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Ann Thorac Surg 2001;71:1224-1228
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Early results of coronary grafting using ultrasonically skeletonized internal thoracic arteries

Tetsuya Higami, MDa, Teruo Yamashita, MDa, Hideaki Nohara, MDa, Kazuhiko Iwahashi, MDa, Tsutomu Shida, MDa, Kyoichi Ogawa, MDa

a Division of Cardiovascular Surgery, Hyogo Brain and Heart Center, Himeji, Japan

Accepted for publication November 28, 2000.

Address reprint requests to Dr Higami, Division of Cardiovascular Surgery, Hyogo Brain and Heart Center, 520 Saisho-ko, Himeji 670-0981, Japan
e-mail: thigami{at}kba.att.ne.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. We have developed an ultrasonic complete skeletonization technique for obtaining internal thoracic artery (ITA) grafts and have used this method clinically since January 1998. In this report, we discuss the early results of bilateral ITA grafts obtained with our method.

Methods. We studied 200 consecutive patients who underwent coronary artery bypass grafting using ITAs obtained by this technique. Angiography of the grafts was performed in 188 patients (94%) within 1 month after coronary artery bypass grafting.

Results. The ITA grafts were about 4 cm longer than pedicled ITA grafts. The free flow through the grafts was at least 30% higher than through pedicled ITAs. The early patency rate determined by postoperative angiography of the grafts was 99.7% for left ITAs and 100% for right ITAs. No patient required postoperative intervention or repeated surgery.

Conclusions. Ultrasonic complete skeletonization increases the effective length of ITA bypasses, improves free flow through the bypasses, and it is less invasive than conventional pedicled harvesting. These excellent early results indicate that this technique is a straightforward, safe, less invasive, and optimal method for obtaining ITA bypass grafts.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
The effectiveness of the internal thoracic artery (ITA) for coronary artery bypass grafting (CABG) is well established [1–4]. Skeletonization techniques have been suggested for maximizing the utility of ITA grafts [5], and the benefits of such techniques have increasingly been reported [3, 5–8]. Advantages of ITA skeletonization include an increased effective length of the ITAs and conservation of blood flow around the sternum, leading to a decreased risk of development of mediastinitis. However, skeletonization techniques are not commonly used clinically because they are difficult and time consuming, and because of the risk of damage to the ITA [9]. To overcome these drawbacks, we have developed a new ultrasonic complete skeletonization technique using an ultrasonic scalpel. After histologic and physical confirmation of the safety of this technique in pigs, we began to use this technique clinically in January 1998, and have performed ITA bypasses in more than 250 patients undergoing CABG in the last 2 years. In this report, we present the analysis of our early results in these cases and evaluate the usefulness of bilateral ITA skeletonization using the ultrasonic complete skeletonization technique.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Evaluation was performed for 200 consecutive patients who underwent CABG since January 1998 and from whom ITAs were obtained using the ultrasonic complete skeletonization technique. Patients who underwent CABG and another surgery simultaneously, those undergoing emergent operation within 24 hours after the onset of acute myocardial infarction, and those who underwent off-pump CABG were excluded from analysis. All 200 patients evaluated were Japanese. The patients were aged 63.8 ± 10.9 years, and 143 of the 200 patients (72%) were over 60 years old. Unstable angina, which was consistent with The Society of Thoracic Surgeons (STS) definition, was noted in 50 patients. There were 54 patients (27%) who underwent urgent CABG within 24 hours of presentation. The mean number of diseased vessels was 2.5, and 77 patients (39%) had significant (>= 75%) stenosis in the left main coronary artery. The incidence of left main disease was relatively high in our series. This may be due to the fact that in many cases, patients had undergone percutaneous transluminal coronary angioplasty at our institute even in triple-vessel disease, except for the left main coronary artery. Eighty-six patients (43%) had diabetes mellitus, and 24 had severe diabetes requiring insulin injections (Table 1).


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  		Table 1. Preoperative Data

 


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  		Fig 1. Angiographic control after 13 months. Both internal thoracic arteries are patent and smooth without stenoses. (A) Right internal thoracic artery is grafted to the second obtuse marginal branch and the posterior lateral branch. (B) Left internal thoracic artery is grafted to the first diagonal branch and the left anterior descending artery.

