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Ann Thorac Surg 2003;75:1429-1433
© 2003 The Society of Thoracic Surgeons

Original article: cardiovascular

Does skeletonization compromise the integrity of internal thoracic artery grafts?

Takashi Ueda, MDa,*, Shigeki Taniguchi, MDa, Tetsuji Kawata, MDa, Kazumi Mizuguchi, MDa, Mitsuru Nakajima, MDb, Akira Yoshioka, MDb

a department of Surgery III, Nara Medical University, Kashihara, Nara, Japan,
b department of Pediatrics, Nara Medical University, Kashihara, Nara, Japan

Accepted for publication November 21, 2002.

Keywords 23

* Address reprint requests to Dr Ueda, Department of Surgery III, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8522, Japan. (Email: u-taka{at}naramed-u.ac.jp).


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background: There are few reports that demonstrate the chronologic changes in the functional integrity of the internal thoracic artery (ITA) wall after skeletonization. We investigated the impact of skeletonization on ITA wall integrity by immunohistochemical analyses in acute and chronic phases.

Methods: Nine mongrel dogs underwent bilateral ITA dissection with one skeletonized vessel and the other pedicled. The following studies were performed 1 week (acute phase, n = 3) and 12 weeks (chronic phase, n = 6) after ITA harvesting. All specimens of the ITAs were stained by antibodies against von Willebrand Factor (VWF), endothelial nitric oxide synthase (eNOS), inducible nitric oxide synthase (iNOS), and proliferating cell nuclear antigen (PCNA). After observation with confocal laser scanning microscopy, quantitative analyses of the staining signal for VWF and eNOS expressed on endothelial cells were performed.

Results: There were significantly more microvessels positive for VWF in the adventitia of skeletonized ITAs than in the adventitia of pedicled ITAs but the expression of PCNA in both groups was minimal, as in normal vessels. iNOS was not detected in any specimen. The intensity of VWF and eNOS expressed by endothelial cells had no significant differences between groups at either phase.

Conclusions: The functional integrity of skeletonized ITA was similar to that of pedicled ITA in both acute and chronic phases. Although skeletonization induced neovascularization in the adventitia it did not induce proliferation of smooth muscle cells in the media, which is supposed to be a feature of vascular remodeling.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
The internal thoracic arteries (ITAs) are the supreme grafts for coronary revascularization and the skeletonization technique of the ITAs has been used to accomplish complete myocardial revascularization using arterial grafts. Although previous studies showed that skeletonization of the ITA was clinically acceptable, few reports demonstrated the chronologic changes in the functional integrity of the vessel wall after skeletonization. We investigated the impact of skeletonization on ITA wall integrity in both acute and chronic phases by immunohistochemical analyses using confocal laser scanning microscopy (CLSM).


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Nine mongrel dogs weighing 10 to 15 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" (National Institutes of Health publication 85-23, revised 1985).

Ita harvest and specimen preparation
Each dog underwent bilateral ITA dissection with one skeletonized and the other pedicled. The 9 dogs were divided into two groups with study time periods of 1 week (acute phase, n = 3) and 12 weeks (chronic phase, n = 6). All animals underwent induction of anesthesia with intravenous injection of 5 mL of 4% thiamylal. After endotracheal intubation the animals were ventilated mechanically and anesthesia was maintained by supplying a mixture of nitrous oxide and oxygen (2:1v/v), with 0.5% to 3.0% of halothane added. The bilateral ITAs were dissected through a median sternotomy using an ultrasonic scalpel (Harmonic Scalpel; Ethicon Endo-Surgery, CVG, Cincinnati, OH) from their origin to the bifurcation of the musculophrenic and superior epigastric arteries. In a skeletonized fashion the endothoracic fascia was opened parallel and medial to the internal thoracic vein. The entire length of the ITA was exposed by blunt dissection. The branches were divided by contact with activated blade tip (blunt side) more than 1 mm away from the takeoff or were divided carefully with Hemoclips and scissors to eliminate any damage to the ITA wall if the length of a branch was not enough. The skeletonized ITA was harvested without any surrounding tissue. The pedicled ITA was dissected as the flap of fascia, muscle, and fat tissue containing the ITA and the internal thoracic veins also using an ultrasonic scalpel. The two terminal branches were retained as the runoff and the dissected ITAs were left free in the chest and the wound was closed in a routine manner.

