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Eur J Cardiothorac Surg 1999;15:247-250
© 1999 Elsevier Science NL


Free flow capacity of skeletonized versus pedicled internal thoracic artery grafts in coronary artery bypass grafts1

Olaf Wendler, Dietmar Tscholl, Qi Huang, Hans-Joachim Schäfers

Department of Thoracic and Cardiovascular Surgery, University Hospital Homburg, 66421 Homburg/Saar, Germany

Received 23 September 1998; received in revised form 14 December 1998; accepted 22 December 1998.

Corresponding author. Tel.: +49-6841-162-501; fax: +49-6841-162-788; e-mail: chowen@med-rz.uni-sb.de


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Objective: The internal thoracic artery (ITA) is the ideal conduit for coronary artery bypass grafting (CABG). The skeletonization technique of this arterial conduit has been proposed to reduce chest wall trauma, increase graft length and facilitate construction of sequential anastomoses. Nevertheless, some surgeons decline this technique because of potentially increased trauma to the ITA with impairment of flow. In this investigation we compared the free flow of skeletonized with that of pedicled ITA grafts. Methods: Two surgeons operated on 80 consecutive patients with coronary artery disease for elective CABG. In group I (n=40), the left ITA was dissected using the skeletonization technique. In group II (n=40), it was harvested as a pedicled graft. In 23 patients of group I both ITA's were dissected in skeletonized fashion for complete arterial revascularization. Diluted papaverine was instilled into the lumen of the ITA after distal transection of the vessel in both groups. Free flow of the ITA was registered before and 15 min after intraluminal application of diluted papaverine. Mean arterial pressure was maintained at 70 mmHg. Results: Before the application of papaverine, free flow of skeletonized and pedicled ITA grafts was identical between the two groups. After treatment with papaverine maximum free flow was significantly higher in the skeletonized ITA's (group I 197.2 (±66.6) ml/min; group II 147.1 (±70.5) ml/min; P<0.05). There was no significant difference between free flow after dilatation of the left and right ITA in group I (left 197.2 (±66.6) ml/min; right 198.9 (±61.8) ml/min). Conclusions: Preparation of the ITA with the skeletonization technique results in significantly, higher free flow capacity than in pedicled grafts. This may increase the safety of arterial revascularization by reducing the risk of ITA hypoperfusion syndrome.

Key Words: Coronary surgery • Arterial conduit • Internal thoracic artery • Skeletonization • Vessel preparation technique


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
The internal thoracic artery (ITA), currently, is the conduit of choice for coronary artery bypass grafting (CABG). Improved patency rates may explain superior long-term survival of patients after unilateral and bilateral ITA grafting [1] [2] [3] [4] [5].

Besides the well known pedicle preparation technique of this arterial conduit, skeletonization of the ITA has been described previously as an alternative [6]. Improved graft length and minimized chest wall trauma with reduced risk of sternal wound infection are the apparent advantages of these technique [4] [7]. In addition visual inspection of the skeletonized vessel is possible and sequential anastomoses appear technically easier to construct [7]. Nevertheless, some surgeons decline this preparation technique of the ITA due to the potential for increased trauma to the vessel with effects on the flow, due to vasospasm or mechanical irritation.

In this study we compared the free flow of skeletonized and pedicled ITA grafts during coronary revascularization.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Patients
Between March 1997 and February 1998 two groups of patients underwent elective CABG operated by two surgeons. In group I (n=40) the ITA was dissected by skeletonization, in group II (n=40) with a wide (2 cm) pedicle. In 23 patients of group I both ITA's were skeletonized to perform complete arterial revascularization using a T-graft. The two groups showed no significant differences due to sex (group I, 35 male; group II, 31 male) and age (group I, mean 60.1 (±10.4); group II, mean 65.8 (±9.2) years) of the patients.

Technique
Preparation of the ITA in group I was performed in the skeletonization technique, described by Cunningham et al. [7]. The left sternal wall was elevated with a modified Favaloro retractor. Loose alveolar tissue and parietal pleura, behind the sternum, were dissected away using cautery. After visual and palpatory inspection of the ITA, dissection was initiated in the third intercostal space at the midpoint. The endothoracic fascia was opened parallel and 5–8 mm medial to the internal thoracic vein using low cautery settings. By grasping the endothoracic fascia with a forceps the internal thoracic vein was pushed anteriorly and the ITA was exposed. Dissection continued with the preparation of the side branches, using small scissors. The ITA was never touched directly with the forceps. Branches were divided using low cautery settings or hemoclips. In group II harvesting of the pedicled ITA was performed in the standard technique.

