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Ann Thorac Surg 2002;73:1880-1887
© 2002 The Society of Thoracic Surgeons

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Original article: cardiovascular

Skeletonized radial artery grafting: improved angiographic results

^a Department of Cardiovascular Surgery, Showa University Northern Yokohama Hospital, Kanagawa, Japan
^b Department of Cardiovascular Surgery, Kobari General Hospital, Chiba, Japan
^c Department of Cardiovascular Surgery, Shin-Tokyo Hospital, Chiba, Japan

Accepted for publication February 5, 2002.

* Address reprint requests to Dr Hirose, Department of Cardiovascular Surgery, Kobari General Hospital 29-1 Yokouchi, Noda City, Chiba 278-8501, Japan
e-mail: genex{at}nifty.com

	Abstract

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Background. The radial artery has been used for coronary artery bypass grafting (CABG) but its early angiographic results were relatively inferior to that of the internal mammary artery, most likely due to spasm of the graft. To avoid vasospasm we harvested the radial artery using a skeletonized technique and spasm was completely reversed before use. The graft patency of the skeletonized radial artery was compared with the radial artery graft harvested as a pedicle.

Methods. A total of 112 patients underwent isolated CABG using a pedicled radial artery between September 1, 1999, and August 31, 2000 (group P), and a total of 131 patients with a skeletonized radial artery between September 1, 2000, and August 31, 2001 (group S). An ultrasonic scalpel (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH) was used for skeletonization and removing satellite veins and surrounding tissue. CABG was performed by the standard technique. Perioperative results were prospectively collected and compared between the two groups. Early angiographic results performed within 3 months were also compared.

Results. There were two hospital deaths in group S. Major complications were observed in 11 (8.4%) in group S and 3 (2.7%) in group P (p = not significant [NS]). None were related to the radial artery graft. Angiography was obtained in 96 patients of group S and 76 patients in group P and revealed that the stenosis free graft patency rate of group S (138 of 143, 96.5%) was superior to that of group P (73 of 86, 84.9%) with p < 0.005.

Conclusions. Skeletonization of the radial artery with the ultrasonic scalpel is safe and contributes to reducing the incidence of early graft stenosis.

	Introduction

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Coronary artery bypass grafting (CABG) using arterial grafts is receiving increased attention since the long-term patency rate of arterial grafts is reported to be superior to saphenous vein grafts [1]. The internal mammary arteries (IMAs) are the most frequently used arterial conduits and their patency rates are reported to be 90% or better even 10 years after surgery [1, 2]. Studies have shown that bilateral internal mammary artery grafting could provide better event-free rates than single IMA grafting in selected patients [1, 3]. The graft patency of the right internal mammary artery (RIMA) is reported to be similar to that of the left internal mammary artery (LIMA) [2]. These RIMA and LIMA are considered to be the first and second choices of arterial conduit in most CABG cases: the third choice remains controversial. Previously, we published our data of radial artery bypass grafting [4]. The 3-year patency rate of radial artery bypass in that series was 81.3% but graft stenosis or string signs were observed in 12.2% at early angiography and 12.6% at late. Some of this graft stenosis was considered to be related to graft spasm. Severe graft spasm may result in hypoperfusion syndrome. To prevent early graft spasm a modification of the harvesting technique of the radial artery was considered.

The skeletonized harvesting technique was first adopted for IMA grafting [5]. Skeletonization of the IMA increased the length of the graft and increased the free flow and its caliber size compared with the pedicled graft [6]. Early angiographic results of skeletonized IMA grafting were favorable and graft spasm was not induced by skeletonization itself [7, 8]. Considering the favorable facts of skeletonized IMA grafting we began to harvest the radial artery using the skeletonized technique in September 2000. We report here our 1-year clinical experience of skeletonized radial artery grafting, which was compared with pedicled radial artery grafting.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Patients
Between September 1, 1999, and August 31, 2001, a total of 243 consecutive patients underwent isolated CABG using the radial artery at Shin-Tokyo Hospital Cardiovascular Group (Shin-Tokyo Hospital, Kobari General Hospital and Yokohama City Northern Hospital). In the early half of the study period the radial artery was harvested routinely as a pedicle graft and in the late half as a skeletonized graft. Between September 1, 1999, and August 31, 2000, 112 patients underwent CABG using apedicle radial artery (group P) and between September 1, 2000, and August 31, 2001, 131 patients using a skeletonized radial artery (group S).