 
Operative procedures
A median sternotomy was performed. After dissecting the reflection of the mediastinal pleura from the endothoracic fascia, the ITA and both satellite veins were visualized. The endothoracic fascia was longitudinally incised just medial to one of the satellite veins using an ultrasonic scalpel (Harmonic Scalpel, dissecting hook type; Ethicon Endo-Surgery, Cincinnati, OH). The space between the medial satellite vein and the ITA was carefully dissected using the ultrasonic scalpel (output level: 2). Only the ITA was targeted for dissection. The fatty tissue around the ITA was foamed and easily removed by lightly sweeping it away, moving the ultrasonic scalpel along the length of the vessel to expose the adventitia of the ITA. Importantly, the contact time of the ultrasonic scalpel was set at 0.1 to 0.2 seconds and the scalpel was moved lightly and quickly along several centimeters of the vessel as main trunk ("quick touch" method). In this way, the main trunk was skeletonized safely and quickly. In contrast, treatment of the branches is a slower process. After exposing a branch, the tip (blunt side) of the blade was placed on the branch at least 1 mm from the trunk (output level: 2) [10]. The branch was sealed by ultrasonic protein coagulation within 3 to 4 seconds with averaged-force compression, and then spontaneously divided with complete hemostasis, without injuring the main trunk ("close coagulation"). In almost all patients, no clip was needed for ITA branch closure. Branches should never be separated by pulling the hook inside the tip of the blade; if they are, the target vessel will often be cut before sufficient protein coagulation has been completed. Venous branches rarely cross lateral to medial anterior to the ITA, and when they do, it usually is in the vicinity of the third or fourth interspace. These veins were doubly clipped and cut or ablated by Harmonic coagulation. The ITA was then separated from the fascia, with completion of skeletonization [11].

The ITA was harvested from the bifurcation of the musculophrenic and superior epigastric arteries up to the upper margin of the first rib or higher, which is just distal to the phrenic nerve in the hemithorax. After systemic heparinization, the distal end of the ITA was cut, and 3 mL of dilute papaverine (10 mg in 10 mL saline) was injected from the stump into the ITA. An aortic cannula and two venous cannulae were introduced in preparation for cardiopulmonary bypass before free flow of the ITA was measured. Cardiopulmonary bypass was initiated, the aorta was cross-clamped, and myocardial protection was performed with retrograde continuous administration of cold-blood cardioplegia. When the left ITA (LITA) was anastomosed to the circumflex artery or its branches, the pleuropericardial space was dissected, taking care not to damage the phrenic nerve. This maneuver makes the course of the artery toward the obtuse marginal or the posterolateral branches of the circumflex artery shorter. When the right ITA (RITA) was anastomosed to the circumflex artery, the RITA was passed through the transverse sinus. It is important to confirm free flow through the RITA by releasing the ITA clamp after this procedure. By confirming free flow through the RITA, torsion, if any, on the RITA is completely eliminated.

The ITA was anastomosed with continuous 8-0 monofilament sutures. Special attention was paid not to clip the intima of the ITA, to stitch from the inside to the outside of the graft at the heal part of the anastomosis, and to stitch from the inside to the outside of the native artery at the toe part of the anastomosis. Sequential side-to-side anastomoses were prepared in parallel using 8-0 monofilament sutures in which stitches were made in a continuous manner, similar to those used in end-to-side anastomoses. Because the skeletonized ITAs are light and slim, the grafts could be effectively and completely fixed to the sites of anastomosis by spraying with a fibrin glue (Bolheal; Chemo-Sero-Therapeutic Research, Kumamoto, Japan). This technique was especially useful in sequential bypass grafts, allowing difficult graft routes, such as the s-shape, to be made smooth, and avoiding graft kinking. Nitroglycerine was used during and after the operation in order to avoid spasm of the coronary arteries and arterial grafts and postoperative hypoperfusion syndrome.