One week or 12 weeks later the dogs were anesthetized and the entire bilateral ITAs were harvested through resternotomy with the heart beating. After the ITA was flushed out with cold saline, a short segment of it was excised at 1 to 2 cm proximal to the bifurcation. The segment was fixed in 4% paraformaldehyde in phosphate-buffered saline (PBS) and embedded in paraffin. Sections 5 µm thick were made, some of which were stained with hematoxylin and eosin (HE) and elastica van Gieson (EVG).

Immunostaining
Sections from each ITA were stained with antibodies against von Willebrand Factor (VWF; Dako, Carpenteria, CA), endothelial nitric oxide synthase (eNOS; Transduction Lab, Cincinnati, OH), inducible nitric oxide synthase (iNOS; Transduction Lab), and proliferating cell nuclear antigen (PCNA; Dako).

The paraffin sections were dewaxed, washed with PBS three times, 5 minutes each, and blocked with normal goat serum. The primary antibody to the corresponding antigen was applied at room temperature for 60 minutes (VWF, PCNA) or at 4°C overnight (eNOS, iNOS), washed with PBS three times, 5 minutes each. The secondary antibody to the corresponding primary antibody conjugated with fluorescein was applied for 60 minutes, washed with PBS three times for 5 minutes each, stained with propidium iodide (Sigma, Milan, Italy) and examined with CLSM (Bio-Rad MRC 600, Waltford, UK).

Observation by CLSM
The fluorescence was examined at an excitation wavelength of 488 nm with a barrier filter at 500 nm. The specimens were viewed with a 40x objective lens and confocal images were obtained with the standard data analysis software of the MRC 600 system. The microvessels positive for VWF in the adventitia were counted in the confocal images. To assess cell proliferation, the proliferative index was used. The proliferative index was determined by PCNA positive cell count/total cell count.

After observation with CLSM, quantitative analyses of the staining signals for VWF and eNOS expressed on the endothelial cells were also performed. Three consecutive images of 1.0-µm thickness in each slide were obtained and filtered to diminish the background noise. The fluorescence images were then projected on the two-dimensional plane and three consecutive optimal images, namely an image with the most intensive fluorescence and two adjacent ones, were merged. On the merged image at least 20 endothelial cells were randomly selected and the fluorescence intensity at the selected area was quantitatively analyzed using the standard imaging analysis software ("histogram" function) of the MRC 600 system. The relative fluorescence intensity was linearly correlated with the number of pixels, ranging from 0 to 255 in this system, showing a positive signal. Thus the relative amounts of VWF and eNOS antigens were represented as the number of pixels of fluorescence on the selected endothelial cells.

Statistical analysis
The quantitative values are expressed as mean ± standard deviation. For statistical comparison between the skeletonized and pedicled ITAs, the Student t test was used with an SPSS software package (SPSS, Chicago, IL). Statistical significance was defined as p less than 0.05.


   Results
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 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
There was a little adhesion in the 1-week ITAs but there were adhesions with the lung and the anterior chest wall at various grades in the 12-week ITAs. All ITAs showed good distal free flow.

Microscopic findings (Figure 1) showed that the wall structure of both skeletonized and pedicled ITAs was almost intact in both acute and chronic phases. There was no significant intimal hyperplasia and no hematoma or dissection in the media. The elastic lamella in the media was not disrupted, the endothelial cells lining the luminal surface were well preserved, and signs of degeneration were not observed in either ITA wall.


Figure 1
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  		Fig 1. Microscopic findings show that the wall structure of both skeletonized and pedicled internal thoracic arteries (ITA) is almost intact. There is no significant intimal hyperplasia, no hematoma or dissection in the media. (Top row, hematoxylin and eosin, x10; middle row, elastica van Gieson, x200; bottom row, hematoxylin and eosin, x400.)

