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Ann Thorac Surg 2002;74:S1371-S1376
© 2002 The Society of Thoracic Surgeons


Supplement: Cardiothoracic Techniques and Technologies

Bilateral skeletonized internal thoracic artery graftings in off-pump coronary artery bypass: early result of Y versus in situ grafts

Ki-Bong Kim, MD*a,b, Kwang Ree Cho, MDa,b, Woo-Ik Chang, MDa,b, Cheong Lim, MDa,b, Byung Moon Ham, MDa,b, Yong Lak Kim, MDa,b

a Department of Thoracic and Cardiovascular Surgery, Clinical Research Institute, Seoul National University Hospital, Seoul, South Korea
b Department of Anesthesiology, Clinical Research Institute, Seoul National University Hospital, Seoul, South Korea

* Address reprint requests to Dr Kim, Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, 28 Yeun-Kun Dong, Chong-Ro Ku, Seoul 110-744, South Korea
e-mail: kimkb{at}snu.ac.kr

Presented at the Eighth Annual Cardiothoracic Techniques and Technologies Meeting 2002, Miami Beach, FL, Jan 23–26, 2002.


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Use of bilateral skeletonized internal thoracic arteries (ITAs) in off-pump coronary artery bypass (OPCAB) retains several advantages that may eventually result in better patient outcomes. We compared the early results of OPCAB using bilateral ITAs as Y grafts with results of OPCAB using bilateral ITAs as in situ grafts.

Methods. A total of 223 consecutive patients who underwent OPCAB using bilateral skeletonized ITAs as Y grafts (group I, n = 113) or in situ grafts (group II, n = 110) were studied.

Results. Both the number of distal anastomoses per patient and the number of distal anastomoses per bilateral ITA were higher in group I (3.5 ± 1.0 and 2.9 ± 0.7) than in group II (3.0 ± 0.7 and 2.4 ± 0.5) (p < 0.01). Hospital mortality was 1.8% (2/113) in group I and 0.9% (1/110) in group II (p = ns). There were no differences in postoperative complications including atrial fibrillation (13.3% vs 10.9%), perioperative myocardial infarction (0.9% vs 2.7%), mediastinitis (0.9% vs 1.8%), and hypoperfusion syndrome (0.9% vs 0%) between groups I and II (p = ns). Postoperative coronary angiographies performed in 110 patients in group I and 108 patients in group II showed 99.0% (382/386) overall patency and 99.4% (319/321) patency for distal anastomoses using ITAs in group I, and 98.1% (312/318) overall patency and 98.1% (258/263) patency for distal anastomoses using ITA in group II. There were no significant differences in graft patency rates between the two groups (p = ns).

Conclusions. Our results demonstrate that OPCAB using bilateral skeletonized ITAs is technically feasible, with excellent graft patency. Using bilateral skeletonized ITAs as Y grafts increases the number of distal anastomoses that can be performed and does not cause additional postoperative morbidity.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Development of a lower saphenous vein graft patency rate compared with that of internal thoracic artery (ITA) has encouraged surgeons to examine coronary artery bypass grafting (CABG) with arterial grafts to improve the long-term outcome of myocardial revascularization. Use of the left internal thoracic artery for the left anterior descending coronary artery (LAD) with supplemental saphenous vein grafts has been the standard CABG throughout the world. Recently, advantages such as enhanced survival and greater freedom from reinterventions with the use of two ITAs over one have been demonstrated [1]. With resurgent interest in CABG without cardiopulmonary bypass (ie, off-pump CABG, or OPCAB), the surgical results of OPCAB have demonstrated several advantages by avoiding the potentially detrimental effects of cardiopulmonary bypass and eliminating intraoperative global myocardial ischemia [2, 3]. However, technical complexities and lack of angiographic results make surgeons hesitant to perform OPCAB using multiple arterial grafts.