Dissection in both groups proceeded from 2 to 3 cm cranial to the subclavian vein into the distal ITA-bifurcation. After complete preparation of the graft heparin was given and the vessel was divided distally.

Free flow of the ITA was measured directly after distal division of the vessel allowing it to bleed into a 100 ml container over 20 s and at zero resistance. Mean arterial pressure was maintained at 70 mm HG during assessment of ITA flow.

The first blood flow through the ITA was recorded and diluted papaverine (50 mg/20 ml ringers solution) was injected via an olive-tipped needle into the distal lumen of the graft. After injection of diluted papaverine the distal end of the graft was closed with a hemoclip. Fifteen minutes later the second flow measurement was performed in identical fashion, again maintaining a mean arterial pressure of 70 mmHg.

Statistics
Data were analyzed using the Stat-View software package. Flow measurement data were expressed as the mean±standard deviation. The unpaired t-test was used for comparison between the two groups. A P-value of less than 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
In both groups the preparation of the ITA was performed with satisfactory graft quality and all 103 vessels could be used for bypass grafting.

In group I, 16 patients (40%) received sequential anastomoses with the left ITA. In group II, sequential anastomoses with the left ITA were performed only in six patients (15%). Twenty-three patients of group I received complete arterial revascularization with both skeletonized ITA's using the T-graft technique [8]. In the left 1.52, and in the right ITA 2.04 coronary vessels were anastomosed, with a mean of 3.56 anastomoses per patient.

In each group 1 patient (2.5%) with unilateral ITA developed with sternal dehiscence during the first postoperative week. One patient in group I had been an insulin dependent diabetic for more than 10 years. Both patients received refixation of the sternum and were discharged after an unremarkable course. No patient with bilateral ITA suffered from sternal wound infection.

One patient died, from an overall in-hospital mortality of 1.25%, all others were discharged from hospital. This patient from group I, with an ejection fraction of 42%, suffered from intraoperative infarction and could not be weaned off bypass (Table 1).


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Table 1. Clinical results

 
Free flow of the left ITA before application of papaverine showed no significant difference between the two groups (group I, 51.3 (±39.1) ml/min; group II, 68.7 (±54.5) ml/min). After treatment with papaverine the free flow of the left ITA showed a significant increase in both groups (group I, 197.2 (±66,6) ml/min; group II, 147.1 (±70.5) ml/min). This maximal free flow was, statistically, significantly higher in the group with skeletonized ITA grafts. There was no significant difference in the maximum flow between the left and right skeletonized ITA (left, 197.2 (±66.6) ml/min; right, 198.9 (±61.8) ml/min) ( Fig. 1 ).



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Fig. 1. Free flow measurement results.

 

    Discussion
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Several investigations over the last years have shown that the ITA is the conduit of choice in CABG [1] [2] [3] [4] [5]. Improved patency rates, compared with venous grafts, result in fewer ischemic events and improved long-term survival. Bilateral ITA grafting has been performed for more than 15 years and new data show superior long-term results [2] [3] [4] [9] [10] [11].

Nevertheless, there are some disadvantages in using the ITA as a graft which can result in higher perioperative morbidity and mortality. The collateral blood supply of the sternum is reduced after dissection of the ITA [12]. In bilateral ITA grafting this leads to a higher rate of sternal wound infections [11] [13] [14]. The pedicle surrounding the ITA makes construction of sequential anastomoses more difficult and complete arterial revascularization with sequential anastomoses less practicable. Flow may be limited due to vasospasm or mechanical irritation of the arterial vessel. The hypoperfusion syndrome in CABG with ITA grafting is a well known problem of a disproportion between ITA flow and myocardial demand and has a high mortality [15].

In 1987, Keeley [6] described the operative technique of skeletonized dissection of the ITA. Nevertheless, the pedicled surgical variant has developed into widespread, clinical practice due to the apparently reduced risk of trauma to the ITA. Cunningham in 1992 [7], published his experience with the standardized operative technique to skeletonize the ITA. Excellent clinical long-term results with these conduits in 560 consecutive patients have been reported by Bical et al. in 1996 [4].

