HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

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): Tadahiro Sasajima Naoki Hayashida Lester R. Sauvage Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Sasajima, T. Articles by Sauvage, L. R. Search for Related Content PubMed PubMed Citation Articles by Sasajima, T. Articles by Sauvage, L. R.

Ann Thorac Surg 1998;65:1009-1013
© 1998 The Society of Thoracic Surgeons

Effect of Skeletonizing Dissection on the Internal Thoracic Artery

^a The Hope Heart Institute, Seattle, Washington, USA

Accepted for publication October 24, 1997.

Address reprint requests to Dr Sauvage, The Hope Heart Institute, 528 18th Ave, Seattle, WA 98122

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Skeletonization of the internal thoracic artery (ITA) produces greater length for coronary bypass grafting. We studied the effect of skeletonization on the morphology, histology, and tissue viability of the ITA wall.

Methods. Six mongrel dogs underwent unilateral ITA dissection; the contralateral ITA was the control. Study periods were 3 weeks (n = 3) and 12 weeks (n = 3). At sacrifice, the entire anterior chest wall was removed and dynamically fixed with formalin. Extensive histologic comparisons were performed on three tissue blocks taken from each ITA, 2, 8, and 24 cm from their origin.

Results. Flows at the end of the study were comparable to measurements taken during operation, immediately after skeletonization. Grossly, the ITA wall was not injured by skeletonization and there was no adventitial hematoma or bleeding from the sealed branch ends. Microscopic observations showed intact, normal wall structures. Histologic data showed no major significant difference between controls and skeletonized ITAs.

Conclusions. Careful skeletonizing dissection is not detrimental to the integrity of ITAs, which justifies their use for myocardial revascularization.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Studies have shown that the internal thoracic artery (ITA) provides better long-term patency and survival than any other coronary artery bypass graft [1, 2], and is considered by many to be the preferred graft [3]. Use of the ITA in the elderly [4, 5] and for reoperation [6, 7] has increased.

The main limitation on ITA grafting is length. To overcome this, various techniques have been developed, including one that permits complete revascularization of the left ventricle using only the ITAs [8]. These techniques involve skeletonizing dissection. Although studies have shown that the skeletonized ITA provides additional usable length with adequate flow, several potential disadvantages have not been investigated [9–11]. The major concerns are whether the skeletonization will cause deterioration and interrupt the integrity of the ITA wall structure, including the flow surface, the nutrition from the vasa vasorum, and tissue viability, and whether it will influence flow volume adversely. Therefore, the objective of this study was to determine the effects of skeletonizing dissection on the morphology, histology, and tissue viability of the ITA.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Six randomly selected mongrel dogs of both sexes, weighing 18 to 28 kg (average, 21.5 ± 4.4 kg), were used in this study. Their care and use complied with the "Principles of Laboratory Animal Care" and the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985).

Skeletonization of the internal thoracic artery
Paired comparisons were made. Each subject underwent unilateral ITA dissection, and the contralateral undissected ITA served as the control; sides were altered by cases. The 6 subjects were equally divided into two groups with study time periods of 3 and 12 weeks. All subjects were given proper anesthesia, which was induced with 5 to 10 mL of 4% thiamylal intravenously and then maintained with a combination of 0.5 to 1.0% halothane and a mixture of nitrous oxide and oxygen in a 2:1 ratio through an endotracheal tube connected to a closed circuit respirator. The entire ITA length was approached by dual thoracotomies through the fourth and sixth intercostal spaces, and was carefully skeletonized using a bipolar cauterization technique from its origin to the terminal point at the bifurcation of the musculophrenic and the superior epigastric arteries [12]. The two terminal branches were retained as the runoff, and all the other ITA mural branches were divided. At the completion of the procedure, the skeletonized ITA was left free in the chest and the wounds were closed in a routine manner. Blood flow was measured 2 cm distal to the ITA origin before dissection (for the control) and after skeletonization with a Transonic flowmeter (T-208; Transonic Systems Inc, Ithaca, NY).

