Ann Thorac Surg 2007;84:32-36
© 2007 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Off-Pump Coronary Artery Bypass Grafting With Skeletonized Bilateral Internal Thoracic Arteries in Insulin-Dependent Diabetics
Masashi Kai, MDa,
Michiya Hanyu, MD, PhDa,
Yoshiharu Soga, MD, PhDa,
Takuya Nomoto, MD, PhDa,
Jota Nakano, MDa,
Takehiko Matsuo, MDa,
Eitaro Umehara, MDa,
Masahide Kawato, MDa,
Hitoshi Okabayashi, MD, PhDb,*
a Department of Cardiovascular Surgery, Kokura Memorial Hospital, Fukuoka, Japan
b Department of Cardiovascular Surgery, Iwate Medical University Memorial Heart Center, Iwate, Japan
Accepted for publication February 28, 2007.
* Address correspondence to Dr Okabayashi, Department of Cardiovascular Surgery, Iwate Medical University Memorial Heart Center, Chuodori 1-2-1, Morioka, Iwate, 020-8505, Japan (Email: cardiovascsurg{at}siren.ocn.ne.jp).
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Abstract
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Background: We evaluated the effects of coronary artery bypass with off-pump skeletonized bilateral internal thoracic artery grafting in patients with insulin-dependent diabetes.
Methods: One hundred eighty-five consecutive patients with insulin-dependent diabetes who underwent isolated coronary artery bypass grafting with bilateral internal thoracic grafts were retrospectively compared according to surgical technique, ie, off-pump grafting with skeletonized internal thoracic artery (n = 162) or on-pump grafting with pedicled internal thoracic artery (n = 23).
Results: The on-pump group was younger (62.3 ± 9.2 versus 69.9 ± 8.5 years; p = 0.02) and had fewer distal anastomoses (3.5 ± 1.0 versus 4.0 ± 1.1; p = 0.02) than the off-pump group. No 30-day mortality occurred in either group. The incidence of deep sternal infection was significantly lower in the off-pump group than in the on-pump group (0.6% versus 13.0%; p = 0.01). The early angiographic results did not differ between the two groups. The median duration of follow-up was 3.4 years (range, 0.1 to 9.9 years). Rates of survival, freedom from cardiac mortality, and freedom from cardiac-related events (including cardiac-related death, myocardial infarction, percutaneous coronary intervention, repeat coronary artery bypass grafting, and congestive heart failure) did not differ between the two groups. Dialysis, peripheral vascular disease, ejection fraction less than 0.40, and age were independent risk factors of late death.
Conclusions: Overall, our results support the surgical management of coronary artery bypass grafting in insulin-dependent diabetics using off-pump skeletonized bilateral internal thoracic artery grafting.
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Introduction
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The current evidence suggests that diabetics have better survival with coronary artery bypass grafting (CABG) than with percutaneous coronary interventions [1, 2]. Internal thoracic artery (ITA) grafts are important because the higher survival rate in diabetics after CABG is limited to patients who receive ITA grafts.
Recently, bilateral internal thoracic artery (BITA) grafting was applied to gain further beneficial long-term results. Several reports have indicated that BITA grafting gives better survival rates and higher rates of freedom from cardiac-related events in diabetics than does single ITA grafting, although no randomized trials have been published [3–6]. Patients with insulin-dependent diabetes also benefit from BITA grafting in long-term studies [7].
However, from early results it has been commonly recognized that BITA grafting should be avoided in diabetics and particularly in insulin-dependent diabetics. The reason for avoiding BITA grafting is evidence that BITA grafting is accompanied by increasing rates of deep sternal wound infection [8, 9].
Recently, it was reported that skeletonized harvesting of ITAs was associated with a lower incidence of sternal infection than occurs with pedicled harvesting [10, 11]. In addition, the advantage of off-pump CABG versus the conventional CABG in high-risk patients has been reported in several studies [12–14].
We have been actively performing BITA grafting by using these techniques—skeletonization and off-pump grafting—in selected patients with insulin-dependent diabetes who we believe will gain the most beneficial long-term results from BITA grafting. The purpose of our study was to investigate the effects of off-pump, skeletonized BITA grafting in insulin-dependent diabetics.