An accepted advantage of this technique is the improved length of the skeletonized conduit. The quality and caliber of the vessel is easily ascertained and by unimpaired visual inspection, dissection of the ITA can be ruled out. Cunningham [7], reported that sequential anastomoses were technically easier to construct with this approach. After our personal, sometimes cumbersome experience, using pedicled ITA grafts for multiple sequential anastomoses, we were also impressed by the technical ease using the skeletonized ITA for this purpose.

During dissection of the ITA, injury of the surrounding structures is minimized. Anatomical studies by DeJesus et al. [16] have shown that sternal vascularization is better preserved after skeletonized preparation of the ITA which has been hypothesized to reduce sternal wound infections. This compares favorably with clinical data of bilateral skeletonized ITA dissection [3] [4] [7] with reported sternal wound infection in less than 2% of patients. In bilateral pedicled ITA's Kochoukos [11] presented a rate of sternal wound infection in 6.9%.

Nevertheless, some surgeons are concerned about vasospasm or mechanical irritation of the ITA due to skeletonization. Different groups have shown the positive effect of papaverine on the flow of the ITA. Mills [17] and Dregelid [18] published that treatment with intraluminal application of diluted papaverine results in superior flow rates of the ITA in comparison to spraying it with papaverine. Some histological investigations showed damage of the endothelium by intraluminal application of the acidic papaverine and recommended only external application [19]. On the other hand, there are physiological investigations by Hillier [20], where normal endothelial function and increased lumina of ITA's after treatment with intraluminal papaverine were found. Therefore, we prefer the instillation of diluted papaverine into the lumen of the ITA to maximize free flow and dilate the arterial conduit.

By measuring free flow of the ITA the maximum flow capacity of the graft is determined without interference of the peripheral coronary bed. We found the maximum free flow in ITA's which were harvested with the skeletonization technique. There is a trend to a somewhat reduced flow directly after the preparation, which may be due to vasospasm. This difference, however was not statistically significant. This pattern changed completely after vasodilation with diluted papaverine, in that the free flow of skeletonized ITA's was significantly higher compared with pedicled grafts. This may be the result of less restriction to these skeletonized grafts by fascia and fibrotic bands, resulting in more immediate and pronounced vasodilatation.

In previous investigations by Choi [21] the free flow of pedicled and skeletonized grafts was not significantly different. But in this study pedicled ITA's after intraluminal treatment with diluted papaverine were compared with skeletonized ITA's sprayed only with papaverine.

At our institution skeletonization of the ITA was a cornerstone on the road to complete arterial grafting. With this technique the percentage of complete arterial procedures in coronary artery disease rose from 2.8% in 1996 to nearly 30% in the first half of 1998. Between March 1997 and August 1998, 123 patients with triple vessel disease received complete arterial revascularization with only two grafts using the T-graft technique described by Tector et al. [8]. In 49 patients bilateral skeletonized ITA's and in 56 the left skeletonized ITA and one radial artery were used as arterial conduits. In the group with skeletonized bilateral ITA's the incidence of sternal dehiscence was 0%. No cases of ITA hypoperfusion syndrome occurred in both groups. The in-hospital mortality of all patients operated with bilateral ITA or left ITA and radial artery T-grafts was 1.9%. It has been our impression that the risk of postoperative ITA hypoperfusion syndrome – with its high mortality after CABG – could thus, be reduced by using skeletonized ITA's.

In summary, the skeletonization technique in dissection of the ITA has advantages in increase of length, reduction on chest wall trauma and easier construction of sequential anastomoses [7]. We found an improvement of free flow in the skeletonized grafts after application of papaverine which may increase safety of arterial revascularization by reducing the risk of ITA hypoperfusion syndrome. This makes the prolonged dissection time of 10–15 min acceptable. With this technique complete arterial revascularization with sequential anastomoses and T-grafts may become safer and easier.


