Ann Thorac Surg 2005;79:1805-1811
© 2005 The Society of Thoracic Surgeons
Review
Internal Thoracic Artery: To Skeletonize or Not to Skeletonize?
Shahzad G. Raja, MRCSa,*,
Gilles D. Dreyfus, MD, PhDb
a Department of Cardiac Surgery, Alder Hey Hospital, Liverpool, United Kingdom
b Department of Cardiac Surgery, Harefield Hospital, London, United Kingdom
Accepted for publication May 18, 2004.
* Address reprint requests to Dr Raja, Department of Cardiac Surgery, Alder Hey Hospital, Eaton Rd, Liverpool, L12 2AP UK (E-mail: drrajashahzad{at}hotmail.com).
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Abstract
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The internal thoracic artery has been the most reliable graft material used in coronary artery bypass grafting with an excellent long-term patency rate. Complete myocardial revascularization with internal thoracic arteries improves long-term survival and decreases the rate of repeat operations compared with vein grafts. Adequate length of the graft in coronary artery bypass graft surgery is essential for providing complete arterial revascularization. In the last decade or so, technique of skeletonization of internal thoracic artery has been proposed to achieve extra length. Skeletonization of the internal thoracic artery allows the preparation of longer conduits with a superior free flow and can reduce the incidence of postoperative pulmonary and sternal complications. However, concerns about vasoreactivity of skeletonized internal thoracic artery grafts, the functional consequences of surgical trauma, the possible loss of innervation, and vasa vasorum perfusion in the skeletonized conduits have prevented this technique from being universally accepted. Presently available evidence from retrospective studies (level 3 evidence) suggests that skeletonization is a safe and effective technique for myocardial revascularization. However, there is a need for conducting multicenter, randomized controlled trials comparing the skeletonized and pedicled internal thoracic arteries with special emphasis on long-term patency to conclusively validate the safety and efficacy of skeletonization technique.
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Introduction
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The effectiveness of the internal thoracic artery (ITA) for coronary artery bypass grafting (CABG) is well established [1–4]. It has been postulated that long-term cardiac protection is provided only by arterial grafts, whereas venous conduits undergo pathophysiologic and clinical deterioration that is similar to that from the native coronary disease [3]. Comparative studies have demonstrated that internal thoracic arteries possess improved resistance to the development of arteriosclerosis, intimal hyperplasia, and medial calcification [5, 6]. Recent evidence indicates that bilateral ITA grafting further improves survival and reduces the need for repeat revascularization [7, 8]. Internal thoracic artery grafting is particularly important for patients with diabetes because survival is significantly higher in patients with diabetes after CABG compared with percutaneous transluminal angioplasty [9]. Furthermore, the higher survival in the patients with diabetes after CABG was limited to patients who received ITA grafts. Patients with diabetes represent a subgroup of those who could potentially derive the greatest benefit from bilateral ITA grafting. Unfortunately this technique is limited by the increased risk of deep sternal wound infection associated with conventional pedicled ITA harvesting [10]. Indeed, diabetes is a well-recognized risk factor for sternal infection even in patients receiving a single ITA graft [10, 11]. Pedicled harvesting of both ITA grafts may impair sternal wound healing by decreasing sternal blood flow, resulting in an increased risk of sternal wound infection and dehiscence [12, 13].
Recently skeletonization of the internal thoracic artery (a technique pioneered by Sauvage and colleagues [14]) has been advocated to decrease the occurrence of sternal wound infections and increase the number of arterial anastomoses [13, 15, 16]. Skeletonization involves meticulous dissection of the ITA conduit away from the chest wall with preservation of the collateral sternal blood supply and the internal thoracic veins. On the other hand, when skeletonized, the vessel loses its "milieu," which theoretically may adversely affect its long-term resistance to arteriosclerosis. This coupled with the lack of long-term patency studies of the skeletonized ITA and meticulous follow-up and confirmation by angiography raises concerns about whether this technique sacrifices the superior longevity of the conduit. In this review we evaluate the available evidence on the advantages and disadvantages of skeletonization of internal thoracic artery.