 
Quantitative analyses of immunohistochemistry are shown in Table 1. Both VWF and eNOS expressions were clearly observed in the luminal endothelial cells with CLSM (Figure 2). Regarding the mean numbers of pixels for VWF or eNOS, there were no significant differences between the groups at either study period. The expression of iNOS was not detected in any ITA segments. There were significantly more microvessels positive for VWF in the adventitia of skeletonized ITAs than in the adventitia of pedicled ITAs at both 1 week and 12 weeks after dissection (Figure 3). With regard to the proliferative index of the smooth muscle cells in the media of the ITA, there were no differences between the groups at either phase and any index was as low as in normal vessel wall.


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  		Table 1 Comparison of Quantitative Analyses of Immunohistochemical Findings Between Pedicled and Skeletonized Internal Thoracic Artery 1 Week and 12 Weeks After Harvesting
 

Figure 2
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  		Fig 2. Confocal images show expressions of von Willebrand factor (VWF) and endothelial nitric oxide synthase (eNOS) are clearly observed on the luminal endothelial cells of 12-week internal thoracic arteries (ITAs). (A) Confocal image of staining with VWF in pedicled ITA. (B) Confocal image of staining with VWF in skeletonized ITA. (C) Confocal image of staining with eNOS in pedicled ITA. (D) Confocal image of staining with eNOS in skeletonized ITA.

 

Figure 3
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  		Fig 3. Immunostaining against von Willebrand factor (VWF) shows significantly more microvessels positive for VWF in the adventitia of skeletonized internal thoracic arteries (ITAs) than in that of pedicled ITAs at both 1 week and 12 weeks after dissection. (A) One-week pedicled ITA. (B) Twelve-week pedicled ITA. (C) One-week skeletonized ITA. (D) Twelve-week skeletonized ITA.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The advantages of the skeletonized ITA over the pedicled ITA are increased available graft length, greater blood flow in the early postoperative period, and less invasion of the chest wall. Therefore the skeletonization technique in ITA harvesting has been widely used to accomplish total arterial myocardial revascularization and it is considered acceptable in clinical practice [1–4]. Nonetheless dissection of the ITA with the skeletonization technique may induce mechanical and physical damage to the vessel wall, loss of the vasa vasorum, which may cause ischemia in the outer layer of the media, and loss of the draining vein, which may induce stasis and edema in the vessel wall. These phenomena may result in detrimental effects on the functional integrity of the ITA.

Noera and colleagues [5] showed blood effusion in the adventitia of the skeletonized ITA. Gaudino and coworkers [6] showed intraluminal microthrombus formation and preservation of the endothelium in the skeletonized ITA by immunohistochemical staining with antifactor VIII/VWF antibody. Deja and associates [7] demonstrated that skeletonization did not damage endothelial function in their dose-effect relationship study on relaxation induced by acetylcholine. These studies were on ITAs harvested intraoperatively, however, namely the ITAs immediately after skeletonization, and chronologic changes after skeletonization were not investigated. In the single study on ITAs in the chronic phase after dissection Sasajima and coauthors [8] showed that skeletonization was not detrimental to structural integrity in the canine model; the results of their study were based on histologic analyses, however, instead of functional analyses.

In our study to evaluate the effects of skeletonization on the functional integrity of the ITA, immunohistochemical techniques were used to compare skeletonized with pedicled ITAs of dogs in acute and chronic phases after dissection. The targets of the immunohistochemical staining were VWF, eNOS, iNOS, and PCNA. VWF is a specific marker of the endothelial cells and its overexpression indicates thrombogenesis [9, 10]. VWF staining was used not only to evaluate the luminal endothelial cells but also to count the number of microvessels in the adventitia. eNOS is a marker of the functional integrity of endothelial cells [11, 12] and iNOS is a marker associated with inflammatory or ischemic response in the vessel wall [13]. PCNA is used to assess proliferation of the smooth muscle cells in the media that reflects the remodeling after ischemia or inflammation in the vessel wall [14–16]. Confocal laser scanning microscopy has successfully been used as quantitative immunofluorescence microscopy [17]. We applied this tool to quantitate staining of VWF and eNOS in the luminal endothelial cells.