    Footnotes
 
Presented at the 12th Annual Meeting of the European Association for Cardio-thoracic Surgery, Brussels, Belgium, September 20–23, 1998. Back


    Appendix A. Conference discussion
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 
Dr B. Walpoth (Bern, Switzerland): We have published a similar study in the EJCTS. What is interesting in your presentation are higher free flow values after vasodilatation in the skeletonized vessel (without peripheral resistance). I think there is maybe a word of caution, because you have to measure flow after distal anastomosis. We did such measurements, and as you probably know, there were no significant differences between the skeletonized and pediculated IMA grafts. Do you have any explanation why the skeletonized IMA graft might have a higher flow reserve, if I may call that flow reserve?

Dr Wendler: May I answer the second question first. We have seen that dilatation of the skeletonized grafts is increased compared with the pedicled ones. We think the reason is that the pedicle gives restriction to the ITA itself. This might be the main reason for the extended dilatation after intraluminal papaverine.

We agree that the free flow is only one determination for a good graft function, and so we started a postoperative examination of these patients with intravascular flow wire measurement. These results are not completed yet and therefore they haven't been presented here.

Dr Walpoth: Can you give us a hint how the flow is on postoperative measurements?

Dr Wendler: Yes. We have measured the flow in the main stem of the left ITA in patients with T-grafts. They showed flow up to 200 ml/min. The coronary flow reserve, which was relatively low early postoperative, something like 1.5–1.7, increased in the first 6 months. We have only examined the first ten patients now, so I don't know if these results will be confirmed.

Dr E. Bodor (Budapest, Hungary): Is there not a higher risk of the damage of IMA in skeletonized than in the pedicled. What is your experience?

Dr Wendler: We started with skeletonization of the ITA, because of an article from Bical et al., 1996 [4], where they presented 560 consecutive patients with bilateral skeletonized grafts and the benefit of reduced wound infection. They had excellent long-term survival and patency, with patency rates of 97% over a period of more than 10 years.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Appendix A. Conference...
 References
 