Technique of radial artery harvesting
Radial artery harvest was avoided in patients with renal dysfunction or patients with a positive Allen test. The radial artery was harvested from the nondominant hand in most cases.

The pedicle radial artery harvest was performed in the usual manner described previously [4]. Briefly, a skin incision was made from the wrist to the midantecubital fossa. The brachioradialis muscle was retracted laterally along its entire length. The radial artery was immobilized with the satellite veins, covering fascia, and the surrounding adipose tissue. The branches of the radial artery were clipped and divided at just distal to the satellite veins. Electrocautery to the radial artery or its branches was avoided. After transection of the distal end of the radial artery, it was cannulated and diluted milrinone was slowly injected. The proximal end was then transected at the level of the bifurcation. The harvested pedicle was preserved in warm papaverine solution.

Skeletonization of the radial artery was performed using an ultrasonic scalpel (Harmonic Scalpel, dissecting-hook type; Ethicon Endo-Surgery, Cincinnati, OH). The fascia covering the radial artery and satellite veins was dissected longitudinally using a metzenbaum. The space between the satellite vein and the radial artery was carefully dissected using the ultrasonic scalpel. The removal of excessive tissue around the radial artery was facilitated by the cavitations ability of the ultrasonic scalpel, using it to sweep over the radial artery. This was carried out quickly and the contact time of the ultrasonic scalpel and the radial artery was about 0.2 second to avoid damage to the vessel ("quick touch" method). In this way the main trunk of the radial artery was quickly skeletonized. The branches of the radial artery were also controlled 1 mm distal to main trunk, inside of the satellite veins, with the ultrasonic scalpel, applying the blunt side of the blade perpendicular to the branches at a distance of at least 1.0 mm from the main trunk. In 3 seconds the branch divided spontaneously with a protein coagulum. The hook inside the blade was not used to control a branch, otherwise the branch is often cut before the protein coagulum was made, which might result in incomplete hemostasis. After all the branches were controlled diluted papaverine was sprayed onto the graft to reverse vasospasm. Further dissection of the adventitia was continued using micro-scissors (Fig 1). The vasospasm was further reversed by injecting diluted milrinone intraluminally through the distal end of the graft. Mild gentle pressure was applied during intraluminal injection. After the complete reverse of vasospasm, the proximal end of the graft was transected. The harvested radial artery was preserved in warm papaverine solution until use.

View larger version (152K): [in this window] [in a new window]   Fig 1. The radial artery harvested with the skeletonized technique.

The target of the LIMA was primarily the left anterior descending artery. If the RIMA was used for the bypass to the left anterior descending artery, the LIMA was anastomosed to the diagonal or the circumflex artery. The gastroepiploic artery was used for revascularization of the distal right coronary artery. Thus most of the radial artery was used for revascularization of the branches of the circumflex artery or main trunk of the right coronary artery. When arteriosclerosis of the aorta was expected, the radial artery was used as a composite Y-graft usually made with the LIMA. The proximal diameter of the radial artery was measured just before the proximal anastomosis.

For the prophylaxis of perioperative vasospasm calcium-channel blockers such as nicorandil or diltiazem were administered systemically. An intravenous infusion of diltiazem (1 ug · kg^-1 · min^-1) or nicorandil (0.5 ug · kg^-1 · min^-1) was started after the induction of general anesthesia and continued until the second postoperative day. Oral diltiazem 180 mg/d or nicorandil 15 mg/d was then given for at least 1 year. Anticoagulation was started on postoperative day 2 with aspirin 81 mg/d and dipyridamole 75 mg/d.

Data collection
This study was conducted prospective manner. The institutional ethics committee approved the skeletonized radial grafting. The patients signed an informed consent before surgery. The following data were collected: patient’s age, gender, cardiac profiles, preoperative risk factors, graft material, surgical data, postoperative complications, and mortality. Outpatient follow-up was completed by the referring cardiologists or hospital outpatient clinic. Cardiac events after discharge from hospital were reported. Myocardial infarction, angina, arrhythmia requiring hospitalization, congestive heart failure requiring hospitalization, coronary reintervention (percutaneous transluminal coronary angioplasty [PTCA] with or without stent placement or redo-CABG), and sudden death were counted as cardiac events. These follow-up data were compiled by October 31, 2001. The end points were patient death or the occurrence of one of these cardiac events.

