patency rates and longer survival when compared with saphenous vein grafts [1-4]. The arterial conduit can be used as a pedicled, free graft, or skeletonized vessel. There is no doubt that the ITA graft obtained as a pedicle functions well in myocardial revascularization procedures [1-5]. Despite these excellent results, a skeletonization technique of ITA dissection was adopted by some surgeons because of its potential advantages [51. The dissection technique of ITA may effect a change in the graft flow capacity. The purpose of this study is to compare free flow between skeletonized ITA grafts and ITA pedicled grafts and to evaluate the effect of skeletonization technique on ITA flow. Patients and Methods This study comprised 55 patients who underwent harvesting of the ITA in preparation for coronary artery bypass grafting (Table 1). Only elective operations were included in the study. Patients who were in hemodynamically unstable condition or showed evidence of ischemia before cardiopulmonary bypass were excluded from the study. All patients were operated on by the same surgeon familiar with both pedicle and skeletonization techniques of ITA harvesting. The patients were divided into Accepted for publication Nov 15, Address reprint requests to Dr Choi, Department of Thoracic and Cardiovascular Surgery, Wonkwang University School of Medicine, Sinyong-dong, Iksan, leonbuk, , South Korea. three groups by the techniques used for preparation of the ITA. Measurements of ITA Flow In 55 patients undergoing ITA graft operations, the left ITA was mobilized as a pedicle or skeletonized vessel. Standard cardiopulmonary bypass with moderate hypothermia (28 C) was used in all cases. The blood flow through the ITAs (free flow) at zero distal resistance was measured at a mean arterial pressure of 50 to 55 mm Hg during cardiopulmonary bypass. Two to three measurements were made for 20 seconds each and averaged to calculate the blood flow per minute. The luminal diameter of the distal ITA was measured with a calibrated probe, just before its anastomosis to the LAD. GROUP I. Fourteen consecutive patients (12 men and 2 women) underwent a takedown of the left ITA with a wide pedicle (2 cm) in preparation for coronary bypass grafting. Body surface areas ranged from 1.46 to 1.84 m 2, with an average area of 1.69 m 2. The ITA was harvested from the subclavian vein superiorly to beyond the ITA bifurcation inferiorly and was transected only after the institution of cardiopulmonary bypass. Dilute papaverine (60 mg in 40 ml of lactated Ringer's solution) was sprayed on the ITA graft throughout its whole length with a small syringe and size 25 needle. The ITA pedicle was wrapped in a papaverine-soaked gauze, and it was set aside until cardiopulmonary bypass. The ITA was opened with fine scissors proximal to the bifurcation and at the point of the estimated locus for anastomosis to the 1996 by The Society of Thoracic Surgeons / Published by Elsevier Science Inc SSDI (95)
2 910 CHOI AND LEE Ann Thorac Surg SKELETONIZED ITA FLOW 1996;61: Table 1. Characteristics of Patients in the Three Study Groups ~ Variable Group I Group II Group II1 p Value Preparation Sex (M/F) Age (y) BSA (m 2) No. of distal anastomoses Pedicled graft Pedicled graft + intraluminal papaverine Skeletonized LITA 12/2 10/8 16/7 NS 54.6 ± ± (42-72) (50-65) (45-79) 1.69 ± NS ( ) ( ) ( ) ± _+ 0.7 NS (1-5) (2-6) (2-5) Value is the mean +_ the standard deviation with the range in parenthesis, or the number of patients. BSA body surface area; LITA left internal thoracic artery; NS not significant. LAD. Free flow was measured just before its anastomosis to the LAD [6]. For the remainder of the operation, a standard technique for coronary artery bypass grafting was used [7]. GROUP II. Eighteen patients (10 men and 8 women) had a takedown of ITA pedicle as in group I. Body surface areas ranged from 1.30 to 1.88 m 2, with a mean of 1.63 m 2. Dilute papaverine solution was sprayed on the ITA pedicle as in group I. The ITA was transected just proximal to its bifurcation after cardiopulmonary bypass was instituted and the first (early) free flow was measured at a mean arterial pressure of 50 to 55 mm Hg. A 22-gauge polytetrafluoroethylene catheter (BOC Ohmeda AB, Helsingborg, Sweden) was then introduced into the lumen of the distal ITA. Ten milliliters of dilute papaverine was injected intraluminally, and the pedicled graft was set