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Ann Thorac Surg 1999;68:406-411
© 1999 The Society of Thoracic Surgeons

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Original Articles

Routine use of bilateral skeletonized internal mammary arteries for myocardial revascularization

^a Department of Thoracic and Cardiovascular Surgery, Tel Aviv Sourasky Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

Address reprint requests to Dr Mohr, Department of Thoracic and Cardiovascular Surgery, Tel Aviv Sourasky Medical Center, 6 Weizman St, Tel Aviv 64239, Israel

	Abstract

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Background. Complete arterial myocardial revascularization without the use of saphenous veins grafts was primarily performed on selected patient populations such as the young and nondiabetic. In a recently developed surgical technique, the internal mammary artery is dissected gently as a longer skeletonized artery, providing greater versatility for complete arterial revascularization, without saphenous veins grafts.

Methods. We prospectively evaluated the impact of the routine use of double skeletonized internal mammary artery in 472 patients who underwent coronary artery bypass grafting between April 1996 and June 1997. Their average age was 65 years (30 to 87 years), 383 (83%) were men, and 89 (17%) women. One hundred sixty-nine (36%) of the patients were older than 70 years, and 145 (31%) were diabetic. The average number of grafts was 3.2 per patient (two to six grafts).

Results. Operative mortality was 1.7% (n = 8). The mortality of urgent and elective patients was 0.7% (3 of 410 patients), and that of emergency operations was 8.1% (5 of 62 patients; p < 0.01). There were three (0.6%) perioperative infarcts, and 6 patients (1.3%) sustained strokes. Sternal wound infection occurred in 8 patients (1.7%). Postoperative follow-up (1 to 25 months) was available in 462 patients (99%). Two-year actuarial survival was 96.8%, and 92% of the surviving patients are well and free of angina. Neither diabetes mellitus nor old age (>70 years) were significant independent predictors of any early or late untoward events. None of the 70 diabetic patients more than 65 years of age developed sternal wound infection. Chronic lung disease was found to be the only independent predictor for sternal infections.

Conclusions. Routine use of bilateral skeletonized internal mammary artery is a safe replacement for the current myocardial revascularization technique even in the old and diabetic patients.

	Introduction

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The disappointing long-term results of saphenous vein grafts (SVG) in coronary artery bypass grafting (CABG) has increased the interest of cardiac surgeons in the use of multiple arterial grafts [1–3]. Two popular techniques for achieving this goal are bilateral and sequential internal mammary artery (IMA) grafting [4, 5]. The right gastroepiploic artery might serve as an additional in situ arterial conduit for the right coronary artery [6].

In most centers, the IMA is isolated from the chest wall as a pedicle, together with the vein, muscle, fat, and accompanying endothoracic fascia [1, 2]. Harvesting is relatively quick because cautery is used to separate the pedicle from the chest wall. However, cauterization damages the blood supply to the sternum, which in turn impedes sternal healing and exposes the sternum to the risks of early dehiscence and infection, particularly in operations in which both IMAs are used [7–9]. This risk is especially great in elderly and diabetic patients [9–12].

A surgical technique was recently developed wherein the IMA is dissected as a skeletonized vessel [2, 13]. The skeletonized artery is isolated gently with scissors and silver clips, without the use of cauterization. Skeletonized IMA dissection leaves the vein, muscle, and accompanying tissue in place (Fig 1). The advantage is that the dissected artery is particularly long, and its spontaneous blood flow is greater than that in a pedicled IMA [14], allowing the use of both IMAs as grafts to all necessary coronary vessels.

View larger version (32K): [in this window] [in a new window]   Fig 1. Pedicled internal mammary artery (left), elongation of the internal mammary artery by transverse incisions of endothoracic fascia (middle), and skeletonized internal mammary artery (right).

As of April 1996, we decided to adopt this bilateral skeletonized IMA technique as the exclusive method for myocardial revascularization in our department. In this report we describe our clinical experience in a series of 472 consecutive patients who underwent CABG using bilateral skeletonized IMAs.

