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Ann Thorac Surg 2004;77:120-125
© 2004 The Society of Thoracic Surgeons


Original article: cardiovascular

Skeletonization versus pedicle preparation of the radial artery with and without the ultrasonic scalpel

Andreas Rukosujew, MDa*, Rudolf Reichelt, PhDb, Alexander M. Fabricius, MDc, Gabriele Drees, MDa, Tonny D. T. Tjan, MDa, Markus Rothenburger, MDa, Andreas Hoffmeier, MDa, Hans H. Scheld, MDa, Christof Schmid, MDa

a Department of Thoracic and Cardiovascular Surgery, University Hospital, and, Muenster, Germany
b Institute of Medical Physics and Biophysics, Westfälische Wilhelms-University, Muenster, Germany
c Division of Cardiac Surgery, Heart Center Leipzig, Leipzig, Germany

Accepted for publication July 29, 2003.

* Address reprint requests to Dr Rukosujew, Department of Thoracic and Cardiovascular Surgery, University Hospital Muenster, Albert-Schweitzer-Str. 33, Muenster D-48129, Germany.
e-mail: andreas.rukosujew{at}thgms.uni-muenster.de


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: The radial artery (RA) is increasingly used for myocardial revascularization because of its presumed advantageous long-term patency rates. The vessel can be harvested as a pedicle or skeletonized. The aim of this study was to compare the skeletonization technique with pedicle preparation using either an ultrasonic scalpel or scissors.

METHODS: Forty consecutive patients with coronary artery disease undergoing complete arterial revascularization were included in the study. In 20 patients the RAs were prepared using scissors and clips (group 1: skeletonization; group 2: pedicle). In another 20 patients the arteries harvested were prepared using an ultrasonic scalpel (group 3: skeletonization; group 4: pedicle). The RA was treated with papaverine to prevent spasm of the vessel during and after harvesting. Tissue specimens of each RA were taken to analyze endothelial morphology by scanning electron microscopy. After implantation of the RA, graft perfusion was measured with a flow probe.

RESULTS: Harvesting the RA as a skeletonized vessel took more time as compared with pedicle preparation (group 1 vs group 2: 37.1 ± 3.5 minutes vs 24.4 ± 3.9 minutes; p < 0.001 and group 3 vs group 4: 31.1 ± 3.5 minutes vs 25.6 ± 3.7 minutes; p < 0.01). The number of hemostatic titanium clips was similarly higher in group 1 as opposed to group 2 (58.7 ± 7.1 vs 38.7 ± 7.1; p < 0.01). However, there was no difference between groups 3 and 4 (p = 0.086). The length of the RA after skeletonization with scissors and clips was 20.8 ± 1.5 cm in contrast with 19.1 ± 0.9 cm (p < 0.01) after dissection as a pedicle. In the groups using the ultrasonic scalpel, there was no difference in graft length (p = 0.062). Mean blood flow through the graft after establishing the proximal anastomosis was similar among all groups (groups 1, 2, 3, and 4: 50 ± 20.1 mL/min, 53.8 ± 24.3 mL/min, 56.3 ± 25.1 mL/min, and 51.8 ± 23 mL/min, respectively). Scanning electron microscopy demonstrated endothelial damage in all patients in groups 1, 2, and 3 and in 7 patients of group 4. Most endothelial lesions were minor except in group 3 in which 1 of 5 endothelial lesions were severe. Statistically significant differences was found between groups 1 and 2, and 3 and 4 with respect to the degree of endothelial damage (p < 0.01).