aside during distal anastomoses of the vein grafts. The artery was allowed to dilate under the arterial pressure during the cardiopulmonary bypass, but hydrostatic (manual) or mechanical dilation was not performed. The second (final) free flow was recorded just before its anastomosis to the LAD. The papaverinedilated size of the ITA graft was also measured with a calibrated probe. GROUP III. In 23 patients (16 men and 7 women), the left ITA was harvested in a skeletonized fashion. Body surface areas ranged from 1.35 to 1.81 m 2, with an average of 1.62 m 2. The pleura was not opened and the ITA was harvested from its origin superiorly to beyond the ITA bifurcation inferiorly, by using the skeletonization technique [5]. The dissection of the ITA was made in large part with electrocautery, and the side branches were occluded with Ligaclips (Ethicon Ltd, Edinburgh, UK). The ITA was mobilized from the surrounding fat, veins, and endothoracic fascia. All mediastinal arterial branches including pericardicopleural artery were identified and divided. From the first intercostal space upward, the artery was freed without the use of cautery to avoid injury to the phrenic nerve. Although the skeletonized ITAs showed a marked spasm during dissection, especially in the lower portions, mechanical or hydrostatic dilation to overcome the spasm was not performed. Dilute papaverine was sprayed on the graft, but the graft was not wrapped in the papaverine-soaked gauze to avoid injury to the vessel. Instead, with adequate dilute papaverine solution the wall stayed moist. The ITA was transected distally just proximal to its bifurcation after cardiopulmonary bypass was instituted, and the first free flow was then measured as in group II. The graft was set aside during distal anastomoses of the vein grafts and was allowed to dilate under arterial pressure. After the completion of the distal anastomoses of vein grafts, the distal end of the ITA was prepared for anastomosis on the LAD, and then the second free flow was measured. Data Analysis Data were analyzed using the StatView software package (Abacus Concepts lnc, Berkeley, CA). Continuous data were expressed as the mean _+ standard deviation and compared by analysis of variance with Scheff6's F test and Student's t test. Statistical significance of differences between categoric parameters was evaluated by )(2 contingency analysis. A value of p less than 0.05 was considered statistically significant. Results The demographic data of the three groups are shown in Table 1. There was no significant difference found among the three groups with respect to body surface area and number of distal anastomoses. The skeletonization technique for ITA dissection was used more commonly in older patients (p = 0.012). No patient showed early detrimental effects related to dissection technique and graft preparation method. Flow and luminal diameter measurements of all three groups are shown in Table 2. The flow distribution in each group is displayed in Figure 1. The first flow rate was greater in the skeletonized ITA group than in the ITA pedicle group with topical application of papaverine alone (38.9 +_ 15.8 versus 18.0 _+ 6.8 ml/min; p < 0.001). The first flow rate of the skeletonized ITA group was similar to the second flow rate of the pedicle group with topical application of papaverine ( versus 38.1 _ ml/min; p = 0.87). In comparison of the second
3 Ann Thorac Surg CHOI AND LEE ;61: SKELETONIZED ITA FLOW flow among the three groups, the ITA pedicle group with intraluminal papaverine injection and the skeletonized ITA group showed greater flow rate than the ITA pedicle group with topical application of papaverine alone ( and versus ml/min; p and p < 0.05, respectively), but there was no significant difference between the former two groups (p = 0.53) (see Fig 1). In the skeletonized ITA group, there was also a significant increase in flow from the first flow to the second flow, even without any preparation ( versus ml/min; p < ), whereas it showed greater flow rate than the ITA pedicle group in the first flow measurement. All the distal ITAs in both the pedicle group with intraluminal papaverine injection and the skeletonized ITA group were greater than 1.5 mm in internal diameter at the site of arteriotomy for anastomosis, but in the pedicle group only with topical application of papaverine, 6 ITAs (43%) were less than 1.5 mm in internal