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DOI:10.2214/AJR.05.0683
AJR 2006; 186:1148-1154
© American Roentgen Ray Society

Technical Innovation

Technical Feasibility and Biocompatibility of a Newly Designed Separating Stent-Graft in the Normal Canine Aorta

Young-Cheol Weon1, Sung-Gwon Kang2, Jin Wook Chung3, Young Il Kim3, Jae Hyung Park3 and Do Yun Lee4

1 Department of Radiology, Samsung Medical Center, Sungkyunkwan University College of Medicine, Seoul, Korea.
2 Department of Interventional Radiology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 300 Gumidong, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, Korea.
3 Department of Diagnostic Radiology, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Korea.
4 Department of Diagnostic Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea.

Received April 21, 2005; accepted after revision July 15, 2005.

 
Address correspondence to S.-G. Kang.


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
OBJECTIVE. The objectives of this study were to assess the performance of a newly designed separating stent-graft system with respect to the technical feasibility of transfemoral deployment, the maintenance of vessel patency, and stent deformity due to mechanical defects; and to evaluate its in vivo healing characteristics, including thrombus formation, and endothelial covering of the stent-graft when placed in the normal aorta of a canine model.

CONCLUSION. The newly designed separating stent-graft allowed accurate deployment without migration. This animal study also provided an opportunity to examine the healing process associated with an ultrathin polyester fabric nitinol stent and showed predictable healing characteristics in the normal thoracic aorta in this canine model.

Keywords: animal studies • aorta • endothelialization • nitinol stent • stent-graft


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Thoracic aorta aneurysms and dissections are life-threatening conditions and pose a significant treatment challenge. The incidence of thoracic aortic aneurysms is approximately 6 per 100,000 persons per year [1]. For thoracic aortic aneurysms, surgical repair using a prosthetic graft is the traditional therapy with operative mortalities of 5-20% [2]. This procedure is also associated with substantial morbidity, such as postoperative paraplegia, renal failure, and the need for prolonged ventilator support [2, 3]. Aortic dissection is also one of the most common nontraumatic aortic pathologic conditions, with an annual incidence of 10-20 cases per 1 million people per year, which exceeds the incidence of spontaneous aortic aneurysm rupture [4]. Acute aortic dissection or aneurysm may be treated conservatively, but emergency surgery is often necessary if the risk of rupture is high and organ ischemia is marked. As alternative surgical treatments for aneurysms and dissections of the thoracic aorta, various endovascular techniques and many types of endovascular stents and grafts have been developed over more than 10 years [4-12].

Most of the current endovascular stent-grafts have been developed to treat thoracic aneurysm and dissection; however, their uses are restricted to a range of suitable anatomy and they may lead to long-term failure or may need to be placed with a large guidance delivery sheath, a process that necessitates surgical cutdown of the femoral artery [11-15]. For these reasons, we designed a separating stent-graft system consisting of two separate stents—one ultrathin polyester fabric stent-graft and a bare stent—with the aims to provide a less invasive and more versatile technique, reduce complications, and provide a possible percutaneous approach by reducing the introducer profile in cases involving the smaller iliofemoral artery or the tortuous iliac artery [16]. The reduced profile of the developed device allows introduction of the stent through a 10-French introducing system with a 12-French femoral sheath, and its special design minimizes stent-graft movement during deployment.

The objectives of this study were to assess the performance of a newly designed separating ultrathin polyester fabric stent-graft system with respect to the technical feasibility of transfemoral deployment, the maintenance of vessel patency, and stent deformity due to mechanical defects; and to evaluate its in vivo healing characteristics, including thrombus formation, and endothelial stent-graft coverage when placed in the normal aorta of a canine model.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Animals
In compliance with the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health [17], nine adult mongrel male dogs (weight, 20-30 kg; mean weight, 25 kg) were housed and maintained in facilities approved by the American Association for the Accreditation of Laboratory Animal Care. Animals were fed a normal laboratory diet. Arterial access was obtained by cutdown of the right femoral artery with the animal under general anesthesia (sodium pentobarbital, 30 mg/kg). After the procedure, animals continued to be fed a normal diet. The dogs were sacrificed by exsanguination under deep sodium pentobarbital anesthesia after a follow-up of 4 (group 1, n = 2), 6 (group 2, n = 2), 8 (group 3, n = 2), or 12 (group 4, n = 3) weeks.

Construction of the Separating Stent-Graft
The separating stent-graft systems were handmade in our research laboratory (S & G Biotech Inc.) and consisted of two parts: an outer graft-stent and an inner bare stent (Figs. 1A, 1B, and 1C). The outer stent, named the graft-stent, consisted of three parts: a proximal stent, a graft made of synthetic ultrathin polyester textile fabric (UTD, MiKwang), and a distal stent. The synthetic polyester graft was attached to two stents with the same structure. The thickness of the polyester graft used in this study was less than 100 µm.


Figure 1
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  		Fig. 1A —Components of separating stent-graft (34 mm x 10 cm). Outer graft-stent consists of three parts: proximal stent (A), graft made of synthetic ultrathin polyester textile fabric (B), and distal stent (C).