Angiographic control
Postoperative angiographic control was obtained if the patients agreed to the procedure. Most patients underwent postoperative angiography before discharge from hospital but some patients underwent outpatient angiography within 3 months after surgery as per patient request. The quality of the anastomosis was graded according to Fitzgibbon’s classification [10]. Briefly, grade A stands for excellent graft patency, grade B for graft stenosis more than 50%, and grade O for occlusion. String sign, which was defined as a severe and extensive narrowing of the whole body of the graft [11], was classified into grade B anastomosis.

Statistical analysis
Results were expressed as mean ± standard deviation. Statistical analysis was performed using Student’s t test for continuous variables or ² tests (Fisher’s exact tests if n < 5) for categorical variables. A p value less than 0.05 was considered significant. Postoperative patient survival and event-free rates were calculated using the Kaplan-Meier method and compared with log-rank tests. All statistical analyses were performed using Statview version 5.0 (SAS Institute, Cary, NC).

	Results

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Patient demographics
Group S consisted of 131 patients (102 males and 29 females with a mean age of 65.9 ± 8.9 years), and group P of 112 patients (80 men and 32 women with a mean age of 65.8 ± 8.9 years). The preoperative data are described in Table 1. The two groups were not significantly different in terms of cardiac profile, angiographic profile, coronary risk factors, or preoperative comorbidities.

	Comment

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Parolari and coworkers [14] published a review of radial artery grafting and demonstrated that the early radial graft patency rate was 98.1% (627 of 639) and that the perfect patency rate was 90.8% (474 of 522), reflecting the graft occlusion found in 2.9% and graft stenosis in 7.3%. Other reports also pointed out certain and considerable radial artery stenosis occurring in the early phase after surgery: 5.4% by Acar and colleagues [17], and 6.5% by Weinschelbaum and colleagues [18]. Radial artery graft spasm affecting early graft stenosis was emphasized.

The skeletonization technique was introduced into our institute for IMA harvesting in early 2000. Skeletonization requires immobilization of the arterial trunk from the satellite veins and surrounding tissue. We were initially hesitant to adopt the skeletonization technique due to concerns about graft injury and vasospasm. However, the application of an ultrasonic scalpel made the skeletonized graft harvest easier and safer. Dissection of the tissue planes and hemostasis of the branches were adequately achieved by ultrasonic scalpel with minimum vasoconstriction.

The ultrasonic scalpel converts ultrasonic energy to denature tissue protein into a sticky coagulum that seals blood vessels and bleeding tissue with less heat production than electrocautery [7, 19]. Higami and coworkers [7] reported that protein coagulum sealed the branch of the IMA without damaging the main trunk when the blade was applied to the side branch at least 1 mm from the main trunk. Proper application of the ultrasonic scalpel does not injure the main trunk and achieves complete hemostasis.

From the study of IMAs, skeletonization using ultrasonic scalpel was found not to damage the endothelial function of the IMA. Choi and Lee [8] reported that the skeletonized IMA can deliver a higher blood flow than the pedicle IMA. The response to the intraluminally injected vasodilators was reported to be greater in the skeletonized graft than the pedicle graft [6]. Higher blood flow through the bypass conduit is probably beneficial for early postoperative coronary perfusion and it may decrease the risk of hypoperfusion syndrome [15].

Considering the facts of skeletonized IMA grafting we started to harvest the radial artery using an ultrasonic scalpel. Unlike electrocautery, graft spasm seldom occurs by skeletonization using the ultrasonic scalpel. Dissection between the radial artery and its satellite veins is well performed using fragmentation mechanism. Tight adhesions, which are occasionally observed at the catheterization site, also can be dissected without injuring the main trunk of the radial artery. Even with extensive dissection along the radial artery, graft spasm was not a major problem when the ultrasonic scalpel was used for dissection. Application of topical spray of papaverine and intraluminal injection of milrinone reverses vasospasm in the radial artery. Although skeletonized harvesting takes a longer than pedicle harvesting, it had no influence on the total operative time. We do not use electrocautery for skeletonization of the radial artery, because the electrocautery causes heat injury which may result in graft spasm. It would be interesting to see histologic or functional studies using animal models to support the hypothesis that skeletonization with the ultrasonic scalpel is associated with lower trauma to the radial artery than with the electrocautery.