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Search Methodology
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The scientific literature of the English language was reviewed primarily by searching MEDLINE from 1966 through March 2004 using the OVID interface [17]. Key words used in the search included skeletonized, pedicled, internal thoracic artery, internal mammary artery, conduits, grafts, and harvesting techniques. The reference lists of articles found through these searches were also reviewed for relevant articles. In addition, links on web sites containing published articles were searched for relevant information. The authors for this article chose studies relevant to the discussion. The search was done in stages to achieve high-sensitivity search strategy (ie, it has the highest likelihood of retrieving all relevant articles). Similar search terms were combined using the Boolean operator term "or" to find all abstracts that contained information about a particular search term. These individual terms were then combined using the Boolean operator term "and" to find articles that contained information of all the search terms. This is a well-recognized method for performing sensitive searches and has been described in detail in the British Medical Journal [18].
The articles found by the search strategy were then appraised. The appraisal of each article was performed in a structured format using critical appraisal checklists. These are widely available in several formats and aid in assessing the article for methodological and analytical soundness and to help uncover any significant methodological flaws [19]. In addition, after appraisal, the article was categorized in terms of study type and level of evidence presented [20]. The levels of evidence are presented in Table 1 and enable readers of the article to come to a conclusion about the certainty to which evidence exists to answer the question.
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Skeletonization and Incidence of Sternal Wound Infection
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Three major studies [21–23] have identified the use of bilateral ITAs as a significant risk factor for sternal dehiscence and mediastinal wound infection. Because each hemi-sternum loses >90% of its blood supply upon mobilization of the corresponding ITA [12, 24], it is not surprising that wound healing can be compromised in patients after concomitant mobilization of both the left and right ITAs [25].
Sternal ischemia after mobilization of one or two ITAs was well documented in a study by Carrier and associates [26] who performed sternal bone tomography at 1 week and 4 weeks after median sternotomy in 67 patients. At 1 week, ITA dissection caused significant sternal ischemia that was more marked in patients who had bilateral ITA harvesting. These changes were less pronounced 1 month after operation, probably because of the development of vascular collateral vessels. Deep sternal wound infection is a dreaded complication that portends an increased risk of morbidity and death [27]. Patients who have deep sternal infection have a threefold increase in intensive care unit and hospital length of stay, as well as a threefold increase in mortality [11].
However, skeletonization of ITA conduits results in less reduction of sternal blood flow [13, 15]. Anatomic studies reveal that the sternal and anterior intercostal branches of the ITA originate either directly or as a common trunk from the ITA [28]. Substantial collateral blood flow to the sternum can be maintained in the absence of the ITA, provided the sternal-anterior intercostal trunk is left intact. Skeletonization of the ITA often results in preservation of this common trunk, particularly if meticulous dissection is performed [29].
In a recently published study, Peterson and colleagues [29] confirmed an unacceptably high prevalence of deep sternal wound infection in patients with diabetes (11.1%) receiving pedicled bilateral ITA grafts. Skeletonization of both conduits resulted in a significantly lower prevalence of deep sternal infection (1.2%) that was comparable with rates in patients without diabetes (1.6%). The prevalence of any sternal infection (superficial or deep) was also significantly lower in patients in the skeletonized group. They concluded that skeletonization allows safe application of bilateral ITA grafting in patients with diabetes, a finding that has been demonstrated by others [30–34]. Table 2 summarizes the impact of skeletonization of internal thoracic arteries on the incidence of sternal wound infection.