 

Figure 2
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  		Fig. 1B —Components of separating stent-graft (34 mm x 10 cm). Outer graft-stent consists of three parts: proximal stent (A), graft made of synthetic ultrathin polyester textile fabric (B), and distal stent (C).

 

Figure 3
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  		Fig. 1C —Components of separating stent-graft (34 mm x 10 cm). Outer graft-stent consists of three parts: proximal stent (A), graft made of synthetic ultrathin polyester textile fabric (B), and distal stent (C).

 
The proximal and distal stents were knitted and wound from a single thread of 0.245-mm nitinol wire in a tubular configuration without an inter-locking diamond-shaped pattern. There are connecting bars between the two stents to resist compressive folding during extrusion from the sheath. These bars also help stabilize the stent-graft during reinstrumentation. Six 0.5-cm-long barbs were attached to the proximal stent by winding the stent body. The proximal and distal stents were 20 mm in diameter and 14 mm long.

The three parts of the stent-grafts were tied with blue monofilament (4-0 Prolene, Ailee) using a tapered needle. The two stents were each separated by 0.5 cm from the segment covered with synthetic polyester. This gap allows antegrade aortic flow to be maintained during stent-graft deployment, and the graft fabric never makes the temporary "windsock" effect. The synthetic polyester was 20 mm in diameter and 5 cm long. Gold radiopaque markers were attached at both ends of the proximal, distal, and inner bare stents to enhance stent-graft visibility on fluoroscopy. The inner bare stent was made from a single 0.245-mm nitinol wire in a tubular, noninter-locking configuration; it also had a gold marker on its proximal and distal ends. This stent was 22 mm in diameter and 70 mm long. The inner bare stent was specially designed to improve its conformability.

Deployment Technique
The separating stent-grafts were introduced through a 10-French sheath (S & G Biotech Inc.). The introducing system consisted of four parts: a 10-French outer sheath made of braided tube (S & G Biotech Inc.), a coil pusher (outer diameter, 2.22 mm; inner diameter, 1.5 mm), and a 4-French catheter as a guidewire-passing tube [16] (Fig. 2). The separating stent-grafts, outer graft-stents, and inner bare stents were loaded into the 10-French introducing system. After deployment, the outer graft-stent was centrally supported by a coaxial inner bare stent.


Figure 4
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  		Fig. 2 —Diagrams show components of separating stent-graft introducing system: 10-French synthetic resin sheath (A), synthetic resin pusher (B), coil pusher (C), guidewire-passing tube (D), olive tip (E), loader for inner bare stent (F), loader pusher (G), and pusher for inner bare stent (H). (Reprinted with permission from Kang et al. [16])

 

After the induction of general anesthesia (sodium pentobarbital, 30 mg/kg), a 12-French short vascular sheath was inserted through the right femoral artery with cutdown. A pigtail-shaped angiographic catheter (Cook) was then advanced to the descending aorta, and an aortogram was obtained. A stiff guidewire was then advanced through the angiographic catheter to the ascending aorta, and the angiographic catheter was removed. After systemic heparin (100 U/kg) was administered, the introductory system was advanced over the guidewire under fluoroscopic monitoring into the proximal descending thoracic aorta, just distal to the origin of the left subclavian artery. The graft-stent was then deployed at the proximal descending thoracic aorta.


Figure 5
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  		Fig. 3A —Case from 12-week follow-up. Three angiograms obtained before (A), just after (B), and 12 weeks after stent-graft placement (C) in dog in 12-week follow-up group. Stent is intact without any deformity or migration in follow-up angiogram. Transparent neointima covers all stent-grafts. This neointima was very thin (< 1 mm) and regular on gross (D) and microscopic (E) examination.

 


Figure 6
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  		Fig. 3B —Case from 12-week follow-up. Three angiograms obtained before (A), just after (B), and 12 weeks after stent-graft placement (C) in dog in 12-week follow-up group. Stent is intact without any deformity or migration in follow-up angiogram. Transparent neointima covers all stent-grafts. This neointima was very thin (< 1 mm) and regular on gross (D) and microscopic (E) examination.

 


Figure 7
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  		Fig. 3C —Case from 12-week follow-up. Three angiograms obtained before (A), just after (B), and 12 weeks after stent-graft placement (C) in dog in 12-week follow-up group. Stent is intact without any deformity or migration in follow-up angiogram. Transparent neointima covers all stent-grafts. This neointima was very thin (< 1 mm) and regular on gross (D) and microscopic (E) examination.

 


Figure 8
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  		Fig. 3D —Case from 12-week follow-up. Three angiograms obtained before (A), just after (B), and 12 weeks after stent-graft placement (C) in dog in 12-week follow-up group. Stent is intact without any deformity or migration in follow-up angiogram. Transparent neointima covers all stent-grafts. This neointima was very thin (< 1 mm) and regular on gross (D) and microscopic (E) examination.