Specimen retrieval and preparation
At the end of the implant period the subjects were properly anesthetized and fully heparinized. A small supraclavicular incision was made to approach the proximal part of the study ITA, again for measuring the flow before harvesting. The dog was euthanized with an overdose of potassium chloride. The bilateral subclavian arteries were then ligated and severed 1 cm proximally and distally to the ITA origin, with attachment of a 2-cm segment of the proximal part of the vertebral artery at the opposite side of the origin of the ITA. The entire anterior chest wall (about 20 cm wide and 25 cm long, including the sternum, costal cartilages, and full length of the bilateral ITAs from the subclavian artery to the musculophrenic and superior epigastric arteries) was removed as an intact plate (Fig 1A).

View larger version (57K): [in this window] [in a new window]   Fig 1. Methods for evaluating morphology and histology at an optimal physiologic pressure. (A) Entire anterior chest wall, containing both the skeletonized internal thoracic arteries and the control, is removed. (B) Device for dynamic fixation of the specimen.

Histologic evaluation
After fixation, three segmental tissue blocks were taken from each of the paired control and study ITAs at the same levels, 2, 8, and 14 cm from their origin. Cross-sections were then made from these tissue blocks and stained with hematoxylin and eosin for general histologic study, modified Verhoeff’s van Gieson staining (procedure HT 25; Sigma, St. Louis, MO) for identification of the internal elastic laminae, median elastic laminae, and external elastic laminae, and Masson trichrome for evaluation of the change in the amount of collagen after skeletonization.

Photomicrographs of all cross-sections were taken. A computer image analysis system (Macintosh, Apple Computer Inc, Cupertino, CA) with the public domain program "Image" (NIH Research Service Branch, NIMH, Bethesda, MD) was used to measure the circumference of the internal elastic laminae, including the endothelial lining, external elastic laminae, and the outer boundary of the adventitia, which was defined as the outermost portion of the dense connective tissue. The luminal diameter, the average thickness of the media between the internal and external elastic laminae, and the average thickness of the adventitia were automatically calculated by the system according to the formulas: , where D = diameter; Ciel = circumference of the internal elastic laminae; Th-Med = average medial thickness; Ceel = circumference of the external elastic laminae; Th-Adv = average adventitial thickness; and C_Adv = circumference of the adventitia.

Because there was no intimal thickening in any sections, intimal thickness was negligible. The number of medial elastic laminae varied in different locations within the cross-sections; thus, each cross-section was randomly and equally divided by 45 degrees into eight regions. Instances of well-stained, noninterrupted medial elastic laminae present in each region were counted and then averaged for each cross section.

Statistical analysis
Quantitative data were expressed as means ± standard deviations. For statistical evaluation, the Student’s t test was used with a StatView software package (Abacus Concepts, Inc, Berkeley, CA). Differences were considered statistically significant when the p value was less than 0.05.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
General observations and flow measurement
Grossly, the ITA wall was not injured or deformed during skeletonization with the bipolar cautery and there was no hematoma in the adventitia or bleeding from the sealed branch ends. Approximately 18 to 26 branches were divided along each of the skeletonized ITAs. In specimen harvesting, it was found that the skeletonized ITAs had partially adhered to the lung or anterior parietal pleura. They were pliable and had not become fibrotic. All were patent, without kinking or gross coarctation.

At the end of the study, each skeletonized ITA was delivering a flow comparable to the flow at the beginning of the study. The study ITA flow before skeletonization was 23.6 ± 10.6 mL/min. Immediately after dissection, the flow was decreased to 10.6 ± 9.2 mL/min, which was associated with the closure of all runoff to the mural branches of the ITAs. The mean flow at the end of the study was 10.4 ± 10.5 mL/min for both the 3-week and 12-week groups; this was not significantly different from the flow rate at the beginning of the study.

Histologic evaluation
Microscopic observations showed that the wall structure for both the 3-week and 12-week skeletonized ITAs was intact and normal (Fig 2). There were no substantial differences compared with the control ITAs. Endothelial cells lined the luminal surface, there was no intimal thickening or hyperplasia, there was no necrosis or fibrosis in the media, and the staining characteristics and morphology of the cellular components in the wall were normal without signs of degeneration or lysis; the amount of extracellular collagen was also not increased. The adventitia of the skeletonized ITAs was incorporated into the surrounding connective tissue layer in which many microvessels had developed, extending into the adventitia. This layer seemed to have formed later, due to surgical dissection.