diameter. Comment In the previous reports the free flow of ITA grafts was measured and compared just before [5, 8, 9] or during cardiopulmonary bypass [6]. The comparison of the ITA flow rates may be accurately made at a stable blood pressure, which could be obtained easily during cardiopulmonary bypass without use of inotropics or a vasodilator. Before cardiopulmonary bypass is instituted, the quality of the vessel should be ascertained by palpation of the pulse. In our series, the distal division of the ITA grafts was carried out after bypass was started, and the flow from the cut end was measured when the mean arterial pressure reached 50 to 55 mm Hg. This study showed an average flow of 38.1 ml/min in the ITA pedicled graft prepared only with topical application of papaverine via forceful spraying and wrapping Table 2. Flow and Cut End Diameter in the Three Groups of Left Internal Thoracic Artery Grafts" Variable Group I Group II Group III No. of patients Free flow (ml/min) First flow _ b (8-28) (24-56) Second flow 38.1 _ ± 25.5 c d (22-80) (27-125) (36-140) Luminal diameter of cut end (ram) ~ > a Value is the mean -+ the standard deviation with the range in parentheses, or the number of patients per group. The first flow rate of group II was measured in the internal thoracic arterial pedicle grafts with topical papaverine preparation alone, b p ~ 0.05 compared with the first flow of group II; c p ~ and d p ~ 0.05 compared with the second flow of group I. 140" 120.~ 100" E 80 ~" 60 0 m u. 40' 20' I ~ I, ** ~ r NS I T I II III T Group [] Firet Flow Second Flow Fig 1. Distribution of the free flow rates of left internal thoracic artery (ITA) grafts after three different preparations. Each bar represents the mean + the standard deviation of the mean. The first flow was greater in the skeletonized ITAs {group lid than in the ITA pedicled grafts with topical application of papaverine alone (group II). For the second flow, the skeletonized ITAs without any preparation (group lid showed flow rate similar to the pedicled grafts with intraluminal papaverine injection (group II). (*p < 0.05; **p K 0,005; NS = not significanl) with a soaked sponge. The flow rate is not acceptable for the LAD [6, 8]. The ITA pedicled graft may be still in residual spasm, causing the lesser flow. With intraluminal injection of dilute papaverine, the flow in the pedicled graft increased significantly during the distal anastomoses of vein grafts. Mills and Bringaze [8] reported many benefits of intraluminal administration of papaverine besides an increase in the ITA free flow. With a larger-diameter vessel to work with, the surgeon is less likely to make a technical error. Furthermore, potential bleeders from side branches can be readily identified. Although we have performed the intraluminal papaverine injection to increase the free flow of ITA pedicle grafts with few problems, we have been concerned about a possible adverse interaction between papaverine, which is a potent, acidic vasodilator, and the delicate, friable ITA intima. Recently, we have used the skeletonization technique for ITA dissection in the consecutive patients undergoing coronary bypass grafting. With the technique, only the ITA is teased away from the chest wall, accompanying veins, fascia, lymphatics, and adipose tissue [5, 10]. The vessels have a wall thickness of less than 500 /~m, being nourished entirely by luminal diffusion [10, 11]. There are no vasa in the media of a normal ITA. Therefore, careful skeletonization should not exert any detrimental effects on ITA viability [5, 10]. Excellent long-term results have been reported using both free and skeletonized ITA grafts [12, 13]. When preparing the skeletonized graft, we did not perform intraluminal papaverine injection or mechanical or hy-
