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Eur J Cardiothorac Surg 2002;22:898-903
© 2002 Elsevier Science NL

A new outside stent – does it prevent vein graft intimal proliferation?

Michal Krejcaa*, Janusz Skarysza, Przemyslaw Szmagalaa, Danuta Plewkab, Grazyna Nowaczykb, Andrzej Plewkab, Andrzej Bocheneka

a 1st Cardiac Surgery Department, Silesian University of Medicine, SPSK nr 7, 40-635 Katowice, ul. Ziolowa 45-47, Poland
b Department of Histology and Embryology, Silesian University of Medicine, 40-752 Katowice, ul. Medykow 18-20, Poland

Received 28 June 2002; received in revised form 5 September 2002; accepted 6 September 2002.

* Corresponding author. Tel.: +48-32-202-40-25, ext. 1640; fax: +48-32-252-70-66
e-mail: mkrejca{at}wp.pl


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 
Objective: The saphenous vein subjected to arterial pressure stretches to its elastic limits and constitutes intimal hyperplasia. Sheathing of the vein graft with pressure-resistant tubing might prolong vein graft patency. Methods: Twenty-one sheep received radial vein grafts or hybrid grafts composed of radial vein, collagen fibrin glue and highly flexible torlen/dacron mesh tubing transplanted into the carotid artery position. Veins were examined with the use of light and electron microscopy. Proliferating cell antigen (Ki-67) stains served as markers of proliferation. Results: The mean wall thickness of both intimal and medial layers was evaluated. The mean intimal wall thickness was 19±11 µm in hybrid grafts vs. 24±7 µm in unsheathed grafts (P<0.001); 22±6 vs. 26±10 µm (P<0.001); 23±8 vs. 52±15 µm (P<0.001); 37±21 vs. 90±31 µm (P<0.001); 57±31 vs. 104±28 µm (P<0.001); 58±21 vs. 133±32 µm (P<0.001); and 72±22 vs. 244±100 µm (P<0.001) after respectively 5 days, 9 days, 4 weeks, 6 weeks, 8 weeks, 10 weeks and 12 weeks from implantation. Electronic microscope examination of hybrid grafts revealed a smooth endothelial layer with intact nuclei and an intima composed of layers of collagen and muscle fibers. In unsheathed grafts endothelial edema and nuclear destruction were observed. Conclusions: The external vein graft support with mesh tubing reduces intimal and medial layer thickening and cell proliferation in composite vein grafts transplanted in the arterial position.

Key Words: Coronary heart disease • Coronary vein graft • Hybrid graft • Remodeling • Atherosclerosis


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 References
 
Since the beginning of the nineties the tendency towards surgical treatment of coronary artery disease (CAD), by means of coronary artery bypass grafting (CABG) with the use of artery grafts, has become truly significant. The use of radial and gastroepiploic arteries is becoming more and more popular, while internal thoracic artery (ITA) graft to LAD is a universally accepted standard [1]. However, despite proven longer patency of the arterial grafts, those made out of the autogenous saphenous vein are most commonly used [2].

The occlusion of the venous grafts is a result of the slow process of atherosclerosis acting over the years and progressive thickening of the intima and media acting over the first months [3].

The venous graft transplanted into the arterial system adapts to a higher pressure acting on it by thickening of its wall [4]. The external elastic membrane of arterial vessels probably allows them to withstand much higher pressures. The changes in each element of the graft wall may affect its permeability and accelerate formation of the atherosclerotic lesion [5,6]. The remodeling of a venous graft is modulated by factors similar to those affecting the vascular system, such as atherosclerosis, hypertension, and mechanical trauma following the angioplasty.

According to the Laplace law, the pressure under the spherical surface (single mesh in tubing net) with radius r is described by the following formula:

and the pressure under the cylinder surface (vein without mesh tubing) with radius R is described by the following formula:

where {gamma}={sigma}xd, {sigma} is the stress inside the wall, and d is the wall thickness.

When considering the model of a vein without mesh tubing one can assume that the relation between the pressure inside the vein and stress in its wall is linear. In the model of the vein with mesh tubing, with increasing pressure inside the vein, the vein walls in the mesh form a spherical surface. Its radius decreases with increasing pressure and reaches a minimal value which is equal to the mesh radius.

