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J Thorac Cardiovasc Surg 2001;121:668-674
© 2001 The American Association for Thoracic Surgery
Surgery for Acquired Cardiovascular Disease |
From the Department of Thoracic and Cardiovascular Surgery, Tel-Aviv Sourasky Medical Center, the Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
Received for publication March 20, 2000. Revisions requested May 15, 2000; revisions received Oct 6, 2000. Accepted for publication Nov 6, 2000. Address for reprints: Rephael Mohr, MD, Department of Thoracic and Cardiovascular Surgery, Tel-Aviv Sourasky Medical Center, 6 Weizman St, Tel-Aviv 64239, Israel (E-mail: raphmohr{at}tasmc.health.gov.il).
Abstract
Objective: Increased risk of deep sternal infections has prohibited routine bilateral internal thoracic artery grafting in diabetic patients. The technique for harvesting the skeletonized internal thoracic artery provides the potential to minimize this risk. The purpose of this study was to compare the outcome of bypass grafting with bilateral skeletonized internal thoracic arteries in diabetic and nondiabetic patients.
Methods: From May 1996 to April 1998, 231 consecutive diabetic and 534 nondiabetic patients underwent bilateral skeletonized internal thoracic artery grafting. Mean age was 66 years. Compared with the nondiabetic group, the diabetic group comprised more women (29% vs 18%, P = .001), had a greater prevalence of hypertension (53% vs 44%, P = .019) and congestive heart failure (20% vs 14%, P = .016), but a lower prevalence of preoperative acute myocardial infarction (26% vs 34%, P = .027).
Results: Operative mortality of diabetic patients was comparable with that of nondiabetic patients (3% vs 2.6%). The two groups also had similar occurrences of deep sternal infection (2.6% vs 1.7%, respectively, P = .40). Deep sternal infection was significantly more prevalent in obese, diabetic women (3/20 = 15%) than in diabetic patients without this combination of risk factors (3/211 = 1.4%, P < .0001) (odds ratio 11.1, confidence interval 2.1-59.4). Diabetic patients also had a higher incidence of stroke (3.5% vs 0.9%, P = .014). Three-year actuarial survival of diabetic patients was lower (91.3% vs 94.7%, P = .083).
Conclusions: Bilateral skeletonized internal thoracic artery grafting is a good surgical revascularization option in diabetic patients. Operative mortality and prevalence of sternal infection are comparable with those of nondiabetic patients. However, the risk of sternal infection in obese diabetic women is high, and for them we advocate the use of a single artery instead of bilateral internal thoracic arteries.
For related editorial, see p. 625.
A growing number of diabetic patients with multivessel coronary artery disease have recently been referred for coronary artery bypass grafting (CABG) because of an unfavorable outcome of percutaneous transluminal coronary angioplasty.
1,2 Angioplasty in diabetic patients is associated with increased rates of restenosis and reinterventions 1-4 and a significantly lower 5-year survival compared with CABG. 1,2
The improved survival of diabetic patients who underwent CABG is limited to those who received at least one internal thoracic artery (ITA) graft. 1,5 The superior patency rate of the ITA has led many surgeons to use both ITAs for myocardial revascularization in an attempt to avoid late saphenous vein closure and postoperative return of angina. Several important studies that appeared during the past few years reported survival benefit after bilateral ITA (BITA) compared with single ITA grafting. 6-10 However, extensive arterial grafting with BITAs was confined mostly to nondiabetic patients because of the increased risk of deep sternal wound infection that was documented in patients who underwent surgical procedures with BITA grafting. 11,12
To decrease the risk of sternal infection associated with BITA harvesting, we adopted the technique of a skeletonizing dissection. 13-15 The skeletonized artery is isolated gently with scissors and silver clips, without the use of cauterization. The advantage of using the ITA as a skeletonized artery is the preservation of collateral blood supply to the sternum, enabling more rapid healing and decreasing the risk of infection. 16 Bilateral skeletonized ITA grafting is the preferred method for myocardial revascularization in our service. This procedure is routinely performed in most of the patients referred for CABG, including elderly, obese, and diabetic patients.
As of May 1996, 765 consecutive patients had undergone arterial revascularization with skeletonized BITA grafts, including 231 (30%) diabetic patients. The purpose of this study was to evaluate the impact of diabetes mellitus on early and 3-year outcome of this subgroup by comparing it with the group of nondiabetic patients with skeletonized BITAs.
Patients and methods
Between May 1996 and April 1998, 231 consecutive diabetic patients and 534 nondiabetic patients underwent CABG with BITA grafts at the Tel-Aviv Sourasky Medical Center. Preoperative and operative characteristic of both diabetic and nondiabetic patients are listed in Table I. Female sex, congestive heart failure (CHF), and hypertension were more prevalent in the diabetic group than in the nondiabetic group. However, a larger number of nondiabetic patients had acute myocardial infarction (MI) preoperatively.