CONCLUSIONS: Skeletonization using scissors and clips is more time consuming and technically more difficult, but yield significantly longer grafts. Skeletonization with an ultrasonic scalpel did not result in additional length and was more frequently associated with severe endothelial damage. Pedicle preparation using scissors or an ultrasonic scalpel is much simpler and faster, and does not jeopardize endothelial integrity.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The radial artery (RA) was introduced as a coronary bypass graft more than 30 years ago [1]. The advantages of the RA include its adaptation to systemic blood pressure and its larger diameter as compared with all other arterial bypass grafts [2, 3]. The main obstacle for the utilization of the RA are its vasospastic properties, which are important since the diameter of the RA is usually far lower than that of a saphenous vein, and a reduction of the vessel diameter due to spasm may significantly reduce the blood flow [4]. One of the techniques to avoid spasm of the RA is to harvest the vessel together with its accompanying veins in a pedicle [2, 58]. Skeletonization of the RA is less frequently used [911]. In the latter cases, many colleagues favor preparation of the RA with an ultrasonic scalpel, which was introduced into clinical practice in 1987 [12]. This presumably allows a nontraumatizing preparation of the RA, it is easy to handle, and does not require much time [1317].

The aim of the study was to compare the skeletonization technique with pedicle preparation of the RA using an ultrasonic scalpel or scissors.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Study groups
Forty patients with coronary artery disease scheduled for complete arterial revascularization were divided into 4 groups including 10 patients each. In group 1, the RA was harvested in a skeletonized fashion with the use of scissors and titanium clips, and in group 2 as a pedicled graft, also with the aid of scissors and clips. Skeletonization of the RA in group 3 and harvesting as a pedicled graft in group 4 were performed using an ultrasonic scalpel (Ethicon, Hamburg, Germany). All RA vessels were taken by the same surgeon (AR) after an Allen test had been performed to assess the integrity of the palmar arch of the nondominant hand. Delayed capillary refilling exceeding 10 seconds was considered a contraindication for an RA harvest.

The following factors were assessed during and after RA preparation: time interval needed for graft preparation, length of the graft, amount of titanium clips used, mean blood flow after completion of the anastomosis, and scanning electron microscopy of the endothelium.

RA harvesting technique
The skin incision and the preparation of the RA strongly considered the topographical anatomy to avoid injury to the cutaneous nerve [18]. Subcutis and fascia antebrachia in the upper and middle third of the forearm were divided by electrocautery, and in the lower third with scissors because the RA lies right below the fascia.

Scissors and clips preparation.
The RA was covered with gauze swabs soaked with diluted papaverine (50 mg papaverine diluted in 100 mL 0.9% NaCl) for topical treatment. The distal end was separated; the proximal end was cannulated and perfused with a papaverine solution. The skeletonization was performed with a "no touch" technique. All side branches were clipped with titanium clips. The vessel was prepared, beginning from the bifurcation of the brachial artery. The recurrent radial artery was divided if the offspring was rather distal. For harvesting a pedicle, the RA with adjacent veins and covering fascia was mobilized beginning from the middle of the vessel. After the RA pedicle was removed, the vessel was flushed with a papaverine solution from its the proximal end.

Ultrasonic scalpel preparation.
An ultrasonic scalpel equipped with a 5 mm hooked tip was used to carefully remove the satellite veins from the RA (ie, for skeletonization of the graft). Side branches were occluded applying the blunted side of the hook perpendicular to the branches and were divided afterward with the sharp edge side. Only very large side branches were clipped with titanium clips. Topical and intraluminal treatment with a papaverine solution was used to prevent vasospasm in an identical manner as previously described. During pedicle preparation, the RA (with its satellite veins) was similarly prepared beginning from the middle of the vessel. Side branches of the RA were occluded as previously described.

After harvesting, the graft was stored in a blood papaverine solution in all groups.

Scanning electron microscopy
In all groups, a specimen of approximately 5 mm in length was taken from the distal end of the vessel for scanning electron microscopy. The RA specimens were immediately fixed with 3% glutaraldehyde. For analysis, the specimens were washed three times with Sörensen-phosphate buffer for 20 minutes. The vessels were sliced with a sharp scalpel under a sectioning angle of approximately 45 degrees ("sausage cut"). Then the water was removed by a graded water-ethanol series (30%, 50%, 70%, 90%, 96%, and absolute ethanol), and the dehydrated samples were critical-point-dried with liquid CO2 according to the standard procedure. Subsequently the critical-point-dried samples were mounted on aluminum specimen stubs with a small amount of electrically conductive carbon (PLANO, Wetzlar, Germany) controlled by a light optical magnifying glass and sputter coated with gold using argon gas as the ionizing plasma. The average thickness of the gold film applied to the samples was approximately 15 nm.