As a result of that, the stress in the vein wall is increasing slower than linear compared to the increase in the pressure. At identical pressure inside the vein with and without the mesh tubing and assuming that the mesh radius is equal to 1/10 of the vein radius, the stress exerted in the mesh-protected vein wall could be even 20 times lower than the stress in the non-protected vein wall.

The goal of this research was to evaluate the efficacy of the extravascular stent, made of a dacron mesh that we developed, in prevention of venous grafts degeneration. The dacron mesh placed around the graft should serve as a support to its wall making it more resistant to high pressure, decrease tangential stress and retard graft degeneration processes.


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 References
 
The research was performed in 2000 and 2001 at the Central Animal Laboratory of the Silesian University of Medicine, Katowice, Poland. The approval of the Local Ethical Committee on Animal Research was obtained. Animals received human care in compliance with the European Convention on Animal Care.

Twenty-one male sheep of the same breed at ages between 8 and 10 months and weighing 35–40 kg were used. Genetically, the animals were very close.

In collaboration with Tricomed S.A. Lodz, Poland – a company that has years of experience in vascular prostheses production – we constructed a 4 mm in diameter mesh made out of polyester fiber (torlen/dacron) (see Fig. 1) . This stent consists of empty rhomboidal spaces created by single interlacing torlen threads and plays a role of external support of the native vein. This extravascular stent (patent pending) is very resistant to bending and has an ability to change its diameter depending on forces acting along its long axis. The mesh constructed for further human use is 6 mm in diameter and easily changes its diameter from 10 to 2 mm.



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  		Fig. 1. The polyester mesh used to prepare a hybrid graft (THG, trico hybrid graft).

 
2.1. Surgical technique
After premedication (Atropin 1 mg/20 kg body weight s.c., Xylazine 2% 0.8 ml i.m.), animals were given intravenous anesthesia (Pentobarbital/Vetbutal 0.25 ml/kg b.w. i.v., Biovetalgin/Metamizol 5–10 ml i.v.). The animals were then ventilated (FiO2 of 0.21–0.30) and a gastric tube was introduced to prevent flatulence.

Heparin was administered i.v. (5000 units) and the radial vein was harvested. All side branches were obliterated with the 4-0 silk ligature. The vein with a diameter of 3–4 mm formed the biological component of the hybrid graft. It was then wrapped with the mesh and glued to it with the use of the tissue fibrin glue Beriplast (Centeon, Mannheim, Germany).

The coronary forceps were introduced inside the mesh while the mesh was gently pushed to minimize its long diameter. The 10–12 cm coronary forceps can be fully introduced inside 25 cm long mesh. The distal part of the vein was then grasped by the forceps and the mesh was pulled on the vein. The mesh was ligated to the needle placed in the proximal part of the vein. The distal part of the vein was clamped together with surrounding mesh and the vein was filled gently with saline. With this simple maneuver the mesh nearly automatically closely covers the vein. The composite graft was dried with the sponge, and finally the fibrin part of the glue and then thrombin was applied. The construction of hybrid graft together with glue application lasts about 3–4 min. The total length of the hybrid graft was about 10 cm. The remaining portion of the vein was later implanted as a classical graft.

A 10–15 cm long fragment of a jugular artery was bypassed with the hybrid graft and then cut and ligated for blood to flow exclusively through the graft. The end to side anastomoses were completed with the use of Prolene 7-0 (Ethicon, Somerville, USA). The same was done on the opposite side of the neck, where just an autologous vein graft covered only with tissue glue (without the polyester mesh) was used. Animals were extubated on the operating table and allowed to recover.

2.2. Histology and immunohistochemistry
Samples of tissues were examined after 5 days, 9 days and 4, 6, 8, 10, and 12 weeks, each time from three animals. After premedication animals were anesthetized with Pentobarbital/Morbital 20–30 ml i.v. Samples of vessels were divided into proximal, medial and distal parts and at least three samples from each part were obtained for particular examination. The material to be examined using an optical microscope was flushed with 0.9% NaCl and preserved for 20 h in 4% formaldehyde with phosphate buffer. The sections for histology and immunocytochemistry were dehydrated and embedded in paraffin. Sections for histology were stained with eosin, hematoxylin and van Gieson to make the elastic fibers visible.