Evaluation of early and midterm results
Angiography of the grafts was performed in 188 patients who gave informed consent (94% of the patients enrolled) within 1 month after CABG to evaluate the patency of the ITA and presence or absence of acute changes such as hyperplasia or stenosis of the skeletonized ITA. We followed 199 patients (99.5%) by telephone or office visits for 6 to 30 months (mean 13.9 months) after surgery. Reevaluation of the grafts by means of angiography was performed 1 year after CABG for 20 patients who gave informed consent to undergo reexamination.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
The mean effective length of ITA grafts obtained with this technique from patients 159.8 ± 12.7 cm in mean height and 1.61 ± 0.67 m2 in mean body surface area was 20.7 ± 1.4 cm for the LITA and 20.8 ± 1.6 cm for the RITA. The internal diameter of the distal end of harvested ITAs was 1.87 ± 0.29 mm in LITAs and 1.91 ± 0.25 mm in RITAs. The free flow was 122.2 ± 44.8 mL/min in LITAs and 137.6 ± 51.7 mL/min in RITAs, which was more than adequate for these conduits. Almost none of the ITA grafts required clipping for closure of their branches, and no branches exhibited bleeding after harvesting of grafts. The time required to harvest ITA grafts was 21.9 ± 8.7 minutes.

The average number of grafts used per patient was 2.6, and the average number of arterial grafts was 1.9. Bilateral ITAs were used in 119 patients (60%). Sequential bypass of ITAs was performed in 101 patients for 103 vessels (Table 2). A total of 185 LITAs were anastomosed to 279 vessels, including 94 sequential anastomoses, and 121 RITAs were anastomosed to 130 vessels. Regarding vessels bypassed, 136 LITAs (74%) were anastomosed to 203 left anterior descending (LAD) arteries or their branches, and 48 LITAs (26%) were anastomosed to 75 circumflex (Cx) branches. Fifty-nine RITAs (49%) were anastomosed to 62 LADs or their branches, 52 RITAs (43%) to 57 Cx branches, and 10 RITAs to 11 right coronary artery (RCA) branches (Table 3). Perioperative myocardial infarction was noted in 2 patients (1.0%). One patient exhibited changes in the electrocardiogram (ECG) pattern suggestive of postoperative coronary artery spasm, and had a right ventricular infarction in a territory where there was no coronary stenosis and no grafts were placed. This patient required intraaortic balloon pumping, but improved thereafter. Another patient suffered a mild inferior infarction, where no graft had been placed, associated with slight changes in hemodynamics, and had only slight changes in the ECG. No patient experienced postoperative hemorrhage from the grafts or developed mediastinitis. Noncardiac hospital death occurred in 1 patient with intestinal necrosis, due most likely to an intraaortic balloon pump inserted preoperatively. (Table 3).


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  		Table 2. Operative Data and Results

 

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  		Table 3. Distal Anastomoses

 
Coronary angiography was performed within 1 month after CABG in 188 patients (94%). These patients exhibited favorable early patency rates of 99.7% for the LITA and 100% for the RITA (Table 4). Occlusion of the LITA was noted in a patient who underwent a sequential anastomosis to the diagonal branch (internal diameter, 1 mm) and the LAD. In this patient, the diagonal branch was not visualized due to poor run-off at the site of anastomosis, but the LAD, another vessel anastomosed to the distal portion of the LITA, was clearly visualized, demonstrating that the LITA was intact. In addition, three LITAs and two RITAs exhibited slight stenosis of the peripheral anastomoses, but each of the affected regions had favorable run-off. The remaining ITAs were free of stenosis, and angiography demonstrated completely smooth inner walls in the entire lengths of the ITAs. The mean follow-up duration was 14.8 ± 6.1 months. Late death occurred in 4 patients, all of whom died of nonischemic causes including pneumonia, stroke, sepsis, and sudden death. One patient, who had poor left ventricular function preoperatively, was medically treated for congestive heart failure after transient arterial fibrillation. One patient had implantable cardioverter defribillator implantation for medically refractory multiple premature ventricular contractions. No patient, however, developed recurrent angina pectoris or underwent post-CABG intervention or surgery. Reevaluation of the grafts was performed in 34 ITAs of 20 patients 1 year after CABG. All ITAs were patent and had smooth walls without stenosis, and 29 ITAs (85%) showed an increased or unchanged in graft diameter compared with that immediately after CABG (Fig 1).


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  		Table 4. Postoperative Angiographic Data (Early, < 30 Days)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Skeletonization of ITAs has significant advantages including prolongation of the effective length and ability to use bilateral ITAs. However, skeletonization is not widely used, mainly because it is more traumatic to the arterial wall than conventional pedicled preparations, requires advanced techniques, and is time consuming. To overcome these drawbacks, in 1998, we developed an ultrasonic complete skeletonization technique [11]. With an ultrasonic scalpel, intact ITAs can be readily obtained in a relatively short period of time, with minimal invasion compared with conventional cautery knives.