	Material and methods

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Between April 1996 and June 1997, CABG was performed in 666 patients (Table 1). Fifty-nine of the 666 patients (< 9%) underwent conventional CABG operations. This includes patients from groups 4 and 5 in Table 1, and excludes 17 patients with patent IMA who underwent a repeat CABG. Most of these 59 patients underwent either emergency or urgent CABG, or were operated on during the very beginning of the study period. Bilateral IMA was used in 472 patients who are the ones described in this report. The average age of the patients was 65 years, 169 (36%) were older than 70, and 145 (30%) were diabetic (Table 2). The IMAs were dissected as skeletonized arteries [4] before heparin administration to decrease the risk of damage and hematoma formation in the region of the side branches during dissection.

View larger version (32K): [in this window] [in a new window]   Fig 2. Left internal mammary artery (LIMA) anastomosis to marginal branches of the circumflex, right internal mammary artery (RIMA) to left anterior descending artery (LAD) and right gastroepiploic artery (RGEA) to the posterior descending branch of the right coronary artery (RPDA). (Ao = aorta; D1 = first diagonal branch of LAD; M2 = second marginal circumflex coronary artery; PA = pulmonary artery.)

View larger version (43K): [in this window] [in a new window]   Fig 3. Composite graft: free right internal mammary artery (RIMA) (to marginal circumflex and posterior descending branches [RPDA]) is anastomosed end-to-side to in situ left internal mammary artery (LIMA) (to left anterior descending artery [LAD]) (A, scheme; B, coronary angiogram performed at postoperative day 7). (Ao = aorta; D1 = first diagonal branch of LAD; M2 = second marginal circumflex coronary artery; PA = pulmonary artery.)

View larger version (37K): [in this window] [in a new window]   Fig 4. In situ right internal mammary artery (RIMA) to right coronary artery and left internal mammary artery (LIMA) to left anterior descending artery (LAD) with minicomposite graft. (Ao = aorta; D1 = first diagonal branch of LAD; M2 = Second marginal circumflex coronary artery; PA = pulmonary artery; RPD = posterior descending branch of the right coronary artery; SKEL. = skeletonized.)

To decrease the risk of spasm of the arterial grafts, all patients were treated with high-dose intravenous infusion of isosorbide dinitrate (Isoket) (4 to 20 mg/hr) during the first 24 to 48 hours postoperatively [17]. Systolic blood pressure was maintained at more than 100 to 120 mm Hg. From the second postoperative day, the patients were treated with calcium channel blockers (diltiazem, 90 to 180 mg/day orally) for at least 3 months.

Statistical analysis
Data are expressed as mean ± standard deviation or proportions. The ² test and two sample t tests were used to compare discrete and continuous variables, respectively. Multivariate logistic regression analysis was used to predict unfavorable outcome events by various risk factors. Odds ratio (OR) and 95% confidence intervals (CI) are given. Postoperative survival is expressed by the Kaplan-Meier method. All analyses were performed by SPSS 7.5 software (SPSS Inc, Chicago, IL).

	Results

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We performed two to six grafts per patient (mean, 3.2). The average cardiopulmonary bypass time was 89 ± 41 minutes, and aortic cross-clamping time was 70 ± 27 minutes. Operative mortality (30 days postoperatively) was 1.7% (8 patients). The mortality of urgent and elective patients was 0.7% (3 of 410 patients), and that of emergency operations was 8.1% (5 of 62 patients; p < 0.01). Postoperative morbidity included 3 patients (0.6%) with perioperative myocardial infarction and 6 patients (1.3%) who suffered stroke (three with permanent neurologic deficiency and three who recovered completely). Eight patients (1.7%) sustained sternal wound infection, one of whom was included in the perioperative mortality. Six patients (1.3%) suffered from postoperative bleeding that required reopening of the chest.