  1. 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]
  2. Fiore A.C., Naunheim K.S., Dean P., Kaiser G.C., Pennington D.G., Willman V.L., McBride L.R., Barner H.B. Results of internal thoracic artery grafting over 15 years: single versus double grafts. Ann Thorac Surg 1990;49:202-209.[Abstract]
  3. Galbut D.L., Traad E.A., Dorman M.J., DeWitt P.L., Larsen P.B., Kurlansky P.A., Button J.H., Ally J.M., Gentsch T.O. Seventeen-year experience with bilateral internal mammary artery grafts. Ann Thorac Surg 1990;49:195-201.[Abstract]
  4. Bical O., Braunberger E., Fischer M., Robinault J., Foiret J.C., Fromes Y., Gaillard D., Vanetti A. Bilateral skeletonized mammary artery grafting: experience with 560 consecutive patients. Eur J Cardio-thorac Surg 1996;10:971-976.[Abstract]
  5. Calafiore A.M., Di Giammarco G., Luciani N., Maddestra N., Di Nardo E., Angelini R. Composite arterial conduits for a wider arterial myocardial revascularization. Ann Thorac Surg 1994;58:185-190.[Abstract]
  6. Keeley S.B. The skeletonized internal mammary artery. Ann Thorac Surg 1987;44:324-325.[Abstract]
  7. Cunningham J.M., Mohammad A.G., Fardin R., Meek R.A. Considerations in the skeletonization technique of internal thoracic artery dissection. Ann Thorac Surg 1992;54:947-951.[Abstract]
  8. Tector A.J., Amundsen S., Schmahl T.M., Kress D.C., Peter M. Total revascularization with T-grafts. Ann Thorac Surg 1994;57:33-39.[Abstract]
  9. Dion R., Etienne P.Y., Verhelst R., Khoury G., Rubay J., Bettendorff P., Hanet C., Wyns W. Bilateral mammary grafting. Eur J Cardio-thorac Surg 1993;7:287-294.[Abstract]
  10. Dewar L.R.S., Jamieson E., Janusz M.T., Adeli-Sardo M., Germann E., MacNab J.S., Tyers G.F. Unilateral versus bilateral internal mammary revascularization. Circulation 1995;92(Suppl. II):II8-II13.
  11. Kouchoukos N.T., Wareing T.H., Murphy S.F., Pelate C., Marshall W.G. Risks of bilateral mammary artery bypass grafting. Ann Thorac Surg 1990;49:210-219.[Abstract]
  12. Seyfer A.E., Shriver C.D., Miller T.R., Graeber G.M. Sternal blood flow after median sternotomy and mobilization of the internal mammary arteries. Surgery 1988;104(5):900-904.
  13. Grossi E.A., Esposito R., Harris L.J., Crooke G.A., Galloway A.C., Colvin S.B., Culliford A.T., Baumann F.G., Yao K., Spencer F.C. Sternal wound infections and use of internal mammary artery grafts. J Thorac Cardiovasc Surg 1991;102:342-347.[Abstract]
  14. He G.W., Ryan W.H., Acuff T.E., Bowman R.T., Douthit M.B., Yang C.Q., Mack M.J. Risk factors for operative mortality and sternal wound infection in bilateral internal mammary artery grafting. J Thorac Cardiovasc Surg 1994;107:196-202.[Abstract/Free Full Text]
  15. Jones E.L., Lattouf A.M., Weintraub W.S. Catastrophic consequences of the internal mammary artery hypoperfusion. J Thorac Cardiovasc Surg 1989;98:902-907.[Abstract]
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  19. Noera G., Pensa P., Lodi R., Lamarra M., Biagi B., Guelfi P. Influence of different harvesting techniques on the arterial wall of the internal mammary artery graft: microscopic analysis. Thorac Cardiovasc Surgeon 1993;41:16-20.[Medline]
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R. Cartier, M. Leacche, and P. Couture
Changing pattern in beating heart operations: use of skeletonized internal thoracic artery
Ann. Thorac. Surg., November 1, 2002; 74(5): 1548 - 1552.
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K.-B. Kim, K. R. Cho, W.-I. Chang, C. Lim, B. M. Ham, and Y. L. Kim
Bilateral skeletonized internal thoracic artery graftings in off-pump coronary artery bypass: early result of Y versus in situ grafts
Ann. Thorac. Surg., October 1, 2002; 74(4): S1371 - 1376.
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Ann. Thorac. Surg.Home page
G. Sakaguchi, E. Tadamura, M. Ohnaka, K. Tambara, K. Nishimura, and M. Komeda
Composite arterial Y graft has less coronary flow reserve than independent grafts
Ann. Thorac. Surg., August 1, 2002; 74(2): 493 - 496.
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A. Amano, A. Takahashi, and H. Hirose
Skeletonized radial artery grafting: improved angiographic results
Ann. Thorac. Surg., June 1, 2002; 73(6): 1880 - 1887.
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Y. Takami and H. Ina
Effects of skeletonization on intraoperative flow and anastomosis diameter of internal thoracic arteries in coronary artery bypass grafting
Ann. Thorac. Surg., May 1, 2002; 73(5): 1441 - 1445.
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T. Markwirth, B. Hennen, B. Scheller, H.-J. Schafers, and O. Wendler
Flow wire measurements after complete arterial coronary revascularization with T-grafts
Ann. Thorac. Surg., March 1, 2001; 71(3): 788 - 793.
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Ann. Thorac. Surg.Home page
J. Gurevitch, M. Matsa, Y. Paz, A. Kramer, D. Pevni, I. Shapira, and R. Mohr
Effect of age on outcome of bilateral skeletonized internal thoracic artery grafting
Ann. Thorac. Surg., February 1, 2001; 71(2): 549 - 554.
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O. Wendler and H.-J. Schafers
Have they really seen the effect of the native coronary blood flow?
Ann. Thorac. Surg., July 1, 2000; 70(1): 341 - 341.
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J. Thorac. Cardiovasc. Surg.Home page
O. Wendler, B. Hennen, T. Markwirth, J. Konig, D. Tscholl, Q. Huang, E. Shahangi, H.-J. Schafers, and S. H. G. Borst
T GRAFTS WITH THE RIGHT INTERNAL THORACIC ARTERY TO LEFT INTERNAL THORACIC ARTERY VERSUS THE LEFT INTERNAL THORACIC ARTERY AND RADIAL ARTERY: FLOW DYNAMICS IN THE INTERNAL THORACIC ARTERY MAIN STEM
J. Thorac. Cardiovasc. Surg., November 1, 1999; 118(5): 841 - 848.
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