Portions of vessels to be examined under electron microscopy were fixed in 2.5% glutaraldehyde with cacodyl buffer, and osmium tetroxide, dehydrated and then embedded in Epon fixative. Once obtained, they were contrasted with uranyl acetate and lead nitrate for evaluation in a transmission electron microscope.

The pictures obtained from the optical microscope were scanned which allowed computer image analysis and measurements of media and intima of the venous graft (group I – radial vein RA) and of the hybrid graft (group II – trico hybrid graft, THG). The database consists of many hundreds of measurements at each time point to eliminate as much as possible the potential influence of variability of histological changes along the length of the grafts on final study results. Intima was measured from the subendothelial basal lamina to the internal elastic lamina, from where media extends to the adventitial layer.

Proliferation of the medial and intimal cells was assessed with the use of immunohistochemical reaction with the Ki-67 monoclonal antigen [7,8]. The specimens were fixed overnight in 10% neutral-buffered formalin (phosphate buffer). The samples were subsequently passed through graded alcohol solutions, processed three times in xylene and finally embedded in paraffin blocks. Slices of 5 µm thickness were placed on Apes-coated slides, deparaffinized and rehydrated. To unmask the antigen, sections were boiled in 0.01 M citrate buffer (pH 6.0) in a microwave oven for 10 min at 800 W. For quenching of endogenous peroxidase activity, tissue sections were blocked with normal rabbit serum for 10 min and incubated with primary antibodies for 60 min at 25 °C (Ki-67 Antigen Kit, Novocastra, Newcastle upon Tyne, UK). Next, biotinylated secondary antibodies and ABC reagent were added (30 min, 25 °C each). DAB and H2O2 were used as peroxidase substrates. Finally, tissues were stained with hematoxylin, dehydrated and coverslipped.

Under a 250x magnification field an assessment of a percentage of stained, proliferating cells' nuclei was performed. Usually approximately 100 nuclei were found in one field of vision. Counting was terminated once a number of 1000 was reached or when all cells in a particular section were evaluated.

2.3. Statistical analysis
Normal distribution was confirmed in both groups using the Kolmogorov–Smirnov test. For any further analysis, Student's t-test or the Mann–Whitney U-test were used. Differences were considered significant when the P value was less than 0.05. Results are presented as the mean±standard deviation.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 References
 
Thickening of the graft wall noted in both examined groups was largely due to the overgrowth of the intimal layer (neointima). The mean difference in the total wall thickness between the groups was only 10%. However, the neointima of the venous grafts was a few times thicker, compared to the hybrid grafts, and this discrepancy increased over time (Fig. 2) .



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  		Fig. 2. Changes of the thickness (in micrometers) of the intima (A), media (B) and intima and media (C) over time in both examined groups. Group I, RA (radial vein); group II, THG (trico hybrid graft).

 
The continuous degenerative changes in the venous graft wall seen in the optical microscope were significantly more pronounced in group I (venous graft). Flattened endothelial cells, with focal loss of continuity, proliferation of fibroblasts and myofibroblasts, increasing density of collagen fibers and spots of hyalinization in media and intima were noted in samples collected from this group. In addition an irregularity of collagen fibers in the surrounding tissues was observed. Vasa vasorum were singular and visible.

In group II endothelial cells with intact continuity and proliferation of collagen fibers on the boundary of media and adventitia were found. The vasa vasorum were numerous, some with thickened walls. Focally, infiltration with inflammatory cells could be noted in the proximity of the stent fibers (see Fig. 3) .



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  		Fig. 3. Cross-section of (A) the radial vein with no stent (group I) and (B) the radial vein with a stent (group II) assessed after 12 weeks from grafting. Optical microscope, magnification 150x. Eosin, hematoxylin, van Gieson's staining. INT, intima between the arrows; MED, media between the circles; ADV, adventitia.

