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Ann Thorac Surg 2004;77:2039-2045
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Bilateral versus single internal thoracic artery grafting in oral-treated diabetic subsets: comparative seven-year outcome analysis

Oren Lev-Ran, MDa*, Rony Braunstein, PhDb, Nahum Nesher, MDa, Yanai Ben-Gal, MDa, Gil Bolotin, MDa, Gideon Uretzky, MDa

a Department of Cardiothoracic Surgery, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
b Department of Epidemiology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

Accepted for publication December 22, 2003.

* Address reprint requests to Dr Lev-Ran, Department of Cardiothoracic Surgery, Tel Aviv Sourasky Medical Center, 6 Weizmann St, Tel Aviv 64239, Israel
e-mail: orenlevran{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: Recent interest has focused on the use of arterial conduits in diabetic subsets. To date, the long-term benefits of bilateral internal thoracic artery (BITA) grafting in this subgroup remain in question.

METHODS: Two hundred eighty-five consecutive oral-treated diabetics operated on nonemergent basis (1996 to 1998) were compared according to the surgical technique, left-sided skeletonized BITA (n = 228) or single internal thoracic artery- saphenous veins (SITA) (n = 57). Patients with chronic lung disease, usually preselected to SITA grafting, were not included.

RESULTS: The respective grafts to patient ratio was 3.1 ± 1 and 3.2 ± 0.8 for the SITA and BITA groups (p = NS). Complementary conduits used in the BITA group were gastroepiploic arteries (25%) and saphenous veins (13%). Early outcome was comparable, including the incidence of deep sternal infections (1.8% in both groups). During follow-up (range, 4 to 7.5 years; median, 5), there were less repeat revascularizations (4.4% vs 12.3%, p = 0.025) and major adverse cardiac events (MACE) (11.2% vs 36.8%, p < 0.0001) in the BITA group. At 7 years, survival (Kaplan-Meier) (75% vs 59%, p = 0.006, log-rank), freedom from cardiac mortality (92% vs 68%, p < 0.0001), and freedom from MACE (70% vs 59%, p = 0.004) were superior in the BITA group. Multivariate analysis identified the use of BITA as a protective factor against the occurrence of late cardiac mortality (odds ratio [OR] 0.2) and MACE (OR 0.3); conversely, SITA-saphenous vein arrangements increased the risk by fivefold (OR 5, confidence interval limits [CL] 1.6 to 16.6, p = 0.005) and threefold (OR 3.3, CL 1.5 to 9, p = 0.005), respectively.

CONCLUSIONS: Left-sided BITA grafting confers improved long-term survival and event-free survival in oral-treated diabetics. We, therefore, recommended this approach in this diabetic subset.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Coronary artery bypass grafting (CABG) has been established as the preferred method of myocardial revascularization in diabetic patients [1–3]. Nevertheless, reflecting increased arteriosclerosis, diabetic patients fare worse than nondiabetics in terms of a higher propensity for bypass grafts failure and late mortality [4]. It has been reasoned that these patients may benefit from a conduit most resistant to the augmented diabetic vascular process.

Recent interest has been focused on the use of multiple arterial grafts in diabetics [5, 6]. While several arterial conduits have been proposed [5, 6], the internal thoracic artery (ITA) has been singled out for its superior histologic [7] and vasoreactive properties [8] in diabetic subsets. Moreover, the survival benefit associated with CABG in diabetic patients has been limited to those patients receiving at least one ITA graft [1, 3, 9].

The use of bilateral internal thoracic artery (BITA) in diabetics has been a matter of debate due of the risk of sternal infection. Accumulating data, however, suggest that skeletonized BITA can be performed safely in certain diabetic subgroups [10–12]. While the value of a second ITA in terms of survival and event-free survival has been previously established in nondiabetics [10, 13], the long-term benefits of this approach in diabetics has yet to be determined [9, 14].

The purpose of this study was to compare our data from 1996 to 1998 and determine the long-term outcome following BITA versus single ITA grafting in oral-treated diabetics. We focused on oral-treated diabetics because, with the exception of selected patients [15], use of BITA in the insulin diabetic subgroup is generally deferred.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Study design
Between April 1996 and August 1998, 285 consecutive oral-treated diabetic patients underwent nonemergent isolated CABG for multivessel coronary artery disease. Two hundred twenty-eight patients who underwent BITA grafting (BITA group) were compared to 57 patients in whom single ITA was mobilized (SITA group). The complementary grafts in the SITA group consisted of saphenous veins (SV). The BITA group reported herein constituted 91% of all operated oral-treated diabetics and 26% of the total BITA operations performed during this period.

