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Ann Thorac Surg 2004;78:2050-2053
© 2004 The Society of Thoracic Surgeons


Original Article: Cardiovascular

Routine Use of Bilateral Skeletonized Internal Thoracic Artery Grafts in Middle-Aged Diabetic Patients

Olivier M. Bical, MD*, Wassim Khoury, MD, Yves Fromes, MD, PhD, Marc Fischer, MD, Miguel Sousa Uva, MD, Gilles Boccara, MD, Philipe H. Deleuze, MD

Department of Cardiac Surgery, Fondation Hopital Saint Joseph, Paris, France

Accepted for publication June 4, 2004.

* Address reprint requests to Dr Bical, Fondation Hopital Saint Joseph, 185 rue Raymond Losserand, Paris, 75674, Cedex 14, France (E-mail: ombical{at}hopital-saint-joseph.org).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: The purpose of this study was to determine whether middle-aged diabetic patients aged less than 70 years could have routine use of bilateral skeletonized internal thoracic artery grafting without an increased surgical risk.

METHODS: Between January 1997 and December 2003, 712 consecutive patients aged less than 70 years underwent bilateral internal thoracic artery grafting. Among these, 164 were diabetic and underwent bilateral internal thoracic artery grafting without other preoperative selection than age. The postoperative results of these 164 nonselected consecutive diabetic patients were compared to these of the 548 nondiabetic patients.

RESULTS: The operative mortality rate was 4.3% (7 patients) in the diabetic group and 2.4% (13 patients) in the nondiabetic group (p = not significant [NS]). Deep sternal wound infection was observed in 2 patients (1.1%) in the diabetic group and in 6 patients (1.2%) in the nondiabetic group (p = NS). There were no significant difference in the morbidity rate between the two groups except for renal failure without dialysis (6.7% in the diabetic group vs 2.0% in the nondiabetic group, p < 0.01).

CONCLUSIONS: Routine use of bilateral internal thoracic artery grafting was performed in nonselected middle-aged diabetic patients without increased morbidity. The low rate of deep wound infections could be related to the skeletonized technique of internal thoracic artery harvesting.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Diabetes mellitus is a major independent risk factor for coronary artery disease. Arteriosclerosis accounts for about 80% of all deaths from diabetes, of which three-quarters are from coronary artery disease [1]. Coronary arteriosclerosis proceeds at a more rapid rate and tends to be more extensive in diabetic patients [1]. There is still no firm consensus on the better type of coronary revascularization for diabetic patients. Multivessel diabetic patients treated with stenting had a worse one-year outcome than patients assigned to coronary artery bypass grafting (CABG) or nondiabetics treated with stenting (arterial revascularization therapy study [ARTS]) [2]. However, this ARTS trial does not provide a definitive answer to the preferred revascularization therapy in diabetic patients as drug eluting stents and bilateral internal thoracic artery (BITA) are not used in this study. The indisputable survival benefit of grafting one internal thoracic artery (ITA) on the left anterior descending coronary artery is because of its superior long-term patency [3]. The superior performance of this conduit led to an increase in the use of BITA in an attempt to avoid late saphenous graft closure and improve event-free survival [4, 5]. Several studies that appeared during the past few years confirmed this and reported long-term survival benefit after BITA compared to single ITA grafting [6, 7]. As the survival benefit after BITA grafting was observed after 10 or 15 years, the extensive use of BITA seems justified only for patients aged less than 70 years [8]. However, BITA grafting has been associated with a fourfold to 20-fold increase in the incidence of sternal wound infections in diabetic patients [9, 10]. If the use of BITA in diabetics is associated with higher morbidity and mortality, one could question the wisdom of using BITA grafting for a potential long-term benefit that would be neutralized by an increased early risk. The mobilization of the ITA as a skeletonized vessel reduces postoperative morbidity and, particularly, the incidence of sternal wound infections [11]. Our previous limited series performed bilateral skeletonized ITA grafting in diabetic patients without increased morbidity and mortality [12]. However, this series was limited by an intentional selection process as it was limited to young patients and excluded obese women [12]. The aim of this study was to retrospectively analyze our policy since 1996 of routine use of bilateral skeletonized ITA grafting in middle-aged diabetic patients without preoperative selection.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Between January 1997 and December 2003, 771 consecutive patients aged less than 70 years underwent first-time CABG in our unit for multivessel disease. Among these patients, 5 underwent one ITA graft with other arterial grafts and 54 underwent one ITA graft with venous grafts mainly for technical reasons of ITA harvesting or quality of the second ITA graft. The 59 patients with only one ITA graft were excluded from the study. The 712 other patients less than 70-years old underwent BITA grafting without other preoperative selection. Among these we identified 548 nondiabetic patients (nondiabetic group) and 164 diabetic patients (diabetic group), defined by a preoperative plasma fasting glucose greater than 1.25 mg/dL (7.0 mmol/L). Diabetes was either insulin dependent (n = 35; 21.3%) or treated by oral hypoglycemic agents or diet (n = 129; 78.7%). Preoperative characteristics of both diabetic and nondiabetic patients are listed in Table 1. These characteristics reflect an absence of selective policy of indications for using BITA. In this retrospective study, coronary revascularization with BITA has been routinely used in diabetics as in the nondiabetic population without any preoperative selection.