The aims of this study were: 1) to assess the feasibility of OPCAB using bilateral skeletonized ITAs, and 2) to compare the early results after OPCAB using bilateral ITAs as either Y or in situ grafts.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
A total of 223 consecutive patients who underwent OPCAB for multivessel coronary artery disease, with bilateral skeletonized ITAs as either Y grafts or in situ grafts between August 1999 and December 2001, were studied in a prospective, nonrandomized manner. A computer-based patient database system was used for this prospective study. These 223 OPCABs were 83.2% (223/268) of the total isolated CABGs for multivessel disease performed during the same period. Patients who underwent conventional CABG (32 patients) or OPCAB using single ITA or ITA as a free graft anastomosed on the ascending aorta (13 patients) were excluded from the study. The early results of OPCAB using bilateral ITAs as Y grafts (group I, n = 113) were compared with results of OPCAB using bilateral ITAs as in situ grafts (group II, n = 110). There were no differences between the two groups in terms of sex, age, preoperative risk factors, ratio of unstable to stable angina, left ventricular ejection fraction measured by transthoracic echocardiography, and urgent or emergent operations. The number of patients with triple-vessel disease was larger in group I (p < 0.01); in contrast, the number of patients with left main disease was larger in group II (p < 0.05) (Table 1). All patients stopped taking aspirin the day before surgery and resumed aspirin (300 mg/d) beginning 1 day postoperatively. Postoperative (1.3 ± 1.0 days) coronary angiographies were performed in 97.3% (110/113) of patients in group I and 98.2% (108/110) of patients in group II.


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Table 1. Preoperative Characteristics and Risk Factors of the Study Patients

 
Surgical technique
All operations were performed through a median sternotomy incision, and a cell-saving device was routinely used. Body temperature was maintained at normothermia using adequate room temperature, warm circulating water blankets, and warm infusion solutions.

A standard skeletonizing technique for harvesting the ITA was used in all patients. We routinely opened the pleura before ITA dissection to facilitate exposure. To avoid thermal injury to the ITA, the cautery setting was kept on low throughout the dissection. Cautery was used to cut the endothoracic fascia and to expose the underlying ITA. Using scissors or the tip of the cold cautery device for dissection, the ITA was gently separated from the chest wall, leaving the accompanying veins, fascia, and adipose tissue in place. The sternal and intercostal branches were clipped just after the origin and divided between the two silver clips using scissors. Care was taken to avoid any damage to the sites of branch origin to prevent dissection of the ITA. Throughout the dissection, the ITA was sprayed with warm diluted papaverine solution to minimize spasm and to prevent desiccation. If using bilateral ITAs as in situ or Y grafts did not achieve complete revascularization, a short lower extension of the median incision was made to harvest the right gastroepiploic artery in a skeletonized fashion. If significant narrowing of the celiac axis was found on the preoperative abdominal aortogram or if there was a past medical history of upper abdominal surgery, the radial artery or saphenous vein graft (SVG) was harvested instead. After systemic heparinization, the ITAs were clipped distally. The skeletonized grafts were then immersed in a 10-mL syringe filled with warm diluted papaverine saline solution (1 mg/mL) and allowed to pharmacologically dilate. The ITA was immersed for 5 to 10 minutes in the syringe vertically embedded in the open pleural cavity. We did not use intraluminal injection of papaverine solution.

OPCAB technique
The patients were heparinized with an initial dose of 1.5 mg/kg of heparin, and periodically received supplemental doses to maintain an activated clotting time of more than 300 seconds. One or two supplemental doses of heparin were required during the OPCAB procedure. After the pericardium was opened and the right pleuropericardial fat pads transected, two deep pericardial sutures were placed to facilitate pericardial retraction for cardiac elevation and exposure. To reduce the heart rate to less than 70 to 80 beats per minute and to minimize myocardial oxygen consumption, most of the patients were given boluses or continuous infusion of ß-blockers such as esmolol or adenosine. Ischemic preconditioning was not performed in most of the cases. Anesthesia management, including volume loading and placing the patient in the Trendelenburg position, controlled hemodynamic derangement during displacement or manipulation of the heart. To reduce the amplitude of ventricular wall movement, a compression-type mechanical stabilizer (Ultima Stabilizer; Guidant, Cupertino, CA) or suction-type mechanical stabilizer (Octopus; Medtronic, Minneapolis, MN) was used. To obtain a bloodless operative field, internal vascular control was achieved with a flow occluder (Florester, Bio-Vascular Inc, Saint Paul, MN) or intracoronary shunt (FloCoil Shunt; Guidant, Cupertino, CA). A Blower/Mister (Visuflo; Baxter Healthcare, Midvale, UT) using carbon dioxide gas (flow rate <=3 L/min) or a microsucker system with a rubber tip was also used to obtain a bloodless surgical field. The most critical vessel, the LAD in almost all patients, was revascularized first to provide a backup to the less critical area. The distal anastomosis was constructed using a continuous technique with 8-0 polypropylene sutures. If needed, proximal anastomoses on the ascending aorta were constructed after distal anastomoses, using a single partial clamping of the aorta and a 7-0 polypropylene continuous suture. Protamine was not given at the end of the procedure.