Included in the study were diabetics receiving oral-agent treatment for 6 months or more before the index surgery. All oral-treated diabetics were considered eligible for BITA grafting and patient allocation to this technique was based on technical considerations [16]. Patients were excluded from BITA grafting only when considered as high risk for sternal infection (detailed below), irrespective of the patient's cardiac or overall risk stratification. Reflecting our policy since 1997 for nondiabetics and diabetics alike [16], following interim analysis, patients undergoing emergency operations and patients with chronic lung disease were preferentially allocated to single ITA grafting. We therefore excluded from this study diabetics with these comorbid conditions. The operations were performed by all staff surgeons.

Neurologically symptomatic patients or asymptomatic patients 65 years of age or older were screened preoperatively by carotid Doppler assays; those requiring carotid endarterectomy (symptomatic with unilateral stenosis > 70% or asymptomatic with severe bilateral stenosis), were excluded from this study. Glucose management upon admission included sliding-scale-guided intermittent subcutaneous insulin injections aimed to achieve glucose levels of less than 250 mg/dL.

Surgical technique and postoperative management
All operations were performed through a midline sternotomy using cardiopulmonary bypass (CPB). Myocardial protection involved intermittent, antegrade blood cardioplegia (30°C to 32°C). Internal thoracic arteries were mobilized as skeletonized vessels in all patients.

Bilateral internal thoracic arteries were used to graft the left coronary system; ie, the left anterior descending (LAD) and the circumflex marginals. The arrangements used for left-sided BITA were in-situ BITA with anteaortic crossover right ITA and T grafts composed of free right ITA was attached proximally on the left ITA [16]. The choice of configuration was determined by technical considerations, previously detailed elsewhere [16]. If required, supplemental conduits to the right coronary system were either in-situ (transdiaphragmatic) right gastroepiploic artery or SV. A target coronary stenosis of greater than or equal to 70% was a prerequisite for the use of a gastroepiploic artery. In the SITA group, the LAD was grafted by the left ITA in all patients while other target vessels received SV grafts.

Postoperative management included high doses of intravenously administered isosorbide dinitrate (4 to 20 mg/h) for two days. Glucose management was aimed at maintaining a level of less than 250 mg/dL by sliding-scale-guided intermittent subcutaneous insulin injections. All patients received aspirin 250 mg starting from postoperative day 1 and lipid-lowering agents were renewed on day 3. Patients who had received gastroepiploic artery grafts were treated by calcium-channel blockers for 6 months postoperatively. Postoperative angiography was performed selectively only in symptomatic patients (return of angina or undetermined chest pain), or in those with positive radionuclear scan.

Definition of terms and data collection
Patients' data were collected retrospectively and analyzed according to the STS National Cardiac Surgery database guidelines and definitions. Causes of late death were classified as cardiac or noncardiac. Late cardiac mortality was defined as death occurring in relation to myocardial infarction (MI), cardiac arrhythmia, out-of-hospital sudden death, or deteriorating congestive heart failure. An undetermined cause of death was regarded as cardiac. Major adverse cardiac events (MACE) were defined as the occurrence of one of the following: nonfatal MI, need for repeat revascularization, or cardiac mortality. Follow-up was obtained by a telephone questionnaire and the national registry database.

Data analysis
Data are expressed as mean ± standard deviation. The {chi}2 test was used to compare discrete variables. The Student's t test and the Mann-Whitney test were used for the comparison of continuous variables. Actuarial survival curves were obtained with the Kaplan-Meier method. Statistical significance was calculated with the log-rank test. Logistic regression was used to evaluate the effect of preoperative and operative descriptors on occurrence of late mortality, late cardiac mortality, and MACE. Results of logistic regression were expressed as odds ratio (OR) with associated 95% confidence interval limits (CL) and p values. All analyses were performed by SPSS 11 software (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Preoperative variables were distributed evenly between the groups with the exception of body mass index (BMI) and acute MI (Table 1). The predicted overall risk stratification (logistic Euroscore) was comparable (Table 1). The prevalence of diagnosed diabetic retinopathy at time of surgery, a marker of diabetic microvascular involvement, was comparable in both groups (Table 1).


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  		Table 1. Baseline Characteristics

 
Operative data are listed in Table 2. The mean number of grafts per patient was comparable (3.1 ± 1 vs 3.2 ± 0.8, p = 0.377). Total arterial revascularization was performed in 91% of the patients in the BITA group, using BITA grafts only (66%) or BITA and gastroepiploic arteries. The fact that T grafts, sequential grafts, and arterial anastomoses were more frequent in the BITA group is inherent to the choice of surgical technique.