View larger version (103K): [in this window] [in a new window]   Fig 2. Histologic comparison of the control and skeletonized internal thoracic arteries (ITAs). Top row, hematoxylin and eosin, original magnification x10; middle row, hematoxylin and eosin, original magnification x200; bottom row, Verhoeff van Gieson, original magnification x200.)

	Comment

Top Abstract Introduction Material and methods Results Comment References

The critical element for generating a quality skeletonized ITA is a careful dissection technique that avoids injury to the vessel. Daly and colleagues [13] reported poor results of stripped-free ITA grafts. This may have resulted from a different dissection technique rather than inevitable consequences of skeletonization. Studies have shown that the bipolar cautery is a very useful tool. When properly and carefully used, it will not only avoid damage to the flow surface and wall structure, but also provide a secure seal on severed branch ends during ITA dissection [12, 14]. These advantages are again apparent in this report.

This study showed that the histologic structure had no substantial change after skeletonization. It has been thought that the thinner walled arteries could be nourished entirely by luminal diffusion, which can reach a range of 350 to 600 µm into the superficial part of the arterial wall [15, 16]. In our measurements, the thickest part of the ITA media was approximately 152 µm, which could be reached by luminal diffusion, thus avoiding ischemia despite total disruption of the vasa vasorum.

Studies have shown that revascularization of the adventitial vasa vasorum after dissection could begin 3 days [17] or within 1 week [18–20] after operation. This study also demonstrated quantitatively that the number of vasa vasorum was greater in the adventitia of skeletonized ITAs, compared with controls, in both the 3- and 12-week groups (see Table 1). In this study the skeletonized ITA was left free in the chest after dissection; if it had been placed against the myocardial surface, as in coronary artery bypass grafting, revascularization in the adventitia presumably might have developed sooner and to a greater degree.

The blood flow rate through the ITA decreased after skeletonizing dissection. This was obviously caused by closure of all of the mural branches during the dissection, which resulted in an increase of flow resistance. It might be expected that the flow would resume or increase with the establishment of new anastomoses along the ITA if they were used for bypass grafting [21–23]. The diameter of the ITA was also slightly decreased after dissection (see Table 1). This was believed to be associated with a reversible spasm due to surgical manipulation and decreased flow. If the ITA wall is not injured during dissection, this sort of spasm might be spontaneously corrected or would be eradicated by increased blood flow through the ITA lumen after anastomoses made during the grafting procedure. Our previous study has demonstrated that the ITA luminal diameter adaptively enlarges after blood flow increase, and diminishes after blood flow decrease, with a tendency to normalize wall shear stress [24]. This suggests that even if the caliber of the skeletonized ITA decreases temporarily after dissection, its caliber will gradually increase to adapt to the demands of increased flow after coronary bypass grafting with a persistently good runoff. Data from this study also demonstrated that the skeletonized ITA could deliver a quite stable flow throughout the observation period (see Table 1).

In summary, skeletonizing dissection did not have detrimental effects on the morphology, histology, and tissue viability of ITAs. These observations justify the use of the skeletonized ITA for complete revascularization of the left ventricle. However, careful dissection to avoid any injury to the ITA wall is essential in this procedure.

	References

Top Abstract Introduction Material and methods Results Comment References

 