Revascularization strategies
Bilateral ITAs were preferred for use as in situ grafts for myocardial revascularization on the assumption that multiple blood sources would be better than a single blood source to improve long-term outcome. Both ITAs were used when possible for revascularization of the left coronary territory. The right ITA was used to revascularize the LAD by crossing the midline, the ramus or high obtuse marginal branch through the transverse sinus, and sometimes the right coronary artery or posterior descending artery as an in situ graft. If the right ITA was too short to reach the left coronary territory or if the left coronary territory could not be completely revascularized with bilateral in situ ITA grafts, a Y graft was constructed before starting the distal anastomoses. In most cases of Y graft construction, the right ITA was divided at its proximal section and was anastomosed to the side of the left ITA in a Y fashion using an 8-0 polypropylene continuous suture. Most of these end-to-side Y anastomoses were performed at the level of the pulmonary artery, and occasionally the right ITA was anastomosed to the distal left ITA unless it reached an optimal vessel such as the right coronary territory. If use of the bilateral ITAs as in situ or Y grafts did not achieve complete revascularization, the right gastroepiploic artery, radial artery, or saphenous vein was used for additional revascularization.

Statistical analysis
Statistical analysis was performed with the Statistical Analysis System software package (version 6.12; SAS Institute, Cary, NC). The significance of differences between the two groups was assessed by the unpaired two-tailed t test or {chi}2 test. All results were expressed as mean ± standard deviation, and a p value of less than 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
The average number of distal anastomoses per patient was larger in group I than in group II (3.5 ± 1.0 vs 3.0 ± 0.7; p < 0.01). The average number of distal anastomoses per bilateral ITA was also larger in group I than in group II (2.9 ± 0.7 vs 2.4 ± 0.5; p < 0.01). The number of distal anastomoses using the left ITA was larger in group II than in group I (1.2 ± 0.4 vs 1.4 ± 0.5; p < 0.05), and the number using the right ITA was larger in group I than in group II (1.7 ± 0.6 vs 1.0 ± 0.1; p < 0.01). A greater number of patients in group I needed the sequential anastomosis than in group II (72.6% vs 41.8%; p < 0.01), and a significantly larger number of sequential anastomoses using ITAs was performed in group I than in group II (30.4% vs 16.4%; p < 0.01) (Table 2).


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Table 2. Comparison of Distal Anastomoses

 
When the coronary arteries were classified as anterior (LAD, diagonal branches, ramus intermedius, and proximal or middle right coronary artery), posterior (obtuse marginal branches), and inferior (distal right coronary artery, posterior descending artery, and posterolateral branches) according to their location, the anastomotic proportions of territory in each group were similar between the two groups (p = ns; Table 2). The territories revascularized by each ITA were different between the two groups. In group I, the left ITA was used to revascularize the LAD territories in 93.8% (106/113) of patients. In group II, the right ITA was used to revascularize the LAD territories in 80.9% (89/110) of patients (Table 3). There were no significant differences in the use of other grafts such as right gastroepiploic artery, radial artery, or saphenous vein between the two groups (p = ns). Total arterial revascularizations without using a saphenous vein graft were performed in 93.8% (106/113) of patients in group I and 90.9% (100/110) in group II (p = ns; Table 4).