In this study model we considered that physical damage by surgical manipulation could be avoided by using an ultrasonic scalpel [18] carefully but the loss of the surrounding tissue including the vasa vasorum affected the vessel wall. A previous study showed that revascularization of the adventitial vasa vasorum could begin within 1 week after dissection [19]. Postoperative angiography several months after coronary artery bypass grafting (CABG) showed many new small branches from the ITAs that had been harvested by the skeletonization technique [20]. In our study there were significantly more microvessels positive for VWF in the adventitia of skeletonized ITAs than in that of pedicled ITAs at both 1 week and 12 weeks after dissection. The expression of iNOS was not detected in any ITA specimens, however, and proliferation of the smooth muscle cells in the media was minimal, as in normal vessels. These results suggested that the loss of the vasa vasorum did not induce ischemia or remodeling in the media and neovascularization in the adventitia was just a change secondary to adhesion that did not induce proliferation of the smooth muscle cells in the media after intimal hyperplasia shown in the atherosclerogenesis process [16, 21].

Quantitave analyses with immunohistochemical staining of VWF and eNOS showed that the structural and functional integrity of the endothelial cells in skeletonized ITAs was similar to that of pedicled ITAs at both study periods. Therefore although neovascularization of the vasa vasorum could occur after dissection, skeletonization did not induce ischemia or inflammation of the media and the structural and functional integrity of the endothelial cells was maintained.

A few limitations in the present study need to be considered. First, the ITA was left in situ without an anastomosis to the coronary artery and the adventitia of skeletonized ITA was in direct contact with the parietal pleura compared with the adventitia of pedicled ITA that was not in direct contact with the pleura. This condition might cause an increased neovascularization in the adventitia of a skeletonized graft. In relation to the possibility that our model may not reflect the situation found in our clinical practice after CABG we have experienced some redo CABGs in which the skeletonized ITA graft adhered tightly to the parietal pleura for almost the full length of the graft and could not be identified. We think therefore that our model may be similar to the clinical situation but not the same. Second, the number of animals in our study was small. Although a large number of specimens of each ITA was strictly investigated, we found no difference between skeletonized and pedicled ITAs. We think that these largely reproducible results provided by investigation into many specimens of each ITA may be accepted although we cannot rule out that these findings might result by chance.

In conclusion, skeletonization did not have detrimental effects on the structural and functional integrity of ITAs in either acute or chronic phases excluding physical damage caused by surgical manipulation. These findings justify the use of skeletonized ITAs for myocardial revascularization.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  6. Gaudino M, Toesca A, Nori SL, Glieca F, Possati G. Effect of skeletonization of the internal thoracic artery on vessel wall integrity Ann Thorac Surg 1999;68:1623-1627.[Abstract/Free Full Text]
  7. Deja MA, Wos S, Golba KS, et al. Intraoperative and laboratory evaluation of skeletonized versus pedicled internal thoracic artery Ann Thorac Surg 1999;68:2164-2168.[Abstract/Free Full Text]
  8. Sasajima T, Wu MH, Shi Q, Hayashida N, Sauvage LR. Effect of skeletonizing dissection on the internal thoracic artery Ann Thorac Surg 1998;65:1009-1013.[Abstract/Free Full Text]
  9. Smith JM, Meinkoth JH, Hochstatter T, Meyers KM. Differential distribution of von Willebrand factor in canine vascular endothelium Am J Vet Res 1996;57:750-755.[Medline]
  10. Brinkhous KM, Reddick RL, Read MS, Nichols TC, Bellinger DA, Griggs TR. Von Willebrand factor and animal models. contributions to gene therapy, thrombotic thrombocytopenic purpura, and coronary artery thrombosis. Mayo Clin Proc 1991;66:733-742.[Medline]
  11. Oemar BS, Tschudi MR, Gody N, Brovkovich V, Malinski T, Luscher TF. Reduced endothelial nitric oxide synthase expression and production in human atherosclerosis Circulation 1998;97:2494-2498.[Abstract/Free Full Text]
  12. Butty LDK, Chester AH, Springall DR, et al. Explanted vein grafts with an intact endothelium demonstrate reduced focal expression of endothelial nitric oxide synthase specific to atherosclerotic sites J Pathol 1996;179:197-203.[Medline]
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