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Skeletonization and Length of Internal Thoracic Artery
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The use of skeletonized ITAs allows the use of both ITAs as grafts to practically all coronary vessels requiring surgical revascularization, thus obtaining complete arterial revascularization [35]. The pedicled right internal thoracic artery (RITA) is less useful than the left internal thoracic artery (LITA), as it will not always reach the right coronary artery branches without tension, leading to its use predominantly as a free graft with a lower patency rate when attached to the ascending aorta [36]. Skeletonization bestows the advantage of extra length [37], which permits composite arterial grafting. Connecting the skeletonized free RITA end-to-side to the skeletonized LITA as a T graft or end-to-end as a tandem–sequential graft locates the RITA 10 or more cm closer to the coronary arteries on the inferior and posterior surface of the heart [38]. Combining the T graft or tandem–sequential graft with sequential grafting makes it possible for most patients to undergo bypass with purely ITA grafts [38]. The coronary arteries on the anterior surface of the heart are mostly bypassed with the LITA, and the arteries on the posterior and inferior areas are grafted with the RITA. The most important coronary artery in nearly all patients, the left anterior descending artery, is always bypassed with the graft having the greatest proved patency (ie, the attached LITA). A separate harvesting incision and an aortic anastomosis are not needed. In addition, the bypass conduits are placed out of the way of re-entry and are well protected from injury in case the patient needs a repeat sternal incision. Thus, skeletonization allows the use of only two arterial grafts and avoidance of the harvesting of multiple conduits, thereby reducing the morbidity of the operation [38].
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Skeletonization and Internal Thoracic Artery Flow
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Takami and Ima [39] used quantitative coronary angiography with an edge detection algorithm and transit-time graft flow measurement to show that complete ITA skeletonization results in increased graft diameter for the anastomosis, thereby improving graft flow in CABG. Similar findings were reported by Choi and Lee [40] and Wendler and colleagues [41]. An anastomosis with a larger diameter and decrease in graft vascular resistance secondary to skeletonization are factors that may prevent the hypoperfusion syndrome in CABG using ITA. This syndrome is a rare but life-threatening perioperative clinical syndrome manifested by low cardiac output, left ventricular failure, and cardiac arrest [42, 43]. The major contributory factor to ITA hypoperfusion is a disproportion between ITA flow and myocardial demand because of the small ITA size, overzealous use of sequential grafting, and severe left ventricular hypertrophy. Considering the current wide use of ITAs, including sequential and bilateral, ITA skeletonization may be an efficient strategy to prevent perioperative hypoperfusion syndrome, especially in off-pump CABG without assisted circulation [44].
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Additional Benefits of Skeletonization
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Skeletonization also allows visual inspection of the vessel to identify any injury, which if unnoticed may jeopardize the long-term outcome [45]. Another potential benefit of skeletonization is decreased postoperative chest wall pain. Intercostal nerve damage occurs frequently after pedicled ITA harvesting [46]. In one study, three quarters of patients who underwent coronary bypass showed evidence of intercostal nerve damage after pedicled harvesting, and 15% of these patients experienced persistent postoperative pain [47]. The anterior branch of the intercostal nerve is avoided during skeletonized harvesting, which may in turn decrease the frequency and severity of postoperative chronic chest wall pain [29].
Skeletonization has been shown to be associated with a lower prevalence of low cardiac output syndrome and intraaortic balloon use than the use of pedicled grafts [29]. Improvement in early cardiac outcomes may relate to the increased conduit diameter and blood flow reported in skeletonized compared with pedicled grafts [39, 48]. Peterson and colleagues [29] also showed that patients who received skeletonized grafts had lower red blood cell transfusion requirements. This is attributed to the meticulous dissection and hemostasis that is necessary during skeletonization. Their study also revealed that patients who received skeletonized grafts had shorter ventilation times, shorter intensive care unit stays, and shorter hospital stays than patients who received pedicled grafts [29]. However, skeletonization per se was not the only reason for this improvement as "fast-tracking" protocols were implemented in their institution at about the same time as the skeletonization technique was adopted.
Finally, complete arterial revascularization with the skeletonized ITAs as the sole source of blood supply for CABG to eliminate manipulation of the aorta, when there is atheromatous plaque (the "no-touch" technique), can potentially reduce the incidence of stroke.