1. Barner H.B., Standeven J.W., Reese J. Twelve-year experience with internal mammary artery for coronary artery bypass. J Thorac Cardiovasc Surg 1985;90:668-675.[Abstract]
2. Loop F.D., Lytle W.B., Cosgrove D.M., et al. Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events. N Engl J Med 1985;314:1-6.
3. Sabiston D.C., Jr, Spencer F.C. Surgery of the chest, 6 ed. Philadelphia: Saunders, 1995:1911-1912.
4. Gardner T.J., Greene P.S., Rykiel M.F., et al. Routine use of the left internal mammary artery graft in the elderly. Ann Thorac Surg 1990;49:188-194.[Abstract/Free Full Text]
5. Azariades M., Fessler C.L., Floten H.S., Starr A. Five-year results for coronary bypass grafting for patients older than 70 years: role of internal mammary artery. Ann Thorac Surg 1990;50:940-945.[Abstract/Free Full Text]
6. Loop F.D., Lytle B.W., Cosgrove D.M. Bilateral internal thoracic artery grafting in reoperations. Ann Thorac Surg 1991;52:3-4.[Free Full Text]
7. Galbut D.L., Traad E.A., Dorman M.J., et al. Bilateral internal mammary artery grafts in reoperative and primary coronary bypass surgery. Ann Thorac Surg 1991;52:20-28.[Abstract/Free Full Text]
8. Sauvage L.R., Wu H.D., Kowalsky T.E., et al. Healing basis and surgical techniques for complete revascularization of the left ventricle using only the internal mammary arteries. Ann Thorac Surg 1986;42:449-465.[Abstract/Free Full Text]
9. Cunningham J.M., Gharavi M.A., Fardin R., Meek R.A. Considerations in the skeletonization technique for internal thoracic artery dissection. Ann Thorac Surg 1992;54:947-951.[Abstract/Free Full Text]
10. Loop F.D., Lytle B.W., Cosgrove D.M., Golding L.A.R., Taylor P.C., Stewart R.W. Free (aorta-coronary) internal mammary artery graft. Late results. J Thorac Cardiovasc Surg 1986;92:827-831.[Abstract]
11. Van Son J.A.M., Smedts F., Vincent J.G., van Lier H.J.J., Kubat K. Comparative anatomic studies of various arterial conduits for myocardial revascularization. J Thorac Cardiovasc Surg 1990;99:703-707.[Abstract]
12. Yoshida H., Wu M.H., Kouchi Y., Onuki Y., Shi Q., Sauvage L.R. Comparison of the effect of monopolar and bipolar cauterization on skeletonized, dissected internal thoracic arteries. J Thorac Cardiovasc Surg 1995;110:504-510.[Abstract/Free Full Text]
13. Daly R.C., McCarthy P.M., Orszulak T.A., Schaff H.V., Edwards W.D. Histologic comparison of experimental coronary artery bypass grafts. J Thorac Cardiovasc Surg 1988;96:19-29.[Abstract]
14. Sauvage L.R. Extensive myocardial revascularization using only internal thoracic arteries for grafting the anterior descending, circumflex and right systems. In: Meyers W.O., ed. Cardiac surgery: state of the art reviews. Philadelphia: Hanley & Belfus, 1992:387-419.
15. Geiringer E. Intimal vascularization and atherosclerosis. J Path Bact 1951;63:201-211.[Medline]
16. Goff S.G., Wu H.D., Sauvage L.R., et al. Differences in reendothelialization after balloon catheter removal of endothelial cells, superficial endarterectomy, and deep endarterectomy. J Vasc Surg 1988;7:119-129.[Medline]
17. Wyatt A.P., Rothnie N.G., Taylor G.W. The vascularization of vein grafts. Br J Surg 1964;51:378-381.[Medline]
18. McCune W.S., Thistlethwaite J.R., Keshishian J.M., Blades B. The nutrition of blood vessel grafts. Surg Gynecol Obstet 1952;94:311-316.[Medline]
19. Brook W.H., Baird R.J., Silver M.D. Vasa vasorum in autogenous dog vein bypass grafts. J Cardiovasc Surg 1974;15:655-659.[Medline]
20. McGeachie J., Campbell P., Prendergast F. A quantitative study of revascularization by vasa vasorum and its relationship to intimal hyperplasia. Ann Surg 1981;194:100-107.[Medline]
21. Vogel J.H.K., McFadden R.B., Sence R., Jahnke E.J., Jr, Love J.W. Quantitative assessment of myocardial performance and graft patency following coronary bypass with the internal mammary artery. J Thorac Cardiovasc Surg 1978;75:487-498.[Medline]
22. Singh R.N., Sosa J.A. Internal mammary artery: a "live" conduit for coronary bypass. J Thorac Cardiovasc Surg 1984;87:936-938.[Abstract]
23. Ivert T., Huttunen K., Landou C., Bjork V.O. Angiographic studies of internal mammary artery grafts 11 years after coronary bypass grafting. J Thorac Cardiovasc Surg 1988;96:1-12.[Abstract]
24. Kouchi Y., Onuki Y., Wu M.H.-D., Shi Q., Sauvage L.R. Effect of altered blood flow on the caliber and morphology of the internal thoracic artery in the dog. J Thorac Cardiovasc Surg 1997;113:114-120.[Abstract/Free Full Text]