Radial artery graft spasm rarely occurs under our skeletonization protocol. No postoperative myocardial infarction occurred in the territory of the radial graft. The angiographic study successfully demonstrated the reduction of string sign in the radial artery by use of our skeletonization technique. We hypothesized that these angiographical improvements were attributed to the complete reverse of vasoconstriction by removing all surrounding tissue. The role of the adventitia should be further analyzed in relation to the vasospasm. The angiographic follow-up of our series was extremely limited. It is of great concern how the skeletonized radial artery graft patency will progress in the remote follow-up. Furthermore, randomized study using the pedicle graft versus skeletonized graft is necessary to confirm our initial data.

Hemostasis of the ultrasonic scalpel was adequate. No patients developed postoperative bleeding from the skeletonized conduits. Care should be taken in selecting the angle of the blade when applying to the branch of the artery. Inadequate angle of the blade may cause immature hemostasis. In addition venous bleeding may not be stopped with ultrasonic scalpel, as the venous wall has too small an amount of protein to create coagulum [7].

Extensively reversed vasospasm and a larger caliber of the graft makes the anastomosis easier. Sequential grafting is carried out more easily in the skeletonized graft than the pedicle graft because the skeletonized graft has no adventitia and a good length. The pedicled radial artery anastomosed to the mildly stenosed coronary artery often showed a narrowing in early angiography, because of flow competition between the graft and the native coronary artery [4]. Thus a mildly stenosed coronary artery used to be bypassed with the saphenous vein, accepting the risk of vein graft disease. However, in this situation now we can use the skeletonized radial artery as a valveless, large-caliber conduit that can deliver high flow. In our study bypass to the mildly stenosed coronary artery was performed in 13 patients (11.6%) in group P and 30 patients (22.9%) in group S (p < 0.05). Among the 13 radial grafts to the mildly stenosed coronary artery, 1 developed string sign by the early angiography; however, no string signs were observed in the skeletonized group. To optimize the high blood flow through the radial artery graft, proximal anastomosis of the radial artery graft should be the ascending aorta rather than creating a composite graft with the LIMA.

The harvested skeletonized radial graft appeared to be longer than the pedicle graft. In our study the length of the radial artery was not compared between the two groups because the length of the skin incision was modified according to the condition of the radial artery. Skin incision can be shortened in the skeletonized group compared with the pedicle group. Furthermore the distal part of the radial artery has often been injured by previous coronary angiography or arterial blood pressure monitoring. The skeletonized and lengthened radial artery allows us to discard the distal portion of the radial artery. Calcification or focal arteriosclerosis was reported to be present in about 5% of radial arteries [15]. Because focal arteriosclerosis in the graft may influence graft patency, the graft should be examined carefully. The skeletonized radial artery graft is easily accessed whether or not arteriosclerosis is present. Any affected portion of the radial artery should not be used.

While we harvested the radial artery as a pedicle, the length of the graft was sometimes shorter than we had expected. In that case a composite graft was made with the LIMA to lengthen the radial artery. Flow competition between the radial artery and the LIMA was a great concern [4]. Because the skeletonized technique allows us to harvest the radial artery with sufficient length for aortocoronary bypass, frequency of the composite grafting has been reduced. The application of composite grafts using the skeletonized radial artery is limited to high-risk patients for aortocoronary bypass, such as patients with severe arteriosclerosis including aortic calcification. Another factor influencing decreased frequency of the composite graft is the availability of the bilateral IMAs. During the period of radial skeletonization all the IMAs were harvested with skeletonized fashion. Skeletonized harvesting of the IMA is reported to maintain venous return from the sternum and to reduce the incidence of sternal wound problems even with bilateral IMA harvesting [20, 21]. Bilateral IMA harvesting was increased from 28.6% in the early phase of our study to 52.7% to the late phase but the incidence of mediastinitis was not increased.

Summary
Although skeletonized radial artery harvesting was not previously recommended, the accurate application of an ultrasonic scalpel allowed us to safely harvest the skeletonized radial artery. In the skeletonized radial artery, vasospasm was easily reversed. Skeletonized radial grafting contributes to a wider range of selection of grafting techniques including sequential bypass or bypass to a high-flow and mildly stenosed coronary artery. The initial angiographic findings of the skeletonized radial artery grafts successfully showed reduction of string sign. No skeletonized grafting-related adverse effects were observed. The fate of the skeletonized grafts should be followed up carefully.

	References

Top Abstract Introduction Material and methods Results Comment References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Atsushi Amano Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Amano, A. Articles by Hirose, H. Search for Related Content PubMed PubMed Citation Articles by Amano, A. Articles by Hirose, H.