Follow-up was available in 462 of the 464 surviving patients (99%) up to 25 months postoperatively. There were seven late deaths, two of which were unrelated to the operation (abdominal aneurysm, gastrointestinal bleeding after gastrointestinal operation). Three patients (0.6%) had late myocardial infarction and there were four new cases (0.8%) of congestive heart failure. Ten patients (2.1%) reported return of the angina. In the last follow-up, 431 of the surviving patients (92%) are well and free of angina. Twenty-four patients underwent cardiac catheterization during the follow-up period, 13 because of chest pain, and the remainder consented to elective catheterization within the framework of learning to use the composite graft. Seventy-one of 75 distal anastomoses (94.6%) were patent.

Analysis of early and late mortality
Kaplan-Meier analysis of the entire cohort showed 2-year actuarial survival of 96.8%, (Fig 5). Univariate analysis (Table 2) demonstrated that emergency operation, left ventricular dysfunction (ejection fraction, < 35%), preoperative use of intraaortic balloon pump, and old myocardial infarction were significant predictors of early mortality (30 days). Bypass time (88 ± 41 minutes) and cross-clamping time (64 ± 10 minutes) were not significant predictors. However, after adjustment for previously identified demographic, clinical, and surgical predictors of outcome, only emergency operation (OR 12; 95% CI 2.8 to 53) and old myocardial infarction (OR 5.8; 95% CI 1.1 to 29.8) emerged as independent risk factors for early mortality. Analysis of both early and late mortality events showed the following risk factors to be independent predictors of overall mortality: emergency operation (OR 9.7; 95% CI 3 to 31), repeat CABG (OR 7.5; 95% CI 1.5 to 36.7), chronic obstructive pulmonary disease (OR 6; 95% CI 1.6 to 23), and old myocardial infarction (OR 3.4; 95% CI 1.0 to 11.3).

View larger version (10K): [in this window] [in a new window]   Fig 5. Survival curve (Kaplan-Meier).

	Comment

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This report summarizes our early experience with the routine use of bilateral skeletonized IMAs. We have adopted this surgical technique as our standard approach for myocardial revascularization. The current conventional and most commonly used operative procedure for CABG includes one IMA together with one or more SVG [18, 19]. Vein graft atherosclerosis, however, continues to be the major cause of late failure of CABG. Consequently, techniques were sought for complete arterial myocardial revascularization without the use of SVG. Most of the reported series on bilateral IMA grafting are based on selected patient populations such as young and nondiabetic individuals collected over the course of several years [2, 4, 5, 9, 18, 20]. Unlike those studies, our reported operative procedure (without the use of vein grafts) was performed in almost all patients undergoing CABG. Our patients were typical for an urban center (ie, relatively older population), and included patients with decreased myocardial function, emergency cases, those who had sustained a recent myocardial infarction, people more than 70 years of age, and diabetics. Our intention in performing this type of operation was to minimize the potential for recurrence of angina and all other untoward events associated with SVG failure, and to decrease morbidity associated with leg wound infection, edema, and pain in the leg harvesting site.

The extended length of the skeletonized IMA compared to the pedicled IMA, and its better blood flow provides the surgeon with practically unlimited versatility in providing total arterial revascularization. The only contraindication for the use of arterial grafts during the study period was hemodynamic instability and decreased blood pressure (requiring rapid connection to cardiopulmonary bypass) in emergency operations. It should be noted that arterial grafts were used after hemodynamic stabilization with or without intraaortic balloon pump support in many emergency and critically ill patients. The mortality rate in the 62 patients undergoing emergency operations (8.1%) was significantly higher than that of the 410 patients undergoing urgent or elective procedures (0.7%). This mortality, however, is still lower than that documented in recently reported series of emergency CABG, ranging between 13.4% to 31.7% [21, 22].