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Patients and Methods
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Between January 1996 and December 2005, 802 consecutive patients with diabetes underwent isolated CABG with BITA grafting at Kokura Memorial Hospital. Among them, 185 patients (23.1%) treated with insulin were retrospectively analyzed. The insulin-dependent diabetics were subdivided into two groups, off-pump ITA grafting group (n = 162) and on-pump ITA grafting group (n = 23). Internal thoracic arteries were harvested in a skeletonized manner in the off-pump group and in a pedicled manner in the on-pump group in accordance with the hospital protocols at the time (see below). The two groups were compared with regard to operative mortality, morbidity, early angiographic results, and late results. Permission to use the appropriate database was obtained from the review board of Kokura Memorial Hospital, and informed consent was obtained from each participant. The preoperative characteristics of the patients and the operative data are summarized in Table 1.
Surgical Technique
Before January 2000, ITAs were harvested in a pedicled manner and cardiopulmonary bypass was used routinely. Thereafter, the skeletonized technique and off-pump grafting was introduced as another option and used in isolated CABG cases as a first choice. Pedicled ITAs were harvested by the standard technique. Skeletonized ITAs were dissected as isolated arteries with an ultrasonic scalpel (Harmonic Scalpel, dissecting-hook type; Ethicon Endo-Surgery, Cincinnati, OH). Internal thoracic arteries were harvested from the subclavian vein level to about 5 cm distal to the bifurcation of the musculophrenic and superior epigastric arteries. Our basic strategy was in situ BITA grafting for left-sided revascularization (left ITA to left anterior descending artery, right ITA routed through the transverse sinus to major branches of the circumflex artery) and either gastroepiploic artery or saphenous vein grafting for right-sided revascularization. However, in cases in which the in situ right ITA did not reach the major branches of the circumflex artery, a Y graft was constructed by attaching the free right ITA proximally to the left ITA in an end-to-side manner. Since 2001, before closing the chest we had routinely removed the xiphoid process: we had seen some cases in which the xiphoid process had become necrotic—possibly because of ischemia—and had become a source of infection after BITA harvesting. For blood glucose control in the early postoperative period, we used intravenous insulin injections every 3 to 6 hours in a directed attempt to maintain blood glucose levels less than 200 mg/dL. If it was difficult to control glucose levels by the above method, we used continuous insulin injection protocols [15]. Postoperative angiography was performed approximately 2 weeks after surgery (before discharge) for graft evaluation. All the anastomoses were performed by one experienced surgeon.
Definition
"Deep sternal wound infection" was defined according to the guidelines of the Centers for Disease Control and Prevention, with patients meeting at least one of the following criteria: (1) isolation of an organism from culture of mediastinal tissue or fluid; (2) evidence of mediastinitis during sternal reexploration; or (3) chest pain, sternal instability, or fever present in combination with purulent discharge from the mediastinum or isolation of an organism from blood or tissue cultures.
Statistical Methods
Data are expressed as mean ± standard deviation. Unrelated two-group comparisons were done with unpaired, two-tailed Student’s t tests for continuous variables and the 
2 or Fisher’s exact test for categorical data. Survival curves, curves of freedom from cardiac mortality, and curves of freedom from cardiac events were estimated by the Kaplan–Meier method. Statistical significance was calculated by the log-rank test. Cox proportional hazard models were used to determine the influence of patients’ characteristics and operative data on late survival. Hazard ratios, 95% confidence intervals, and levels of statistical significance (p values) were calculated. In all statistical tests a two-sided probability value less than 0.05 was considered significant. All data were analyzed with StatView version 5.0 (SAS Institute, Inc, Cary, NC).
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Results
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Patient Characteristics and Operative Data
The off-pump, skeletonized group was significantly older and had more distal anastomoses (Table 1).
Early Results
Table 2
shows early results. No 30-day mortality occurred in either group. The off-pump, skeletonized group had a significantly lower incidence of deep sternal infection. Of the 4 patients with deep sternal infection, 2 were dialysis patients.
Early Angiographic Results
Twenty-three patients (100%) in the on-pump, pedicled group and 137 patients (84.6%) in the off-pump, skeletonized group underwent early angiography (Table 3). The Fitzgibbon classification was used for graft evaluation [16]. Only Fitzgibbon A was considered to be patent. All of the 4 patients with occluded ITA grafts (2 left ITAs and 2 right ITAs) subsequently underwent percutaneous coronary intervention for revascularization of the branches of the coronary arteries in which the bypass failures had occurred.
Late Results
The median duration of follow-up was 3.4 ± 2.1 years (range, 1 month to 9.9 years). Kaplan–Meier 5-year survivals were 68.6% ± 5.5% in the off-pump, skeletonized group and 78.3% ± 8.6% in the on-pump, pedicled group (excluding hospital deaths; Fig 1). The difference between the two groups was not significantly different (p = 0.130, log-rank).