 
For the purpose of this study the grading system of vascular changes shown in Table 1 has been applied. Table 2 shows the changes in histological grading over time (note that only the time periods with significant differences are shown).


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  		Table 1. Histological grading system of vascular changes

 

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  		Table 2. Changes in histological grading over time (note that only the time periods with significant differences are shown)

 
The electron microscope examination of the sample slices obtained from group I revealed a degradation of the smooth muscle cells, often attributable to apoptosis. The cells were shrunk and nuclei presented with numerous invaginations or were occasionally fragmented. Often the endothelium was covering the interrupted intimal layer. In group II endothelial cells with a smoothened cell membrane with a well preserved structure of the nucleus were observed. Intima was made of singular layers of dense collagen fibers.

The ratio of proliferating cells was assessed in the aforementioned time points with the use of immunocytochemical reaction of monoclonal Ki-67 antibody with nuclear antigen. The proliferation ratio after 4 weeks from surgery was similar in both groups and equaled about 8%. However, after 6 and 8 weeks the appropriate values were 7% and 7.5% (group I) vs. 5% and 5.5% (group II). In group I the number of proliferating cells continues to decrease after 10 through 12 weeks (6.5% and 5.5%) while in group II the process is already nearly terminated (1.5%) (Fig. 4) .



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  		Fig. 4. Changes in the number of proliferating cells in both examined groups over time. Group I, RA (radial vein); group II, THG (trico hybrid graft).

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
References
 
A graft patency depends on its biological characteristics, i.e. anatomy, size and physiological properties of the vessel used for grafting [9]. Typical atherosclerotic lesions are extremely rarely encountered in human veins, though they develop quickly once a vein is transplanted into the arterial system [10]. Remodeling is a homeostatic response of the normal arteries to the changes of the blood flow characteristics and stretching of their walls. This allows for shear stress and wall tension to be brought back to normal levels.

Increased wall tension and endothelial disruption permits blood cellular elements to penetrate the vessel wall, a process that induces intensive proliferation. Injured endothelium is unable to produce and secrete adequate amounts of the antiplatelet, vasodilatating and antimitotic factors. As a consequence, growth factors, tromboxan, angiotensin and endothelin are released [11]. Such an abnormal wall remodeling is characterized by migration and proliferation of smooth muscle cells from intima to media and formation of neointima [12]. The pathological mechanisms described have certain distinct features, being associated with a specific vein physiology and histological structure.

Unlike in the saphenous vein, the synthesis of nitric oxide (NO) by the ITA endothelium is stimulated by platelet-derived products, such as ADP and ATP. ITA endothelium has an ability to promote vasodilation, exert antiplatelet effects and help to break forming platelet cloths, features that saphenous vein endothelium does not have. Hormones like bradykinin, histamine, and substance P stimulate NO production to a much greater degree in ITA then in saphenous vein [13]. Also prostacycline (PGI2) is secreted in much lesser quantities in saphenous vein than in ITA [14].

With time venous grafts become more reactive to the vasorelaxing effects of acetylcholine, ADP and thrombin, but never to the same extent as arterial grafts [15].

Several research groups tried to modify venous grafts with external stents in order to make them more pressure-resistant [6,16–20]. In cooperation with Tricomed S.A. (Lodz, Poland), we were able to create a mesh stent which is highly resistant to forced bending. Several of its advantages need to be pointed out, i.e. preparing the hybrid graft in the conditions of the operating room is simple, attaching an external surface of the vein with the use of fibrin glue is easy, and the torlen/dacron net remains adherent to the vein after it is trimmed with scissors before performing an anastomosis.

Most of the hybrid grafts described in the literature were unique and hand-made from vascular prostheses of a different degree of porousness [6,16,19]. In 1996 Zurbrugg et al. [17] described the use of an external stent, made of steel mesh, and reported its protective effects on intima and media. In our study we showed that overgrowth of both intima and media in a vein wrapped with a stent is retarded, and that the effect is especially pronounced in intima. We observed the media overgrowth due to infiltration with acute inflammatory cells and transformation of medial myocytes into fibrocytes in both groups, however the difference is pronounced strongly after 12 weeks.