Imaging was performed on a scanning electron microscope (S-450 [Hitachi Ltd, Tokyo, Japan]) with secondary electrons at 20 keV at room temperature. The primary magnifications were in the range of 50x to 2,000x. Micrographs were recorded from a high-resolution cathode ray tube using negative film (Agfapan, APX100; Agfa-Gevaert AG, Lever Kusen, Germany).

Histologic study
A pathologist who was blinded to the procedure studied the samples in order to determine possible damages of the endothelium on the basis of criteria, which were previously described by Gundry and coworkers [19]. The criteria included endothelial cell separation or alteration, endothelial cell loss, basement membrane exposure, intima or media edema, and intima fractures, as well as a classification of the severity of the endothelial damage into "occasionally observed" and "severe." Each criterion was expressed as follows: 0 = no change, 1 = occasionally observed, and 2 = severe.

Measurement of the free blood flow
The intraoperative measurement of the free blood flow was performed after completion of all anastomoses (ie, connection of the RA to the distal end of the right internal mammary artery) and weaning from extracorporeal circulation. In the pedicled group (group 2), the RA was freed from the surrounding tissue and veins. The bidirectional perivascular HQ2 MB and HQ3 MB 2.5 to 3 mm Doppler probes were used in conjunction with the flow meter HT311 (Transonic Systems Inc, Ithaca, NY). Sterile gelly (Aquasonic [Parker Laboratories, Inc, Orange, NJ]) was applied to improve recording. The flow was recorded within 10 seconds and displayed in mL/min under consideration of the mean arterial pressure.

Statistical analysis
Statistical analysis was performed using the SPSS 11.0 (SPSS Inc, Chicago, IL). All appropriate data were assessed for mean and standard deviation. Groups were compared using the Mann-Whitney U test. A p less than 0.05 was considered statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Harvesting the RA as a skeletonized vessel took more time as compared with pedicle preparation (group 1 vs group 2: 37.1 ± 3.5 minutes vs 24.4 ± 3.9 minutes; p < 0.001 and group 3 vs group 4: 31.1 ± 3.5 minutes vs 25.6 ± 3.7 minutes; p < 0.01) (Tables 1, 2). The amount of placed hemostatic titanium clips was similarly higher in group 1 compared with group 2 (58.7 ± 7.1 vs 38.7 ± 7.1; p < 0.01). However there was no difference between groups 3 and 4 (p = 0.086). The length of the RA after skeletonization with scissors and clips was 20.8 ± 1.5 cm, in contrast with 19.1 ± 0.9 cm (p < 0.01) after dissection as a pedicle. In the groups using the ultrasonic scalpel, there was no difference in graft length (p = 0.062). Mean blood flow through the graft after establishing the proximal anastomosis was similar among all groups (groups 1, 2, 3, and 4: 50 ± 20.1 mL/min, 53.8 ± 24.3 mL/min, 56.3 ± 25.1 mL/min, and 51.8 ± 23 mL/min) demonstrated endothelial damage in all patients in groups 1, 2 and 3 and in 7 patients in group 4. The results are listed in Tables 3, 4. Most endothelial lesions were minor except in group 3 in which 1 of 3 endothelial lesions were severe (Figs 1–4) . Combined together there were 30 endothelial lacerations in group 1, 52 in group 2, 48 in group 3, and 18 in group 4 corresponding to a score of 31, 55, 57, and 21, respectively (p < 0.01 for groups 1 and 2; p < 0.01 for groups 3 and 4).