The immediate operative results and predictors of early mortality are comparable to those described in operations in which one IMA was used [18]. This is true not only for operative mortality, perioperative myocardial infarction, and stroke, but also for rates of sternal infection and dehiscence. Our results in this area are also satisfactory in the groups of patients with an elevated risk of these complications, such as elderly patients (>70 years) and diabetics (mortality of 2.7% and 2.1%, sternal infections 1.4% and 2.1%, respectively; Table 2). Horneffer [23] at Johns Hopkins University noted a high incidence of noncardiac complications for patients more than 70 years of age, which contributed to the 9.3% mortality for that group compared with 2.2% for younger patients.

A growing number of diabetic patients who suffer from multivessel coronary artery disease have recently been referred for operation due to unfavorable results of percutaneous transluminal coronary angioplasty [24]. In the recently reported Bypass Angioplasty Revascularization Investigation (BARI) study, the better average of 5.4-year survival of diabetic patients who underwent CABG was attributable to reduced cardiac mortality (5.8% versus 20.6% with percutaneous transluminal coronary angioplasty; p = 0.0003) [25]. The better survival for CABG patients was limited to those who received at least one IMA graft. The use of the pedicled IMA as a coronary graft is associated with increased risk of sternal wound infection, and mediastinitis: In the New York University report, the prevalence of sternal wound infection was 2.2% in the IMA group, compared to only 0.8% in the SVG group [10]. Kouchoukos and associates [12] reported that the use of bilateral IMA was associated with increased risk of sternal infection (6.9%) than that with unilateral IMA (1.9%) or SVG (1.3%; p < 0.001). The relative risk of sternal wound infection for patients with diabetes and bilateral IMA was 5.00 (95% CI 2.4 to 10.5) in the Cleveland clinic experience of 6,504 patients [11]. It is of interest to note that no wound complications were observed in another report on 63 diabetic patients who underwent bilateral skeletonized IMA grafting [20]. Our report bestowed significant clinical proof of the basic assumption concerning the technique of skeletonized IMA—that it causes less damage to the sternal blood flow [7, 15].

Analysis of sternal infection in this cohort (8 patients) revealed that the only independent predictor of sternal wound infection was chronic obstructive pulmonary disease; 4 of the 42 patients with this condition (9.5%) suffered postoperative sternal infection compared to only 4 of 430 of the patients without this risk factor (0.9%). We assume that the increased respiratory mechanical forces produced in these patients in the first few postoperative days causes sternal dehiscence, secretion of mediastinal fluids through the skin, and secondary deep wound infection. At present, results of this analysis are implemented in our daily practice; we are reluctant to use bilateral IMAs in patients with chronic obstructive pulmonary disease, and recommend the use of only one IMA (to the left anterior descending coronary artery) with combination of veins or other arterial conduits in this group.

Another disadvantage of this operative technique is that harvesting the skeletonized arterial graft is time consuming. Therefore, the use of the skeletonized artery is not advised when rapid connection to cardiopulmonary bypass is necessary.

In summary, routine use of the skeletonized IMA for all patients undergoing CABG is a somewhat revolutionary approach. We acknowledge that it might be too early to leap to conclusions. The benefits of using arterial grafts should be evaluated in a long-term follow-up of at least 5 to 10 years. However, the relatively short-term results are satisfactory and justify continuing the routine use of this technique for myocardial revascularization, with minimal use of saphenous vein grafts.

	Addendum

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Up until January 6, 1999, 1,000 patients have undergone CABG with bilateral skeletonized IMA grafting in our department. Of these, 36% were older than 70 years of age and 40% were diabetics. Hospital mortality was 2.4%, and the rate of sternal wound infection was 1.8%. Late mortality (up to 33 months postoperatively) was 1.5%.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Jacob Gurevitch Yaron Moshkovitz Rephael Mohr Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gurevitch, J. Articles by Mohr, R. Search for Related Content PubMed PubMed Citation Articles by Gurevitch, J. Articles by Mohr, R. Related Collections Related Article