4 912 CHOI AND LEE Ann Thorac Surg SKELETONIZED ITA FLOW 1996;61: drostatic dilation to identify the character of natural flow and to avoid injury to the intima. We used a so-called intraluminal no-touch technique in preparing the skeletonized graft. Our result confirms a previous observation that intraluminal papaverine preparation of the pedicled ITA offers the best flow to the myocardium with an improvement of the ITA size [8]. In our study, manual (hydrostatic) dilation was not performed in the pedicled or the skeletonized graft, and the flow was measured at a low mean arterial pressure of 50 to 55 mm Hg on cardiopulmonary bypass. In addition, the mean body surface area in our group of patients was much smaller when compared with patients in the previous studies [8, 9]. Therefore, average ITA flow rates might be expected to be lower in our patients because of their smaller size. In the present study, the early flow rate was greater in the skeletonized ITAs as compared with the pedicled grafts. In the skeletonization technique, the ITA is denuded of the perivascular tissue, which may limit the free flow. An absence of excessive perivascular tissue may allow topical papaverine to minimize spasm while awaiting cardiopulmonary bypass. Therefore, the skeletonized graft can provide sufficient early flow. Moreover, the skeletonized ITA dilates easily with time and shows an insignificant difference in the final flow when compared with the pedicled graft with the intraluminal papaverine injection. The luminal diameter at the prepared distal end of ITA was larger in the skeletonized ITA group than in the pedicle group with topical application of papaverine, although it was less than in the pedicled grafts with intraluminal papaverine injection. By skeletonizing the ITA, the artery is functionally lengthened [14]; therefore, the distal portion of the artery can be trimmed off to obtain a larger diameter with an optimal length. This allows resection of the muscular segment of the ITA and minimization of spasm [15]. This may be another factor providing the greater flow at the second measurement, especially in the skeletonized ITA grafts. In our series, however, a several-centimeter difference in distance above the ITA bifurcation site made little change in the free flow rate. From the first intercostal space upward, the artery was freed without the use of cautery to avoid injury of the phrenic nerve. After the division of the mediastinal arterial branches, the phrenic nerve is identified by bluntly dissecting the proximal mediastinal pleura off the mediastinal structures. O'Brien and associates [16] described a significant impairment of phrenic nerve function and perfusion in an adult swine model if the pericardicophrenic artery is divided during ITA harvesting. In our series, however, permanent or transient phrenic nerve paralysis did not occur. We have never seen direct cold trauma to the phrenic nerve since using cold lactated Ringer's solution instead of iced slush for topical cooling. We used the retractor adapter that was introduced by Brown and Dougenis [17] to dissect the ITA, and modified their pedicle technique. The endothoracic fascia and internal thoracic vessels are dissected away from the chest wall through a longitudinal incision that is made just medial to the internal thoracic artery and veins. The internal thoracic artery and veins are then freed from the inner surface of the fascia, using the tip of the cold cautery, and the ITA is skeletonized with the veins removed. The time required for dissection does not increase in comparison with the pedicle technique. The parietal pericardium is incised along its visceral reflection onto the transverse aortic arch, the bifurcation of the pulmonary artery, and the hilum of the left lung. The shortest pathway for descent of the left ITA is made behind the thymus [10, 17]. In summary, skeletonization of the ITA is as efficient a strategy to increase ITA flow as intraluminal papaverine injection for the pedicled graft. It also provides a reasonable diameter for its anastomosis to the LAD, even without intraluminal papaverine injection. These advantages may offset the slight increase in difficulty required to harvest the vessel. We gratefully acknowledge the assistance of Dr Sung Suk Yoon and Dr Kyung Sook Park in the preparation of the manuscript. References 1. Grondin CM, Campeau L, Lesperance J, Enjalbert M, Bourassa MG. Comparison of late changes in internal mammary and saphenous vein grafts in two consecutive series of patients 10 years after operation. Circulation 1984;70(Suppl 1): Sing RN, Sosa JA, Green GE. Long-term fate of the internal mammary artery and saphenous vein grafts. J Thorac Cardiovasc Surg 1983;86: Okies JE, Page US, Bigelow JC, Kraus AH, Salomon NW. The left internal mammary artery: the graft of choice. Circulation 1984;70(Suppl 1): Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal mammary artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314: Cunningham JM, Gharavi MA, Fardin R, Meek RA. Considerations in