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Skeletonization and Concerns About the Functional Integrity of Internal Thoracic Artery Grafts
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Despite the advantages of increased available graft length, greater blood flow in the early postoperative period, and less invasion of the chest wall, dissection of the ITA with the skeletonization technique may theoretically induce mechanical and physical damage to the vessel wall, loss of the vasa vasorum (which may cause ischemia in the outer layer of the media), and loss of the draining vein (which may induce stasis and edema in the vessel wall). These phenomena may result in detrimental effects on the functional integrity of the ITA [49].
The wall of the ITA is more resistant to arteriosclerosis than the wall of the venous conduit, because of differences in muscular layers and in the lamina elastica interna [50]. In free harvested vein grafts, endothelium lost to sloughing (in both human beings and experimental animals) requires up to 3 months to be re-populated by blood elements [51]. Furthermore, the degree of subendothelial hypertrophy appears to be related to the number of vasa vasorum of the vein wall [52, 53]. Long-term changes due to the lack of vasa vasorum are likely to take longer in the ITA than in the in situ saphenous vein graft because other factors are involved. Theoretically there is a higher risk of damaging an ITA during skeletonization than in preparing a pedicled graft, especially in regard to intraluminal hematoma. If the ITA is partially denuded of the adventitia and its vasa vasorum during skeletonization, patchy areas of degeneration may develop [50].
Noera and colleagues [54] showed blood effusion in the adventitia of the skeletonized ITA. Gaudino and colleagues [55] showed intraluminal microthrombus formation and preservation of the endothelium in the skeletonized ITA by immunohistochemical staining with antifactor VIII (von Willebrand factor antibody). Deja and colleague [48] also demonstrated that skeletonization did not damage endothelial function in their dose-effect relationship study on relaxation induced by acetylcholine. In a canine model, Sasajima and colleagues [56] showed that skeletonization was not detrimental to the structural integrity of the ITA. In another study using canine models and immunohistochemical techniques to evaluate the effects of skeletonization on the functional integrity of the ITA, it was shown that the loss of the vasa vasorum did not induce ischemia or remodel the media and neovascularization in the adventitia was just a change secondary to adhesion that did not induce proliferation of the smooth muscle cells in the media after intimal hyperplasia shown in the atherosclerogenesis process [49]. Furthermore, quantitative analyses with immunohistochemical staining of von Willebrand factor and endothelial nitric oxide synthase showed that the structural and functional integrity of the endothelial cells in skeletonized ITAs was similar to that of pedicled ITAs at both study periods. Therefore, although neovascularization of the vasa vasorum could occur after dissection, skeletonization did not induce ischemia or inflammation of the media, and the structural and functional integrity of the endothelial cells was maintained.
In a recently published clinical study using a scanning electron microscope, Yoshikai and colleagues [57] confirmed the findings of Higami and colleagues [58] that ITAs skeletonized with an ultrasonic scalpel did not show any endothelial cell injury. Hence, skeletonization per se does not have detrimental effects on the structural and functional integrity of ITAs provided physical damage caused by surgical manipulation is avoided.
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Skeletonization and Concerns About Vasoreactive Profile of Internal Thoracic Artery Grafts
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The adventitia of the ITA has sympathetic unmyelinated fibers from the autonomic nervous system that supply the muscular layers [50]. These nerve endings release a variety of vasoactive agents [59]. These vasoactive agents along with potent vasodilators, such as the endothelium-derived relaxing factor (now called nitric oxide or NO) [60, 61], prostacyclin, and endothelium-derived hyperpolarizing factor, or with vasoconstrictors such as endothelin-1 [62] regulate the arterial tone. Concerns have been raised that the ITA loses its ability to autoregulate flow when skeletonized [50]. However, in a recently published study Gaudino and colleagues [63] have shown that skeletonized thoracic grafts have a vasoreactive profile that is not different from that of the criterion standard pedicled ITA, even in the early postoperative period (when the effect of the surgical trauma and denervation should be maximal). In fact, skeletonized grafts showed a contractile response to endovascular serotonin infusion similar to that of pedicled ITAs with a comparable vasodilatory reserve. Their data are concordant with the observations of Kushwaha and colleagues [64] who found no difference in the endothelial function of the free versus in situ ITA graft, showing how denervation and loss of vasa vasorum and lymphatics do not affect ITA vasoreactivity (at least in the long term).