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  		Table 2. Operative Data

 
Operative mortality and morbidity
Data on operative mortality and morbidity are listed in Table 3. The logistic Euroscore predicted-mortality was 3.8% (CL, 0.032 to 0.043) for the BITA group, and 3.6% (CL, 0.024 to 0.047) for the SITA group. Early outcome, including 30-day mortality, perioperative MI, neurologic events, and sternal complications were comparable (Table 3). The primary mode of late death was cardiac (Table 3).


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  		Table 3. Early and Latea Results

 
Follow-up status
Follow-up ranged from 4 to 7.5 years (average, 5.25 years; median, 5.25 years) and was ascertained for 98% of the patients. Late outcome is presented in Table 3. One hundred twenty-six distal anastomoses were demonstrated by 38 coronary angiograms; 26 (11.4%) and 12 (21%) in the BITA and SITA groups, respectively. The distal ITA patency rate was 91.5% and 25 of 26 (96%) patients of the T anastomoses were patent. The SV patency rate was 72% (mean, 35.4 months postoperatively; range, 18 to 60). The reintervention rate was significantly higher in the SITA group (p = 0.025) (Table 3), however, the difference in the rate of redo CABG did not reach statistical significance (0.9% vs 3.5% in the BITA and SITA groups, respectively).

Survival data are presented in Figures 1–3. Seven-year survival (Kaplan-Meier) was 74.9% and 58.6% in the BITA and SITA groups, respectively (p = 0.006, log-rank). The respective freedom from cardiac mortality at 1, 5, and 7 years was 99.5% versus 92.6%, 93.3% versus 73.3%, and 91.9% versus 67.7% in the BITA and SITA groups (p < 0.0001, log-rank). The respective freedom from MACE at 1, 5, and 7 years for the BITA and SITA groups was 99.5% versus 92.6%, 89% versus 71%, and 70.4% versus 59% (p = 0.004, log-rank).



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  		Fig 1. Cumulative survival; BITA (----) versus SITA (—) groups. (BITA = bilateral internal thoracic artery; SITA = single internal thoracic artery.)

 


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  		Fig 2. Freedom from cardiac-related mortality; BITA (----) versus SITA (—) groups. (BITA = bilateral internal thoracic artery; SITA = single internal thoracic artery.)

 


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  		Fig 3. Freedom from major adverse cardiac events (MACE); BITA (----) and SITA (—) groups. The occurrence of one or more of the following: late nonfatal myocardial infarction, reintervention, or cardiac-related mortality. (BITA = bilateral internal thoracic artery; SITA = single internal thoracic artery.)

 
Prediction of late adverse outcome
Univariate (Table 4) and multivariate (Table 5) analyses were used to assess the effect of confounding factors on all-cause mortality, cardiac-related mortality, and MACE . Peripheral vascular disease (PVD) was identified as independent predictor of mortality (OR 3.6, CL 1.72 to 7.67, p = 0.001), cardiac-related mortality (OR 4.3, CL 1.57 to 12.2, p = 0.05), and the occurrence of MACE (OR 2.5, CL 1.13 to 5.70, p = 0.024). Preoperative congestive heart failure (OR 2.4, CL 1.11 to 5.30, p = 0.026) and acute MI (OR 2.6, CL 0.87 to 8.23, p = 0.084 [trend]) correlate with mortality and cardiac-related mortality, respectively. Bilateral internal thoracic artery grafting was identified as a protective factor against cardiac-related mortality (OR 0.2, CL 0.06 to 0.62, p = 0.005) and MACE (OR 0.3, CL 0.11 to 0.67, p = 0.005); conversely, the use of single ITA increased the risk of these endpoints by fivefold (OR 5, CL 1.61 to 16.6, p = 0.005) and threefold (OR 3.3, CL 1.49 to 9.09, p = 0.005), respectively.


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  		Table 4. Univariate Analysis: Predictors of All-Cause Mortality, Cardiac-Related Mortality, and MACEa

 

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  		Table 5. Multivariate Logistic Regression Analysis: Predictors of All-Cause Mortality, Cardiac-Related Mortality and MACEa

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
The results of this study indicate that BITA grafting in oral-treated diabetics confers long-term advantage in terms of survival and event-free survival in comparison to the traditional single ITA-SVG combination. Corresponding to its benefits in nondiabetics [10], BITAs use independently achieved superior freedom from cardiac mortality and freedom from MACE in this diabetic subset. While the survival benefit of (single) ITA in diabetics has been recognized, this study provides evidence that multiple left-sided ITA grafts further extend this benefit.