This article has been cited by other articles:

				M. Malinowski, M. A. Deja, K. S. Golba, T. Roleder, J. Biernat, and S. Wos Perivascular tissue of internal thoracic artery releases potent nitric oxide and prostacyclin-independent anticontractile factor Eur J Cardiothorac Surg, February 1, 2008; 33(2): 225 - 231. [Abstract] [Full Text] [PDF]

				S. G. Raja and G. D. Dreyfus Internal Thoracic Artery: To Skeletonize or Not to Skeletonize? Ann. Thorac. Surg., May 1, 2005; 79(5): 1805 - 1811. [Abstract] [Full Text] [PDF]

				T. Athanasiou, M.-C. Crossman, G. Asimakopoulos, A. Cherian, A. Weerasinghe, B. Glenville, and R. Casula Should the internal thoracic artery be skeletonized? Ann. Thorac. Surg., June 1, 2004; 77(6): 2238 - 2246. [Abstract] [Full Text] [PDF]

				G. Bolotin, W. W. Scott Jr, T. C. Austin, P. J. Charland, A. P. Kypson, L. W. Nifong, K. Salleng, and W. R. Chitwood Jr Robotic skeletonizing of the internal thoracic artery: is it safe? Ann. Thorac. Surg., April 1, 2004; 77(4): 1262 - 1265. [Abstract] [Full Text] [PDF]

				T. Ueda, S. Taniguchi, T. Kawata, K. Mizuguchi, M. Nakajima, and A. Yoshioka Does skeletonization compromise the integrity of internal thoracic artery grafts? Ann. Thorac. Surg., May 1, 2003; 75(5): 1429 - 1433. [Abstract] [Full Text] [PDF]

				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. [Abstract] [Full Text] [PDF]

				H. Jeanmart, L. P. Perrault, N. Desjardins, O. Chavanon, M. Carrier, and J. D. Fonger Arterial balloon catheter: a new atraumatic device for dilating arterial grafts Ann. Thorac. Surg., September 1, 2001; 72(3): 810 - 815. [Abstract] [Full Text] [PDF]

				T. Higami, T. Yamashita, H. Nohara, K. Iwahashi, T. Shida, and K. Ogawa Early results of coronary grafting using ultrasonically skeletonized internal thoracic arteries Ann. Thorac. Surg., April 1, 2001; 71(4): 1224 - 1228. [Abstract] [Full Text] [PDF]

				M. A. Deja, S. Wos, K. S. Golba, P. Zurek, W. Domaradzki, R. Bachowski, and T. J. Spyt Intraoperative and laboratory evaluation of skeletonized versus pedicled internal thoracic artery Ann. Thorac. Surg., December 1, 1999; 68(6): 2164 - 2168. [Abstract] [Full Text] [PDF]

				M. Gaudino, A. Toesca, S. L. Nori, F. Glieca, and G. Possati Effect of skeletonization of the internal thoracic artery on vessel wall integrity Ann. Thorac. Surg., November 1, 1999; 68(5): 1623 - 1627. [Abstract] [Full Text] [PDF]

				T. Sasajima, V. Bhattacharya, M. Hong-De Wu, Q. Shi, N. Hayashida, and L. R. Sauvage Morphology and histology of human and canine internal thoracic arteries Ann. Thorac. Surg., July 1, 1999; 68(1): 143 - 148. [Abstract] [Full Text] [PDF]

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): Tadahiro Sasajima Naoki Hayashida Lester R. Sauvage Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Sasajima, T. Articles by Sauvage, L. R. Search for Related Content PubMed PubMed Citation Articles by Sasajima, T. Articles by Sauvage, L. R.