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Table 1. Preoperative Demographics
 
Surgery
As for all coronary revascularization, the infection prophylaxis was carried out by a second generation cephalosporin stopped in all cases by the end of surgery. All operations were performed as described previously using a skeletonized technique for ITA harvesting [11]. Normothermic cardiopulmonary bypass was used and myocardial protection was achieved by intermittent antegrade warm blood cardioplegia. Cardiopulmonary bypass times were 83 ± 25 mn in diabetic patients and 82 ± 25 mn in nondiabetic patients (p = NS). Cross – clamp times were 61 ± 19 mn and 60 ± 19 mn in the diabetic and nondiabetic patients, respectively (p = NS). Bilateral internal thoracic arteries were used preferentially to graft the left coronary system [11]. The sternum was closed avoiding bone wax with interrupted 6 to 8 stainless-steel wires, interrupted double-layer polydiaxone musculofascial sutures, and polydiaxone absorbable continuous dermal suture or cutaneous staples. In obese patients, we used 10 wires for the sternum closure and subcutaneous high-suction catheter drainage for 3 to 5 days. After surgery all patients had blood glucose determination at 3-hour intervals and continuously adapted insulin infusion to a blood glucose target level of 150 to 200 mg/dL until postoperative day 2. Thereafter, either subcutaneous insulin or the oral hypoglycemic agents were resumed.

Definitions
Deep sternal wound infection was defined by infection involving tissues beneath the subcutaneous tissue with at least one of the following: positive mediastinal culture; evidence of mediastinitis at operation; fever, chest pain, or sternal instability, as well as either purulent drainage from the mediastinum or a positive blood culture or culture of mediastinal drainage. Superficial wound infection involved only skin or subcutaneous tissue below the incision with either purulent drainage, organism isolated, or incision opened by the surgeon [12].

Follow-Up
Patients were examined by the surgeon or the referring cardiologist 2 months after operation and the follow-up was 100% complete.

Statistical Methods
Data were expressed as the mean ± standard deviation. Statistical analysis was performed using Fisher's exact test and t test for discrete variables and unpaired t test for continuous variable comparisons. Statistical significance was established at a p value less than 0.05. Statistical analysis was also carried out using the software Stata for Macintosh (StataCorp LP, College Station, TX). For the multivariate analysis, we used the multinomial logistic regression model.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Mortality
Operative mortality within 30 days was 4.3% (7 patients) in the diabetic group and 2.4% (13 patients) in the nondiabetic group (p = NS). The cardiac-related operative mortality was similar in the two groups (1.83% for the diabetic group vs 1.82% for the nondiabetic group, p = NS). In contrast, the noncardiac-related operative mortality (multiple organ failure) was higher in the diabetic group (2.44%, 4 patients) than in the nondiabetic group (0.55%, 3 patients, p < 0.05).