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13 before heparin administration to decrease the risk of damage and hematoma formation in the region of the side branches during dissection. The operations were performed with cardiopulmonary bypass. The myocardial preservation technique involved intermittent infusion of warm cardioplegic solution (30°C-32°C). 17 In 45 diabetic patients (19%) and in 131 nondiabetic patients (24.5%), the right gastroepiploic artery was used as a third arterial conduit to bypass the posterior descending branch of the right coronary artery. A composite graft was prepared before connection to cardiopulmonary bypass in 478 patients (62%)(Table I
). Most of the composite grafts included end-to-side anastomosis of a free right ITA on an in situ left ITA. When the proximal part of the left ITA was damaged, or when its spontaneous free flow was not sufficient, a free left ITA was anastomosed end to side to an in situ right ITA. A third variation was the small Y-graft, wherein a small distal section of an ITA was anastomosed end to side to a more proximal part of the same artery. When no graft to the posterior wall of the heart was necessary (the circumflex region), the left ITA was grafted to the left anterior descending coronary artery and the right ITA to the right coronary artery or to its posterior descending branch. In most cases it is impossible to reach this branch of the right coronary artery when using the regular technique of isolating the pedicled ITA. The skeletonized right ITA, however, is longer and therefore can usually reach the better quality distal posterior descending artery.
To decrease the risk of spasm of the arterial grafts, we treated all patients with high-dose intravenous infusion of isosorbide dinitrate (Isoket) (4-20 mg/h) during the first postoperative 24 to 48 hours. Systolic blood pressure was maintained above 100 to 120 mm Hg. From the second postoperative day, the patients were treated with calcium channel blockers (diltiazem 90-180 mg/day orally) for at least 3 months.
Statistical analysis
Data are expressed as mean ± SD or proportions as appropriate. The 
2 test was used for late events and the Fisher exact test for the remaining discrete variables. A 2-sample t test was used to compare discrete and continuous variables. Multivariable 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 and survival was compared by the log rank test. The Cox proportional hazard model was used to evaluate risk factors for overall mortality in diabetic patients. All analyses were performed by SPSS 9.0 software (SPSS, Inc, Chicago, Ill).
Results
The 765 patients with skeletonized BITA grafts received 2 to 5 (mean 3.2) grafts per patient. The average cardiopulmonary bypass time was 79 ± 37 minutes, and aortic crossclamping time was 65 ± 28 minutes. Operative mortality of the 231 diabetic patients was 3% (7 patients)(Table II), which was not significantly different from the mortality of the 534 nondiabetic patients with skeletonized BITA grafts (2.6%, 14 patients)(Table II). (Operative mortality was defined as death occurring during hospitalization for the operation, no matter how long after the original operation the death occurred, and/or any death within 30 days in patients who were discharged from the hospital.) However, diabetic patients had higher rates of perioperative stroke (cerebrovascular accident [CVA] resulting in permanent neurologic deficits and computed tomographic evidence of cerebral infarction) (3.5% vs 0.9%, P < .05).
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There were no perioperative MIs (usually defined by the appearance of new Q waves in the electrocardiogram associated with serum levels of creatine kinase MB fraction > 50 mU/mL) among the diabetic patients (1.7% perioperative MIs in nondiabetic patients, P < .05), and the rates of deep sternal wound infection were similar in the two groups (2.6% vs 1.7%, respectively).
The univariate analysis performed in the diabetic group revealed female sex and obesity to be significant risk factors for deep sternal infection; however, only the combination of obesity and female sex was an independent risk factor for this complication (OR 11.1, CI 2.1-59.4)(Table III).
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None of the preoperative characteristics of the diabetic patients was found to be a significant predictor of early mortality; however, univariate analysis revealed age over 70 years, left ventricular ejection fraction less than 35%, CHF, and emergency operation to be predictors of overall (ie, combined early and late) mortality. Older age, emergency operation, and ejection fraction less than 35% were also found to be independent predictors in the multivariate analysis(Table IV).