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Table 3. Target Coronary Territories by Bilateral Internal Thoracic Arteries

 

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Table 4. ConduitS

 
Operative mortalities were 1.8% (2/113) in group I and 0.9% (1/110) in group II (p = ns). There were no significant differences in the incidence of postoperative morbidities such as atrial fibrillation (13.3% vs 10.9%), perioperative myocardial infarction (0.9% vs 2.7%), acute renal failure (0.9% vs 0.9%), mediastinitis (0.9% vs 1.8%), bleeding reoperation (6.2% vs 1.8%), or hypoperfusion syndrome (0.9% vs 0%), between group I and II (p = ns). We did not experience any low cardiac output syndrome or stroke in either group.

Postoperative coronary angiographies demonstrated a 99.0% patency rate in group I and 98.1% in group II. There were no differences in graft patency rates between the two groups (p = ns) (Table 5).


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Table 5. Postoperative Angiographic Patency Rates

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
This study reveals two main findings. First, OPCAB using bilateral skeletonized ITAs is technically feasible with excellent graft patency. Second, using the bilateral skeletonized ITAs as Y grafts demonstrates an increased number of distal anastomoses and does not increase additional postoperative morbidities (including hypoperfusion syndrome or low cardiac output syndrome) as compared with in situ grafts.

Enhanced long-term survival has been shown when the left ITA is grafted to the LAD rather than the SVG, or when bilateral ITAs are used rather than a single ITA in patients with triple-vessel disease [1, 4]. The skeletonized technique for harvesting the ITA allowed easier use of bilateral ITAs with good results [5, 6]. Those results have provided the foundation for using more arterial conduits to achieve complete myocardial revascularization. With resurgent interest in OPCAB, there have been concerns about accuracy and patency of the grafts and the long-term outcome. Ömeroglu and associates [7] demonstrated a significantly lower patency rate for SVG (47.1%) than for ITA (95.7%) in 3-year follow-up results after OPCAB. They suggested that the decreased patency rate for SVG might result in part from the type of graft, and the exposure and quality of stabilization during OPCAB. Regional cardiac wall immobilization with specially designed stabilizer systems provides excellent stabilization of the target area, enables surgeons to perform coronary anastomoses safely without cardiopulmonary bypass, and greatly enhances graft patency in a predictable manner [8]. Mariani and associates [9] demonstrated that procoagulant activity was increased in the first 24 hours after OPCAB, and suggested not antagonizing the heparin with protamine at the end of the procedure, along with more aggressive perioperative anticoagulation policy for patients undergoing OPCAB than that for patients undergoing conventional CABG with cardiopulmonary bypass. Kim and colleagues [10] also demonstrated that the patency rate of saphenous vein graft after OPCAB was significantly lower than that of arterial grafts as seen in early postoperative coronary angiographies, and was also significantly lower than the saphenous vein graft patency rates for conventional CABG and on-pump beating CABG as seen in 1-year postoperative coronary angiographies. They suggested not antagonizing the heparin with protamine at the end of the OPCAB procedure, and performing the OPCAB using exclusively arterial grafts to avoid the low patency rate and sequelae of saphenous vein graft occlusion. However, technical difficulties and lack of angiographic results make surgeons hesitant to perform OPCAB using multiple arterial grafts. Mack and associates [11] reviewed publications that examined outcomes of left ITA grafting in conventional CABG and minimally invasive direct CABG. They suggested that early graft patency after both techniques could confidently be stated as being 90% or greater. Calafiore and associates [12] demonstrated the feasibility of arterial revascularization without cardiopulmonary bypass, with results similar to those obtained with cardiopulmonary bypass. They showed a 98.9% patency rate of arterial grafts at about 1 month after OPCAB. Postoperative coronary angiographies were performed in the present study 1.3 ± 1.0 days postoperatively. These data showed that the patency rate for distal anastomoses using bilateral ITAs was 99.4% (319/321) in patients with Y grafts and 98.1% (256/261) in patients with in situ grafts (p = ns), demonstrating excellent early patency comparable to those of recent reports [11, 12], and suggested the feasibility OPCAB using bilateral skeletonized ITAs.