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Table 1. Comparison of Two Different Techniques of Conduit Preparation Using Scissors and Clips

 

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Table 2. Comparison of Two Different Techniques of Conduit Preparation Using Ultrasonic Scalpel

 

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Table 3. Scanning Electron Microscopy Findings and Damage Score Using Scissors and Clipsa

 

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Table 4. Scanning Electron Microscopy Findings and Damage Score Using Ultrasonic Scalpela

 


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Fig 1. Scanning electron microscopy showing severe endothelial cell alteration after radial artery skeletonization with scissors and clips (arrow).

 


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Fig 2. Scanning electron microscopy showing severe endothelial cell loss, endothelial cell separation and alteration after radial artery harvesting as a pedicle with scissors and clips (arrows).

 


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Fig 3. Scanning electron microscopy showing severe endothelial cell loss, exposed basement membrane after radial artery skeletonization with the harmonic scalpel (arrows).

 


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Fig 4. Scanning electron microscopy showing severe endothelial cell alteration, intima edema and media edema after radial artery ultrasonic harvest as a pedicle (arrows).

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The use of the RA as a bypass graft has undergone a renaissance after Acar and colleagues [9] reported on their experience in 1992. Since then, many publications recommend harvesting of the RA as pedicled graft together with its accompanying veins and perivascular tissue. The reasons for promoting this technique are the vasospastic properties of the vessel [6, 16]. Moreover, the pedicle technique is simpler and less time consuming. In contrast, skelotonization is technically demanding, as it requires careful and meticulous dissection of the graft. In our series, skeletonization with scissors and clips mandated an additional 13 minutes for graft harvesting.

Much more interesting than the need of hemostatic clips are the findings during scanning electron microscopy. We found minor (occasional) endothelial damage in all groups. It is our impression that these occasional endothelial lesions are unavoidable, and should be considered as not clinically relevant. In group 2, this endothelial damage was significantly more expressed, which is hard for us to explain, because the RA preparation using scissors and clips should not be traumatic to such an extent. Maybe the number of patients per group was too low and larger groups would have obviated these findings. A much more important prognostic factor is severe damage to the endothelium. These findings were most often seen when skeletonizing the RA with the ultrasonic scalpel. On average, one of five lesions was graded severe. Therefore we believe that skeletonizing the RA with an ultrasonic scalpel is associated with a higher risk of endothelial damage.

Interestingly, endothelial damage was lowest in group 4, in which RA harvesting was done as a pedicle using the ultrasonic scalpel. Probably, the distance of the ultrasonic scalpel to the graft vessel is far enough to avoid endothelial laceration and side branches can be dissected with less trauma. Nevertheless, dissection of the RA as a pedicle with an ultrasonic scalpel is far from being perfect. Only 3 of 10 specimens showed an overall intact endothelial layer, and in 1 case severe alterations were evident.

The skeletonization technique with scissors and clips has some evident advantages, which makes the technique quite attractive, mainly providing a long graft. Besides, sequential bypass grafting is easier, because the optimal anastomotic site can be identified much easier. Moreover, the skeletonized graft is free of adventitial tissue, which makes prevention of vasospasm through topical application of vasodilative drugs simple. The vessel diameter is usually larger, facilitating side-by-side-anastomosis and its visual control, and thus may leave less anastomotic stenosis. Because the RA, similar to the coronary arteries, is characterized as an artery of the muscular type, it tends to develop arteriosclerosis. The incidence of arteriosclerosis is much higher in the RA as compared with the internal mammary artery. After skeletonization, arteriosclerotic plaques are readily visible, which is not the case in a pedicled graft.