There were 30 late deaths in the off-pump, skeletonized group. Nine were attributed to cardiac causes: congestive heart failure (n = 5) and sudden death (n = 4). The other 21 deaths had noncardiac causes: cerebrovascular disease (n = 5), sepsis (n = 4), renal failure (n = 2), liver cirrhosis (n = 2), cancer (n = 2), and others (n = 6).
There were 8 late deaths in the on-pump, pedicled group. Six were attributed to cardiac causes: sudden death (n = 4), congestive heart failure (n = 1), and ventricular fibrillation (n = 1). The other 2 deaths were related to noncardiac reasons: cancer and pneumonia.
We examined the rates of freedom from cardiac-related mortality (Fig 2). The 5-year cardiac-related mortality-free rate was 86.1% ± 5.1% in the off-pump, skeletonized group and 87.0% ± 7.0% in the on-pump, pedicled group (excluding hospital deaths; Fig 1). This difference was not significant (p = 0.985, log-rank).
We examined the rates of freedom from cardiac-related events (including cardiac-related death, myocardial infarction, percutaneous coronary intervention, redo CABG, and congestive heart failure; Fig 3). The 5-year rate of freedom from cardiac-related events was 77.7% ± 5.7% in the off-pump, skeletonized group and 73.7% ± 9.2% in the on-pump, pedicled group (excluding hospital deaths; Fig 1). This difference was not significant (p = 0.709, log-rank).
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Fig 3. Freedom from cardiac-related events (including cardiac-related death, myocardial infarction, percutaneous coronary intervention, redo coronary artery bypass grafting, and congestive heart failure; p = 0.709). (ITA = internal thoracic artery.)
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Cox proportional hazard models (Table 4) were used to assess the effect of confounding factors on late death. Significant predictors of late death were dialysis, peripheral vascular disease, ejection fraction less than 0.40, and age.
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Comment
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The most dreaded complication when using BITA grafting in insulin-dependent diabetics is deep sternal infection. Patients who experience deep sternal infection have a 300% increase in hospital mortality rates [8]. However, insulin-dependent diabetics are believed to benefit the most from BITA grafting in the long run. Recently, because of its conservation of sternal blood flow, skeletonized BITA grafting has been reported to result in a lower incidence of deep sternal infection in diabetics than pedicled grafting [10, 11]. Our study demonstrated that a higher risk group, insulin-dependent diabetics, can benefit from skeletonized BITA grafting. We believe that a 0.6% risk of deep sternal infection is acceptable. This result supports our ongoing use of BITA grafting in insulin-dependent diabetics. One recent article reported a 3.2% incidence of deep sternal infection after BITA grafting in insulin-dependent diabetes patients—higher than in their single ITA grafting group (1.2%; not significant) [17]. These researchers used a pedicled technique with low electrocautery settings and ligation of the arterial branches. We believe that use of a skeletonized technique with an ultrasonic scalpel is more beneficial in terms of preservation of sternal vascularity and reduces the incidence of deep sternal infection. Indeed, improved sternal vascularity after skeletonized harvesting has been reported by single photon-emission computed tomography [18, 19].
The major concern with off-pump grafting and skeletonization is poor long-term clinical outcome. This could occur because of suboptimal anastomosis quality and incompleteness of revascularization [20]. Potential endothelial damage of the harvested ITAs and poor late clinical results are other concerns when the skeletonized technique is used [21, 22]. However, our study showed that the off-pump, skeletonized group was comparable to the conventional group in terms of early angiographic results and late cardiac results. The long-term survival of the conventional group tended to be better, but the conventional group was significantly younger. We think that this is a primary factor that explains the above phenomenon and also the limitations of this study. Indeed, our Cox proportional hazard model demonstrated that age was an independent risk factor for late death. Thus, we believe that optimal anastomosis and complete revascularization are possible in off-pump grafting. Furthermore, we believe that the ITAs were harvested safely by the skeletonized technique.
This was a retrospective study and was not randomized because the off-pump technique was introduced after the on-pump one. The on-pump group was smaller and younger, as we mentioned above. These are primary limitations of our study, although it is still one of the largest to have assessed the effects of off-pump, skeletonized BITA grafting in patients with insulin-dependent diabetes.
In conclusion, the incidence of deep sternal infection was reduced by use of the off-pump, skeletonization technique in patients with insulin-dependent diabetes. Early angiographic and late clinical results were similar between the two groups. These results support our surgical management of patients with insulin-dependent diabetes by off-pump grafting with bilateral skeletonized internal thoracic arteries.
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References
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Abstract
Introduction