Morbidity
Deep sternal wound infection developed in 2 patients in the diabetic group (1.2%) and in 6 patients in the nondiabetic group (1.1%) (p = NS). The bacteriologic findings were similar in diabetic and nondiabetic groups with mainly staphylococcus infections. All patients with deep sternal wound infection were treated successfully by intravenous antibiotics, multiple high-suction catheter drainage and rewiring. Superficial wound infection treated by local debridement was noted in 9 patients (5.5%) in the diabetic group and in 16 patients in the nondiabetic group (2.9%). The comparison of diabetic and nondiabetic patients by monovariate and multivariate analysis revealed renal failure as a predictive factor for sternal infection (p < 0.002). Furthermore, comparison of insulin-dependent and noninsulin-dependent patients confirmed only renal failure as a predictive factor for sternal infection (p < 0.002). There were no cases of sternal wound infection after discharge from the hospital. The incidences of nosocomial pneumonia and of cerebrovascular accidents were comparable in the two groups (Table 2).


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Table 2. Postoperative Morbidity
 

    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
This retrospective study showed that with skeletonized dissection, BITA grafting could be used routinely in middle-aged diabetic patients without increased cardiac-related mortality and morbidity. Diabetes is an independent major risk factor for coronary arteriosclerosis. Patients with diabetes are at increased risk of myocardial infarction and have more extensive and severe coronary artery disease than the general population [1]. Multivessel diabetic patients treated with stenting had a worse one-year outcome than patients assigned to CABG [2]. However, there is still no firm consensus on the better type of coronary revascularization for diabetic patients. The rationale for coronary revascularization with both ITA is based on the superior durability of this conduit and the reduction in the rate of adverse cardiac events, and in the 10-year or 15-year survival [4, 5]. If the long-term benefit of the use of BITA grafting in a diabetic population is to be seen, there must be no increase in the early risk. The aim of this study was to determine if routine use of BITA grafting in the diabetic population does not increase early risks for a potential late benefit. Diabetes, either treated by insulin or not, increases the risk of surgical wound infection whatever the type of operation. Several studies have shown diabetes to be a risk factor for sternal wound infection either independently or in association with other factors such as obesity, gender, age, tobacco use, or respiratory disease [9, 13, 14]. Mobilization of the ITA leads to devascularization of the ipsilateral hemisternum; if both arteries are mobilized the entire sternum is significantly devascularized [15]. Because devascularization itself is a risk factor for wound infection, BITA take-down in diabetic patients is traditionally considered hazardous. The use of skeletonization for ITA harvesting has been associated to a higher residual sternal blood flow than that dissected as a pedicle [16]. Skeletonization using accurate and atraumatic ligation of branches as close as possible to the ITA itself ensures maximum residual collateral blood flow to the sternum [17]. The skeletonization dissection of ITA is more technically demanding but the late patency rate is comparable to that of pedicled grafts [18]. Limited clinical series showed that skeletonization dissection of both ITAs can be used for CABG in patients with diabetes mellitus without increased morbidity and mortality [12, 19]. However, these series are limited by an intentional selection process, as they are limited to young patients and excluded obese women. Our study shows that bilateral skeletonized ITAs could be routinely used in a middle-aged diabetic population without increased cardiac-related mortality and morbidity. Our only criteria of selection is age (< 70 years old) as the benefit of BITA revascularization is observed at long term (10 or 15 years). The age of our patients, the presence of obese women, of tobacco users, of patients with chronic obstructive pulmonary disease, and of a great number of insulin-dependent diabetes mellitus confirm our policy of nonselection and real routine use of BITA grafting. These results were achieved through the conjunction of various