Although using bilateral skeletonized ITAs increases the difficulty and duration of the operation, it retains several advantages that may eventually result in better long-term outcomes for patients. The advantages of bilateral skeletonized ITA dissection are that the dissected ITA is longer and that its spontaneous blood flow is greater than that of the pedicled ITA [13], allowing use of both ITAs as grafts to all necessary vessels requiring surgical revascularization. Additional advantages are that collateral blood supply to the sternum is preserved, enabling more rapid healing and decreasing the risk of deep sternal infection [14]. The use of bilateral ITAs as in situ grafts for myocardial revascularization was preferred in the present study based on the belief that multiple blood sources may be better than a single blood source for improving long-term outcome. However, using bilateral ITAs as in situ grafts sometimes does not achieve complete arterial revascularization for patients with multivessel coronary disease. If the right ITA was too short to reach the left coronary system, or if the left coronary system could not be completely revascularized with bilateral in situ ITA grafts, the right ITA was divided at its proximal part to construct a Y graft. Construction of a Y graft further increases the length of the skeletonized ITA, and allows the extensive use of bilateral ITA grafts to revascularize the left coronary system as well as the right coronary system [15]. The present study showed that the number of distal anastomoses per bilateral ITA was 2.9 ± 0.7 in patients with Y grafts and 2.4 ± 0.5 in patients with in situ grafts, demonstrating greater versatility of Y grafts compared with in situ grafts (p < 0.01). Although construction of Y grafts has shown an increase in total ITA free flow [16], there is a concern that graft flow may be inadequate, resulting in a hypoperfusion syndrome manifested by low cardiac output, left ventricular failure, increasing pulmonary wedge pressure, hypotension, and cardiac arrest [17]. There was no low cardiac output syndrome in patients with Y grafts or in situ grafts. There was only one case of hypoperfusion syndrome in a patient with Y grafts, not a significant difference in the incidence of hypoperfusion syndrome between patients with Y grafts and in situ grafts. We believe that our low incidence of low cardiac output syndrome or hypoperfusion syndrome may result from the OPCAB technique, by avoiding intraoperative myocardial ischemia, as well as from our method of meticulous ITA dissection and pharmacological ITA dilatation to minimize surgical trauma and perioperative spasm of the ITA.

Multiple retrospective clinical studies have documented an increased risk of sternal wound complication associated with bilateral ITA grafting, particularly in diabetic patients [18]. The increased risk of wound complications appears to be caused by sternal ischemia. One anatomic study predicted a decrease in sternal blood flow resulting from ITA dissection [19], and postoperative flow studies have confirmed that sternal blood flow is decreased postoperatively by ITA dissection, more after bilateral ITA grafting than after single ITA grafting [20]. The skeletonized ITA dissection leaves those accompanying veins, muscle, and endothoracic fascia in place and preserves the collateral blood supply to the sternum, enabling more rapid healing and decreasing the risk of infection. De Jesus and Acland [19] suggested that all ITA branches be ligated as close as possible to the main vessel trunk to minimize damage to the collateral blood supply of the sternum. Studies of bilateral skeletonized ITA graftings have demonstrated similar incidences of deep sternal infection in elderly and diabetic patients, and using bilateral skeletonized ITAs is suggested as a good surgical revascularization option even in elderly or diabetic patients [5, 6]. The present study showed that the postoperative incidence of mediastinitis was 0.9% in patients with Y grafts and 1.8% in patients with in situ grafts, demonstrating comparable results with previous studies.

In conclusion, OPCAB using bilateral skeletonized ITAs is feasible and demonstrates excellent early graft patency. Using bilateral skeletonized ITAs as Y grafts increased the number of distal anastomoses that could be performed and did not increase operative morbidity, compared with those of in situ grafts.