Because most available studies are limited by short follow-up periods and include relatively small samples, the long-term outcome after left-sided BITA grafting in diabetics has remained in question. We have reviewed our data from 1996 to 1998 in order to address this issue. Based on their high propensity for sternal infections, diabetics with chronic lung disease and emergent cases [11, 16, 17] are usually preselected to undergo single ITA grafting (considered as relative contraindications for BITA grafting). We excluded such patients in order to study a more homogeneous population.

The 4.4% BITA rate of repeat revascularizations at 7 years was significantly lower than the 12% SITA rate (Table 3), the latter having been compatible with previous observations of 11% [18] and 13% [19] in diabetic patients after a similar time interval. Considering that ITA attrition is confined to the early postoperative years [20] while the SV process is progressive, this difference may be further disparate with time. The high mortality rate (11%) associated with redo CABG in diabetics [21] may explain the fact that rate of re-CABG was comparable between both study groups. Hence, this may reflect a policy in which percutaneous interventions are preferred over re-CABG in diabetics. Nevertheless, durable patent left-sided BITA may retain survival benefit from the initial CABG and reduce the indication for reoperation. Patency rates could not be elucidated from this study due to the stringent indications for coronary angiograms.

Multivariate analysis further identified the use of BITA as a protective correlate of improved long-term cardiac outcome. Reciprocally, the choice of single ITA was identified as an independent risk factor for cardiac mortality and the occurrence of MACE, increasing the risk by fivefold and threefold, respectively. Contradictory to previous observations [14], our results indicate that the choice of ITA grafts independently affects long-term cardiac outcome after CABG in oral-treated diabetics. Calafiore and colleagues [14], however, have recently suggested that intraoperative variables, including extensive use of arterial grafting, do not affect late cardiac mortality in diabetics. These differences may be explained by the fact that in our study all BITA patients received left-sided revascularization, that no arterial grafts other than ITA were used to the left coronary system, and that the analysis included only oral-treated diabetics. It should be noted that only left-sided BITA revascularization has been recognized as a predictor of improved survival [10, 13].

This study validates the safety of skeletonized BITA grafting in oral-treated diabetics, provided that several guidelines are followed. It appears that BITA use should be precluded in emergent cases and diabetics with chronic lung disease since these factors have been delineated as correlates of sternal infections [11] and in nondiabetics as well [16]. Still, after exclusion of these subsets, the majority of diabetics (80%) are eligible for BITA grafting. The 1.8% post-BITA incidence of deep sternal infection observed in our study is compatible with the reported rate following single ITA mobilization in diabetics [1, 6]. Moreover, the recommendation for continuous perioperative glucose control, aimed at maintaining the glucose level at 200 mg/dL or less for 48 postoperative hours [22], now considered a mainstay of therapy in diabetics, appeared after our patients were operated. It could be, then, that the incidence of 1.8% could be further reduced. The 2.2% 30-day mortality was lower than the Euroscore predicted mortality and compares favorably with the 3.2% mortality in the corresponding Society of Thoracic Surgeons database oral-treated diabetic subgroup [23]. The BITA operation requires a longer preperation time (before the initiation of CPB) and a longer overall operation time (skin to skin), reflecting a more demanding surgical technique; ie, the construction of T grafts, frequent use of sequential anastomoses, and sequenced harvesting of conduits. This technique may, therefore, be inappropriate in emergent cases.

The second graft of choice in diabetics remains in question. Despite increasing popularity of the radial artery, this conduit is less resistant to arteriosclerosis, intimal hyperplasia, and medial calcification in comparison to ITA [7]. Equally important is the fact that competitive flow may preclude its use in noncritical target coronary stenoses [24]. Moreover, the ITA has been the only conduit thus far to effect on survival in diabetics [1, 3]. The long-term impact of non-ITA arterial grafts awaits confirmation.

Several limitations of this study need to be addressed. This is a retrospective study and the comparison involved BITA with single ITA saphenous veins. A prospective long-term comparison between BITA and SITA radial artery arrangements would be further required to determine the strategy of choice in diabetic subgroups. Insulin-treated diabetics were not included in this study. To date, small datasets of insulin-treated diabetics undergoing BITA grafting did not offer a clear mandate for the routine use of BITA. While this study represents a conseutive group of oral-treated patients, the use of BITA in insulin diabetics is highly selective and involves preselection to either surgical technique.

In conclusion, left-sided BITA grafting can be performed safely in oral-treated diabetics. This approach confers superior long-term cardiac outcome and is, therefore, recommended in this diabetic subset.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

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Oren Lev-Ran
Nahum Nesher
Yanai Ben-Gal
Gil Bolotin
Gideon Uretzky
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