factors, including ITA harvesting technique, meticulous wound closure (particularly in obese women), and continuous aggressive blood glucose control throughout the perioperative period [20]. The higher noncardiac-related mortality in the diabetic population is probably related to the diffuse character of their atherosclerotic disease. From this study we conclude that with appropriate surgical technique, BITA coronary artery grafting does not carry an increased operative risk for all diabetic patients aged less than 70 years. However, the advantage of this kind of surgical revascularization in terms of event-free survival remains to be compared in diabetic patients to the new devices used in percutaneous revascularization.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Webster MWI. What cardiologists need to know about diabetes Lancet 1997;350:SI23-8.
  2. Abizaid A, Costa MA, Centemero M, et al. Clinical and economic impact of diabetes mellitus on percutaneous and surgical treatment of multivessel coronary disease patients. Insights from the arterial revascularization therapy study (ARTS) trial Circulation 2001;104:533-538.[Abstract/Free Full Text]
  3. Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal mammary artery graft on 10 year survival and other cardiac events N Engl J Med 1986;314:1-6.[Abstract]
  4. Barner HB, Standeven JW, Reese J. Twelve year experience with internal mammary artery for coronary artery bypass J Thorac Cardiovasc Surg 1985;90:668-675.[Abstract]
  5. Naunheim KS, Barner HB, Fiore AC. Results of internal thoracic artery grafting over 15 years: single versus double grafts (update) Ann Thorac Surg 1992;53:716-718.[Medline]
  6. Carrel T, Horber P, Turina M. Operation for two vessel coronary artery disease: midterm results of bilateral ITA grafting versus unilateral ITA and saphenous vein grafting Ann Thorac Surg 1996;62:1289-1294.[Abstract/Free Full Text]
  7. Pick AW, Orszulak TA, Anderson BJ, Schaff HV. Single versus bilateral internal mammary artery grafts: 10 year outcome analysis Ann Thorac Surg 1997;64:599-605.[Abstract/Free Full Text]
  8. Lytle BW, Blackstone EH, Loop FD, et al. Two internal thoracic artery grafts are better than one J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
  9. Cosgrove DM, Lytle BW, Loop FD, et al. Does bilateral internal mammary artery grafting increase surgical risk? J Thorac Cardiovasc Surg 1998;95:850-856.
  10. Grossi EA, Esposito R, Harris LJ, et al. Sternal wound infections and use of internal mammary artery grafts J Thorac Cardiovasc Surg 1991;102:342-347.[Abstract]
  11. Bical OM, Braunberger E, Fischer M, et al. Bilateral skeletonized mammary artery grafting: experience with 560 consecutive patients Eur J Cardiothorac Surg 1996;10:971-976.[Abstract]
  12. Sousa Uva M, Braunberger E, Fischer M, et al. Does bilateral internal thoracic artery grafting increase surgical risk in diabetic patients? Ann Thorac Surg 1998;65:2051-2055.
  13. Kouchoukos NT, Wareing TH, Murphy SF, et al. Risks of bilateral internal mammary artery bypass grafting Ann Thorac Surg 1990;49:210-219.[Abstract]
  14. HE GW, Ryan WH, Acuff TE, et al. Risk factors for operative mortality and sternal wound infection in bilateral mammary artery grafting J Thorac Surg 1994;107:196-202.[Abstract/Free Full Text]
  15. Seyfer AC, Shiver CD, Miller TR, Graeber GM. Sternal blood flow after median sternotomy and mobilization of the internal mammary arteries Surgery 1988;104:899-904.[Medline]
  16. Parish MA, Asai T, Grossi EA, et al. The effects of different techniques of internal mammary artery harvesting on sternal blood flow J Thorac Cardiovasc Surg 1992;104:1303-1307.[Abstract]
  17. De Jesus RA, Acland RD. Anatomic study of the collateral blood supply of the sternum Ann Thorac Surg 1995;59:163-168.[Abstract/Free Full Text]
  18. Calafiore AM, Vitolla G, Iaco AL, et al. Bilateral internal mammary artery grafting: midterm results of pedicled versus skeletonized conduits Ann Thorac Surg 1999;67:1637-1642.[Abstract/Free Full Text]
  19. Matsa M, Paz Y, Gurevitch J, et al. Bilateral skeletonized internal thoracic artery grafts in patients with diabetes mellitus J Thorac Cardiovasc Surg 2001;121:668-674.[Abstract/Free Full Text]
  20. Furnary AP, Gao G, Grunkemeier GL, et al. Continuous insulin infusion reduces mortality in patients with diabetes undergoing coronary artery bypass grafting J Thorac Cardiovasc Surg 2003;125:1007-1021.[Abstract/Free Full Text]



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