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Unlike pedicled ITA harvesting, skeletonizing dissection of the ITA leaves the vein, muscle, and accompanying endothoracic tissue in place. Besides preserving collateral sternal blood supply and minimizing the risk of deep sternal infection, the advantage here is that the dissected artery is longer, and its spontaneous blood flow is greater than that of the pedicled ITA, 14,18 allowing the use of both ITAs as grafts to almost all necessary coronary vessels. No additional vein graft is required in most cases. 19
The findings in our current report do not directly prove that sternal collateral blood supply is improved with skeletonized ITA dissection. However, they do strengthen the basic assumption concerning this harvesting technique, that it causes less damage to sternal blood flow 15,20,21 and therefore enables the use of BITA grafts in diabetic patients. Diabetes mellitus alone was found not to be a significant risk factor for early mortality or deep sternal infection when BITAs are harvested as skeletonized arteries. The current study also delineated a subgroup of diabetic patients with increased risk of deep sternal wound infection—diabetic obese women. The combination of diabetes, obesity, and female sex was found to be associated with a 10-fold rate of deep sternal infection (15% vs 1.4% in diabetic patients without this combination of risk factors). Previous reports have shown obesity to be an independent risk factor for deep sternal infection and sternal dehiscence. 11,22,23 A study by Loop and associates 11 of 6504 consecutive patients having CABG identified obesity (OR 2.9) as the most important risk factor for sternal wound complications. Other risk factors for this complication included BITA grafting, diabetes mellitus, and old age. In another recently published study of 11,101 CABG patients by Birkmeyer and coworkers, 23 the risk of sternal wound infection was more than twice as high among the obese and nearly three times higher among the severely obese CABG patients. In view of this unacceptably high risk of sternal infection, we do not advocate the use of BITA grafts in obese diabetic women, for whom we prefer to use single ITA and saphenous vein grafts.
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24 In another report from Emory University in Atlanta, stroke was significantly more prevalent in patients with diabetes than in those without diabetes (2.9% vs 1.4%, respectively, P < .05). 25
A recently published multicenter prospective study on 2108 patients by Roach and colleagues 26 reported an incidence of 6.1% for adverse cerebral outcome and of 3.1% for strokes (fatal and nonfatal) after CABG. The incidence of strokes was 5 times higher in patients with intraoperatively palpable atherosclerotic plaque in the proximal aorta. In this study, diabetes was defined as a significant risk factor for stroke (OR 2.46). Despite the relatively older age of our patients (mean 66.3 years, 33% older than 70 years), the rate of postoperative stroke was slightly lower than that in the report by Roach and associates 26 (1.7% vs 3.1%). This may be explained by the fact that complete arterial revascularization was achieved without the use of vein grafts in 89% of our patients. Complete arterial revascularization permits the limitation of aortic manipulations to the necessary procedures alone, that is, aortic cannulation, insertion of cardioplegia needles, and crossclamping of the aorta. In this technique, the ITAs are used as the sole source of blood supply for CABG to eliminate manipulation of the aorta when there is atheromatous plaque (the "no-touch" technique). 27
The diffuse and advanced nature of the atherosclerotic plaques in the aorta and brain vessels of diabetic patients is probably the most likely explanation for the higher incidence of stroke. 28,29 Another possible explanation is the elevated level of ß-thromboglobulin and circulating platelet aggregates in the blood of diabetic patients, which may reflect platelet activation and may cause postoperative microemboli. 30 Finger palpation of the ascending aorta may underestimate the frequency and severity of atherosclerotic plaques involving this part of the aorta. Epiaortic or transesophageal echocardiography might improve intraoperative detection of pathologic aortic plaques and thus reduce the rate of postoperative strokes.
The midterm results of this study include up to 3 years of follow-up. Late and overall mortality rates of patients with diabetes were higher than those of patients without diabetes (6% and 9% vs 2.8% and 5.4%). The 3-year actuarial survival of nondiabetic patients was better, but the difference between survivals was not significant, probably because of the relatively short period of follow-up. The adverse effect of diabetes mellitus on late survival was described by Morris, 31 Lawrie, 32 Thourani, 25 and their colleagues.
Our report suggests that diabetes may be an important risk factor for late mortality at a longer follow-up period, even in patients undergoing arterial myocardial revascularization with BITAs. We found emergency operation, older age, and severe left ventricular dysfunction to be predictors of late mortality in diabetic patients.
In summary, the use of BITA grafting is an appropriate surgical revascularization technique for diabetic patients. It provides multiple arterial grafting with the best conduits (ITAs) and at the same time is associated with a relatively low risk of deep sternal infections. The prevalences of early mortality and deep sternal infection in diabetic patients in this study are similar to those of nondiabetic patients. The occurrence of perioperative MI in diabetic patients was low. However, our study showed that diabetic patients have an increased risk of stroke, which is probably related to the diffuse character of their atherosclerotic disease. The 3-year cumulative survival was favorable, albeit not as good as in the nondiabetic patients. Long-term follow-up of randomized studies comparing this surgical technique to the more conventional techniques (left ITA plus saphenous vein graft) is needed.
Acknowledgments
We thank Esther Eshkol for her editorial assistance.
References
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