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Skeletonization and Concerns about Patency of Internal Thoracic Artery Grafts
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The skeletonized ITA has not been used long enough to establish whether a decline in patency will occur after several years. However, available patency studies [16, 65–67] as shown in Table 3 have yielded very encouraging results. Hirose and colleagues [66] have compared the quality of skeletonized and pedicled ITAs by angiographic control in a retrospective analysis of their practice to use bilateral ITAs in diabetic patients. They performed angiographies in 87 patients (75.7%) with skeletonized ITAs (group S; n = 115) and 36 patients with pedicled ITAs (group P; n = 99) before discharge from the hospital after first time isolated CABG. This allowed them to evaluate 100 anastomoses of the LITA and 95 anastomoses of the RITA in group S, and 39 anastomoses of the LITA and 38 anastomoses of the RITA in group P. There were no ITA occlusions in either group. A string sign (diffuse narrowing of the graft) was observed in two in group P, but none in group S. Similarly, Kim and colleagues [16] in their comparison of the early results of off-pump coronary artery bypass surgery using skeletonized bilateral ITAs as Y grafts (group I; n = 113) and in situ bilateral ITAs grafts (group II; n = 110) performed postoperative coronary angiographies in 110 patients in group I and 108 patients in group II. Their findings revealed 99.0% (382 of 386) overall patency and 99.4% (319 of 321) patency for distal anastomoses using ITAs in group I, and 98.1% (312 of 318) overall patency and 98.1% (258 of 263) patency for distal anastomoses using ITA in group II. The findings of these studies suggest that skeletonization does not adversely affect the patency of ITA grafts, although the long-term results remain unknown at this point.
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Other Drawbacks
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Technically skeletonization may be more demanding than pedicled ITA harvesting, and skeletonization has a definite learning curve. Peterson and colleagues [29] found an insignificant 15-minute increase in operating times for patients undergoing skeletonization. Another potential drawback of skeletonization is that it is a relatively new surgical technique; therefore there is no current data on long-term patency rates. However, it is unlikely that long-term patency rates will be worse than for pedicled ITA grafts.
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Conclusion
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Skeletonization of internal thoracic arteries with its proven advantages of decreased incidence of sternal wound infection, greater length, and multiple arterial anastomoses appears to be an attractive technique for myocardial revascularization. Speculations about worse long-term patency rates have not been substantiated by retrospective comparative studies. In an era of evidence-based medicine, there is no denying the fact that multi-institutional, randomized controlled trials comparing the skeletonized and pedicled ITA techniques with respect to long-term patency must be conducted with complete or near-complete angiographic and freedom-from-reintervention data to conclusively prove the true superiority of the skeletonization technique. However, until such prospective, randomized studies of pedicled versus skeletonized ITA grafts are conducted, with follow-up periods of 15 to 20 years, available evidence suggests that skeletonization does not adversely affect patency and justifies the use of skeletonized ITAs for myocardial revascularization.
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J. Shi, T. Iesaki, N. Kubota, K. Sumiyoshi, K. Kajimoto, K. Kikuchi, H. Daida, and A. Amano
Skeletonization with an ultrasonic scalpel is as safe as a non-skeletonized dissection in preserving the endothelial function of the human gastroepiploic artery
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M. Gwozdziewicz
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S. J. Durham and J. P. Gold
Late Complications of Cardiac Surgery
Card. Surg. Adult,
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E. Gongora and T. M. Sundt III
Myocardial Revascularization with Cardiopulmonary Bypass
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F. Onorati, A. Esposito, F. Pezzo, A. di Virgilio, P. Mastroroberto, and A. Renzulli
Hospital Outcome Analysis After Different Techniques of Left Internal Mammary Grafts Harvesting
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S. G. Raja and G. D. Dreyfus
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Top
Abstract
Introduction