the skeletonization technique of internal thoracic artery dissection. Ann Thorac Surg 1992;54: Rankin JS, Newman GE, Bashore TM, et al. Clinical and angiographic assessment of complex mammary artery bypass grafting. J Thorac Cardiovasc Surg 1986;92: Mills NL, Rigby CS. Technique of coronary artery operations and reoperation. In: Baue AE, Geha AS, Hammond GL, Laks H, Naunheim KS, eds. Glenn's thoracic and cardiovascular surgery. Connecticut: Appleton & Lange, 1991: Mills NL, Bringaze WL III. Preparation of the internal mammary artery graft: which is the best method? J Thorac Cardiovasc Surg 1989;98: Sasson L, Cohen AJ, Hauptman E, Schachner A. Effect of topical vasodilators on internal mammary arteries. Ann Thorac Surg 1995;59: Sauvage LR. Extensive myocardial revascularization using only internal thoracic arteries for grafting the anterior descending, circumflex, and right systems. In: Myers WO, ed. Cardiac surgery. Philadelphia: Hanley & Belfus, 1992;6: Landymore RW, Chapman DM. Anatomical studies to support the expanded use of the internal mammary artery graft for myocardial revascularization. Ann Thorac Surg 1987;44: Galbut DL, Traad EA, Dorman MJ, et al. Seventeen-year
5 Ann Thorac Surg CHOI AND LEE ;61: SKELETONIZED ITA FLOW experience with bilateral internal mammary artery grafts. Ann Thorac Surg 1990;49: Barner HB, Standeven JW, Reese J. Twelve-year experience with internal mammary artery for coronary artery bypass. J Thorac Cardiovasc Surg 1985;90: Keeley SB. The skeletonized internal mammary artery. Ann Thorac Surg 1987;44: He G-W. Contractility of the human internal mammary artery at the distal section increases toward the end: empha- sis on not using the end of the internal mammary artery for grafting. J Thorac Cardiovasc Surg 1993;106: O'Brien JW, Johnson SH, VanSteyn SJ, et al. Effects of internal mammary dissection on phrenic nerve perfusion and function. Ann Thorac Surg 1991;52: Brown AH, Dougenis D. Dissection of the two internal mammary arteries with maximal exposure and minimal adverse sequelae by means of an inexpensive, simple, atraumatic retractor. J Thorac Cardiovasc Surg 1991;102: INVITED COMMENTARY Currently, one or more arterial conduits are used routinely in primary or secondary myocardial revascularization procedures. If the internal thoracic artery (ITA) is available, most cardiac surgeons dissect the vessel as a variable-width pedicle containing an assortment of venae comitantes, lymphatics, adipose tissue, muscle, and fascia. Topical or intraluminal papaverine solution is frequently used to minimize spasm and enhance ITA diameter and flow. Some surgeons, however, prefer ITA skeletonization as an alternate harvesting technique. Each method has its own inherent advantages and disadvantages, but both techniques provide excellent longterm results. In this report, Choi and Lee used both ITA procurement techniques and then compared free flow rates after initiating cardiopulmonary bypass. Skeletonized ITAs had higher initial flow rates than the pedicled ITAs and essentially the same preanastomosis flow rates as ITAs subjected to intraluminal papaverine. Choi and Lee concluded that "skeletonization of the ITA is as efficient a strategy to increase ITA flow as intraluminal papaverine injection for the pedicled graft." In the final analysis, both harvesting techniques produce satisfactory conduits with equivalent flow rates. Therefore, is there any reason to spend the extra prebypass time and effort required to skeletonize the ITA? Perhaps. If the ITA is going to be used for sequential grafting, side-to-side anastomoses are technically easier to construct if the ITA is skeletonized. Also, anastomoses can be done expeditiously because no further dissection of tissue surrounding the ITA is required. Additionally, a skeletonized ITA may provide more distal anastomotic options because it usually is longer and has a larger diameter than a pedicled ITA. Finally, if both ITAs are used in diabetic, obese, or pulmonary compromised patients, there is a definite increase in postoperative sternal wound infection. Previous reports suggest that the incidence of sternal wound infection may be decreased in these patients if the ITAs are skeletonized rather than dissected as pedicles. }ames M. Cunningham, MD Columbus Cardiothoracic and Vascular Surgical Associates 2522 Warm Springs Rd Columbus, GA 31904
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