    Acknowledgments
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
We thank Dawn Schuessler for the preparation of the manuscript.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Lytle B.W., Blackstone E.H., Loop F.D., et al. Two internal thoracic artery grafts are better than one. J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
  2. Matata B.M., Sosnowski A.W., Galiñanes M. Off-pump bypass graft operation significantly reduces oxidative stress and inflammation. Ann Thorac Surg 2000;69:785-791.[Abstract/Free Full Text]
  3. Ascione R., Lloyd C.T., Underwood M.J., Lotto A.A., Pitsis A.A., Angelini G.D. Inflammatory response after coronary revascularization with or without cardiopulmonary bypass. Ann Thorac Surg 2000;69:1198-1204.[Abstract/Free Full Text]
  4. Cameron A., Davis K.B., Green G., Schaff H.V. Coronary bypass surgery with internal thoracic artery grafts: effects on survival over a 15-year period. N Engl J Med 1996;334:216-219.[Abstract/Free Full Text]
  5. Gurevitch J., Paz Y., Shapira I., et al. Routine use of bilateral skeletonized internal mammary arteries for myocardial revascularization. Ann Thorac Surg 1999;68:406-412.[Abstract/Free Full Text]
  6. Kramer A., Mastasa M., Paz Y., et al. Bilateral skeletonized internal thoracic artery grafting in 303 patients seventy years and older. J Thorac Cardiovasc Surg 2000;120:290-297.[Abstract/Free Full Text]
  7. Ömeroglu S.N., Kirali K., Güler M., et al. Midterm angiographic assessment of coronary artery bypass grafting without cardiopulmonary bypass. Ann Thorac Surg 2000;70:844-850.[Abstract/Free Full Text]
  8. Subramanian V.A. Less invasive arterial CABG on a beating heart. Ann Thorac Surg 1997;63:S68-S71.
  9. Mariani M.A., Gu Y.J., Boonstra P.W., Grandjean J.G., van Oeveren W., Ebels T. Procoagulant activity after off-pump coronary operation: is the current anticoagulation adequate?. Ann Thorac Surg 1999;67:1370-1375.[Abstract/Free Full Text]
  10. Kim K.-B., Lim C., Lee C., et al. Off-pump coronary artery bypass may decrease the patency of saphenous vein grafts. Ann Thorac Surg 2001;72:S1033-S1037.[Abstract/Free Full Text]
  11. Mack M.J., Osborne J.A., Shennib H. Arterial graft patency in coronary artery bypass grafting: what do we really know?. Ann Thorac Surg 1998;66:1055-1059.[Abstract/Free Full Text]
  12. Calafiore A.M., Teodori G., Di Giammarco G. Multiple arterial conduits without cardiopulmonary bypass: early angiographic results. Ann Thorac Surg 1999;67:450-456.[Abstract/Free Full Text]
  13. Wendler O., Tscholl D., Huang Q., Schäfers H.-J. Free flow capacity of skeletonized versus pedicled internal thoracic artery grafts in coronary artery bypass grafts. Eur J Cardio-thorac Surg 1999;15:247-250.[Abstract/Free Full Text]
  14. Parish M.A., Asai T., Grossi E.A., 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]
  15. Calafiore A.M., Contini M., Vitolla G., et al. Bilateral internal thoracic artery grafting: longterm clinical and angiographic results of in situ versus Y grafts. J Thorac Cardiovasc Surg 2000;120:990-998.[Abstract/Free Full Text]
  16. Royse A.F., Royse C.F., Groves K.L., Bus B., Yu G. Blood flow in composite arterial grafts and effect of native coronary flow. Ann Thorac Surg 1999;68:1619-1622.[Abstract/Free Full Text]
  17. Loop F.D., Thomas J.D. Hypoperfusion after arterial bypass grafting. Ann Thorac Surg 1993;56:812-813.[Medline]
  18. Grossi E.A., Esposito R., Harris L.J., et al. Sternal wound infections and use of internal mammary artery grafts. J Thorac Cardiovasc Surg 1991;102:342-347.[Abstract]
  19. De Jesus R.A., Acland R.D. Anatomic study of the collateral blood supply of the sternum. Ann Thorac Surg 1995;59:163-168.[Abstract/Free Full Text]
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