The data presented here seem to confirm that the use of an extravascular mesh stent significantly decreases overgrowth of the intima that is observed after 4 weeks by the other methods. The present study shows that the effect is already evident in the early period of observation (5–9 days; 19–22 vs. 24–26 µm), intensifies with time (8–10 weeks; 57–58 vs. 107–133 µm), and the difference exceeds nearly three times the initial level after 3 months from grafting (72 vs. 245 µm).

Most probably the formation of the neointima plays the key role in a total change in intima and media thickness. Changes occurring over time in a venous graft wall are simply a reflection of the underlying proliferative processes. The endothelial damage caused by surgical trauma, thrombosis and elevated transmural pressure leads to intimal fibrous proliferation. We can speculate that the mesh use should decrease the transmural pressure. The histological changes related to increased transmural pressure are probably becoming more and more evident within weeks from grafting. The early changes are mostly due to endothelial damage caused by surgical trauma.

Angellini et al. [20] noted a significantly lower ratio of proliferating cells in a wall of a vein supported with an extravascular stent. Rodriguez et al. [21] described proliferation of non-smooth muscle cells (NSMC) in the early period following grafting. Both authors used the PC-10 antigen (anti-proliferating cell nuclear antigen: PCNA). PCNA is a nuclear antigen, present at low, but detectable concentrations in nonproliferating cells. Therefore, it makes a useful tool for qualitative assessment, although its ability to determine changes that occur later over time is limited. Antigen reacting with Ki-67 antibody undergoes a very fast catabolism at the end of phase M of cell proliferation [7,8]. This helps to determine changes in proliferative processes with greater accuracy. The differences become significant as early as after 6 weeks: the proliferation rate in stent-free veins (group I) decreases slightly at that time, while it is nearly abolished within hybrid grafts (group II). A lower proliferation rate on day 5 in group II can be explained by a delayed triggering of mechanisms that stimulate that process. At those very early stages it is mostly due to mechanical trauma to the endothelium. It is worth remembering though, that the hybrid graft was constructed from the same portion of the vein as was the standard graft, not to mention that it underwent manipulations aiming at placing the vein inside the dacron net and gluing with elevated intravenous pressure that could further damage the endothelium. Stooker et al. [22] showed, in an in vitro model, the protective effect of the extravascular stent on the endothelium in human saphenous vein perfused for 1 h with blood. We can therefore assume that early endothelium reparative processes (re-endothelialization) occur at faster rates in veins reinforced with extravascular stents, and that the degenerative processes causing higher permeability of the vein are activated later. The fibrin glue, commonly used for hybrid graft construction, probably has no influence on the vein wall structure and function [23]. The fibrin sealant allowed a vein wall and a mesh to adhere and avoid formation of inner lumen foldings [17].

The presence of a stent made a vein lumen remain widely open even in an empty state and suturing an anastomosis incorporating dacron fibers was easy. Fibrin sealant exerts some positive influences on wound healing: it promotes granulation, early fibroblast proliferation, accelerated re-epithelization and revascularization as well as inhibiting leukocyte infiltration [24]. Because of its biocompatibility the fibrin glue has also been advocated as a substrate for endothelial cell seeding in vascular prostheses [25].

The extravascular dacron mesh stent wrapped around a vein that is to be implanted into the arterial system prevents the hypertrophy of the graft's wall, impedes the overgrowth of the intima and decreases the proliferation rate of venous graft cellular elements.


   Acknowledgments
 
The project was supported by a grant from Silesian University of Medicine, Katowice, Poland.


   Footnotes
 
Presented at CTT 2002: Current Trends in Thoracic Surgery VIII, Fort Lauderdale, FL, USA, January 23–26, 2002 and the 20th International Cardiovascular Surgical Symposium, Zurs, Austria, March 2–9, 2002.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 

  1. Lytle B.W., Loop F.D., Cosgrove D.M., Ratliff N.B., Easley K., Taylor P.C. Long term (5–12 years) serial studies of internal mammary artery and saphenous vein coronary bypass grafts. J Thorac Cardiovasc Surg 1985;89:248-258.[Abstract]
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