The validity of ITA skeletonization has been reported by several researchers, although they used bipolar electrocautery [7, 8, 12]. Thinner-walled arteries can be nourished entirely by luminal diffusion, which can reach 300 to 350 µm into the superficial portion of the arterial wall [13–15]. The thickest part of the ITA media was approximately 150 µm [7], which could be reached by luminal diffusion with avoidance of ischemia despite total disruption of the vasa vasorum. These findings suggest that complete skeletonization can maintain the integrity of ITA if it is harvested without damage.

Frequently reported clinical advantages of skeletonization of the ITA include an increased effective length of the ITA [5] and an increase in vessel diameter leading to improved free flow through the ITA [16]. The increase in usable length overcomes one of the main limitations of thick pedicled ITA use, ie, difficulty in reaching distal target sites, and facilitates the performance of total arterial revascularization and complex ITA grafting. With our technique, the LITA and RITA measured before papaverine injection were an average of 4.1 and 3.9 cm longer than conventional LITA and RITA grafts, respectively. Free flow through skeletonized ITAs, measured after papaverine injection, was at least 30% higher than through thick pedicled ITAs. These results demonstrate not only the efficacy of skeletonization but the minimal invasiveness of use of the ultrasonic scalpel, and indicate that spasm associated with ITA harvesting is less common than with conventional harvesting methods, despite the radical techniques used for complete skeletonization.

The second advantage of this technique is a decreased incidence of sternal wound infection. The incidence of sternal wound infections was found to be higher in patients with bilateral ITA grafts than in patients who received only saphenous vein grafts or a single ITA graft [17]. However, Gulbut and associates [18], who harvested both ITAs in a skeletonized fashion using bipolar electrocautery, reported (for more than 1,000 patients) an incidence of sternal wound infections of only 1.5%. Their patient population included 20.4% diabetic patients. Although 43% of our patients had diabetes mellitus and 60% required bilateral ITA grafts, none of our patients developed a sternal wound infection. These favorable results may be related to the fact that collateral circulation to the sternum can be partially preserved if the conduit is harvested as a skeletonized conduit [19, 20], and to the less invasive nature of the Harmonic Scalpel.

The third and most significant advantage of this technique is the increased availability of bilateral ITAs, and especially the increased coverage obtained with the RITA. Completely skeletonized RITAs can be anastomosed to almost the entire LAD, the obtuse marginal artery of the Cx, the posterior descending artery of the RCA, and some other sites. Although one report found inferior patency of RITAs when anastomosed to Cx branches [21], we obtained favorable results for this anastomosis, as demonstrated by the absence on postoperative angiography of occlusion or stenosis in RITAs passed through the transverse sinus to be anastomosed to Cx branches. These results may be related to the following factors: (1) the conduit is slim enough to escape compression in the transverse sinus; (2) torsion or kinking of grafts is rare, because the torsion associated with harvesting procedures is spontaneously released during confirmation of free flow through the bypass, a necessary step after passage of the bypass through the transverse sinus; (3) because postoperative bleeding from branches does not occur with this procedure, there is no risk of bypass occlusion associated with hematoma due to postoperative hemorrhage: and (4) the conduit is long enough to avoid excessive tension on the graft.

In summary, handling of the skeletonized ITA is relatively easy by comparison with conventional pedicled ITAs. Furthermore, the ultrasonically skeletonized ITAs are similar to ITAs skeletonized via cautery techniques in terms of available length, distribution to the different myocardial areas, and clinical results including spasm and myocardial infarction. However, we believe that the ultrasonic skeletonization technique is superior with regard to time required for harvesting, reduced sternal infections, and improved patency results.

In conclusion, the ultrasonic complete skeletonization technique is a simple, safe, and minimally invasive ITA harvesting method. We obtained highly satisfying early and midterm results in 200 consecutive patients undergoing CABG. We believe that this technique will significantly increase safety and suppliable area in bilateral ITA grafting; it should help to and will make CABG using bilateral ITA grafts a standard procedure.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  6. Calafiore A.M., Vitolla G., Iaco A.L., 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]
  7. Sasajima T., Wu M.H., Shi Q., Hayashida N., Sauvage L.R. Effect of skeletonizing dissection on the internal thoracic artery. Ann Thorac Surg 1998;65:1009-1013.[Abstract/Free Full Text]
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