The underlying study has shown that skeletonization with scissors and clips is a technically more challenging and time consuming procedure, but it provides greater length of the graft and allows simple and safe utilization of the graft for sequential anastomoses. Skeletonization using ultrasonic a scalpel has no statistical advantage in length and has often been associated with severe endothelial damage. However, harvesting of the RA as a pedicle using the ultrasonic scalpel is much simpler and faster and seems to protect the endothelium, although there is no statistical evidence in comparison with skeletonization using scissors and clips.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Carpentier A., Guermonprez J.L., Deloche A., Frechette C., Dubost C. The aorta-to-coronary radial artery bypass graft. A technique avoiding pathologic changes in grafts. Ann Thorac Surg 1973;16:111-121.[Medline]
  2. Acar C., Jebara V., Portoghese M., et al. Revival of the radial artery for coronary artery bypass grafting. Ann Thorac Surg 1992;54:652-660.[Abstract]
  3. Acar C., Ramsheyi A., Pagny J.Y., et al. The radial artery for coronary artery bypass grafting: clinical and angiographic results at five years. J Thorac Cardiovasc Surg 1998;116:981-989.[Abstract/Free Full Text]
  4. He G.W., Yang C.Q., Starr A. Overview of the nature of vasoconstriction in arterial grafts for coronary operations. Ann Thorac Surg 1995;59:676-683.[Abstract/Free Full Text]
  5. Bhan A., Choudhary S.K., Saikia M., Sharma R., Venugopal P. Harmonic scalpel: initial experience. Asian Cardiovasc Thorac Ann 2001;9:3-6.[Abstract/Free Full Text]
  6. Buxton B., Fuller J., Gaer J., et al. The radial artery as a bypass graft. Curr Opin Cardiol 1996;11:591-598.[Medline]
  7. Reyes A.T., Frame R., Brodman R.F. Technique for harvesting the radial artery as a coronary artery bypass graft. Ann Thorac Surg 1995;59:118-126.[Abstract/Free Full Text]
  8. Tatoulis J., Buxton B.F., Fuller J.A. Bilateral radial artery grafts in coronary reconstruction: technique and early results in 261 patients. Ann Thorac Surg 1998;66:714-720.[Abstract/Free Full Text]
  9. Amano A., Takahashi A., Hirose H. Skeletonized radial artery grafting: improved angiographic results. Ann Thorac Surg 2002;73:1880-1887.[Abstract/Free Full Text]
  10. Garcia-Rinaldi R., Soltero E.R., Carballido J., Mojica J. Intraluminal milrinone for dilation of the radial artery graft. Tex Heart Inst J 1999;26(3):189-191.[Medline]
  11. Taggart D.P., Mathur M.N., Ahmad I. Skeletonization of the radial artery: advantages over the pedicled technique. Ann Thorac Surg 2001;72:298-299.[Abstract/Free Full Text]
  12. Boddy S.A.M., Ramsay J.W.A., Carter S.S.C., Webster P.J.R., Levison D.A., Whitfield H.N. Tissue effects of an ultrasonic scalpel for clinical surgical use. Urol Res 1987;15:49-52.[Medline]
  13. Isomura T., Suma H., Sato T., Horii T. Use of the harmonic scalpel for harvesting arterial conduits in coronary artery bypass. Eur J Cardiothorac Surg 1998;14:101-103.
  14. Lamm P., Juchem G., Weyrich P., Schütz A., Reichart B. The harmonic scalpel: optimizing the quality of mammary artery bypass grafts. Ann Thorac Surg 2000;69:1833-1835.[Abstract/Free Full Text]
  15. Posaciolu H., Atay Y., Cetinda B., Saribülbül O., Buket S., Hamulu A. Easy harvesting of radial artery with ultrasonically activated scalpel. Ann Thorac Surg 1998;65:984-985.[Abstract/Free Full Text]
  16. Ronan J.W., Perry L.A., Barner H.B., Sundt T.M., III Radial artery harvest: comparison of ultrasonic dissection with standard technique. Ann Thorac Surg 2000;69:113-114.[Abstract/Free Full Text]
  17. Royse A.G., Royse C.F., Groves K.L., 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]
  18. Benner K.U., Snell R.S. Klinische Anatomie. Atlas und Textbuch. . Herrsching: Atlantis, 1988.
  19. Gundry S.R., Jones M., Ischihara T., Ferrans V.J. Intraoperative trauma to saphenous veins: scanning electron microscopic comparison of preparation techniques. Ann Thorac Surg 1980;30:40-47.[Medline]



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