 


Figure 9
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  		Fig. 3E —Case from 12-week follow-up. Three angiograms obtained before (A), just after (B), and 12 weeks after stent-graft placement (C) in dog in 12-week follow-up group. Stent is intact without any deformity or migration in follow-up angiogram. Transparent neointima covers all stent-grafts. This neointima was very thin (< 1 mm) and regular on gross (D) and microscopic (E) examination.

 
After graft-stent deployment, all of the introductory system—including the outer sheath, coil pusher, and guidewire-passing tube—was removed, but the guidewire remained in the aorta. A second introductory system containing the inner bare stent was then advanced over the guidewire, and the inner bare stent was deployed inside the outer graft-stent so that the two stents in the graft-stent and inner bare stent overlapped about 1 cm. The stent-graft was 1.2-1.4 times oversized compared with the thoracic aorta.

Angiography was performed immediately after stent placement to evaluate the position and patency of the stent-graft. A helical CT scan and an angiogram were obtained at the end of each follow-up period. No anticoagulant or antiplatelet agent was administered after stent-graft placement. Blood sampling for CBC and erythrocyte sedimentation rate (ESR) was performed once per week.

Assessment of Stent Thrombosis and Neointimal Formation
A complete necropsy was performed in each case, involving gross examinations of the stomach, intestine, liver, spleen, and kidneys. After the vessels containing the grafts had been removed, thrombus and endothelial formation were evaluated using a digital camera attached to a stereoscope. Endothelial formation was quantified by electron microscopy, and neointimal thickness and inflammatory cell infiltration were determined.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
The transfemoral deployment of a separating stent-graft was successful in all nine dogs. The visibility of the separating stent-graft was excellent because of the gold markers attached to both ends of the stents. The 10-French introducing system was advanced easily to the thoracic aorta, and the mean time required to place the separating stent-graft (defined as the time from aortography before placement to the time of aortography immediately after placement) was 20 min.

Except two animals in the 8- and 12-week groups that showed a slightly elevated WBC count, all had a normal WBC count during follow-up. RBC and hemoglobin and hematocrit counts were in the normal range. Platelet counts were slightly decreased in all groups without any internal hemorrhage or other associated complications. One dog in the 12-week group showed an increased ESR at the 2-week follow-up, and the value subsequently normalized.

Angiograms were obtained before and just after stent-graft deployment and at follow-up examinations at 4 (n = 2), 6 (n = 2), 8 (n = 2), or 12 (n = 3) weeks after stent-graft placement. Neither migration nor deformity of stent-grafts was observed during deployment or the 12-week follow-up period. All stent-grafts were patent when angiograms were obtained immediately before the animals were sacrificed.

Gross investigations performed to obtain evidence of ischemic change or infarction of intestine or solid organs, including the liver, spleen, kidney, and stomach, unearthed no abnormality, except one dog that had a kidney with a wedge-shaped discoloration, probably due to ischemia or infarction, at its apex. No abnormalities of the aorta or renal arteries were evident on angiography.

Pathologic examinations revealed that endothelialization of stent-graft surfaces started from 4 weeks and that the stent-grafts were completely covered in neointima at 12 weeks (Figs. 3A, 3B, 3C, 3D, and 3E). Intimal thicknesses of the groups were measured on stent wire and on graft (Table 1). Intimal thicknesses gradually increased with the duration of follow-up. The neointima was thin (< 1 mm) and regular, and no hyperproliferation, which can disturb aortic flow, was evident in any case (Table 2). The aorta at the stent-graft location showed mild inflammation for the first 4 weeks and normalized during follow-up. No thrombus was observed between the stent-graft and the aorta, which suggests substantial flow restriction by the stent-graft. A single case of small focal hemorrhage at the aortic wall at the junction between the graft and the distal stent was observed in the 4-week group (Figs. 4A, 4B, 4C, 4D, and 4E). Subintimal hematoma and smooth-muscle cell proliferation were seen at the distal portion of the stent-graft (~ 1.2-2.5 mm) but did not influence blood flow, and a thin even neointimal cell layer and smooth-muscle cell layer were observed in the other portion of the stent.


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  		TABLE 1: Intimal Thickness in Each Study Group

 

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  		TABLE 2: The Average Neointimal Thickness in Each Study Group

 

Figure 10
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  		Fig. 4A —Case from 4-week follow-up group. Three angiograms obtained before (A), just after (B), and 4 weeks after stent-graft placement in dog in 4-week follow-up group (C). Focal narrowing was present at distal part of stent.

 

Figure 11
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  		Fig. 4B —Case from 4-week follow-up group. Three angiograms obtained before (A), just after (B), and 4 weeks after stent-graft placement in dog in 4-week follow-up group (C). Focal narrowing was present at distal part of stent.

 

Figure 12
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  		Fig. 4C —Case from 4-week follow-up group. Three angiograms obtained before (A), just after (B), and 4 weeks after stent-graft placement in dog in 4-week follow-up group (C). Focal narrowing was present at distal part of stent.

 

Figure 13
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  		Fig. 4D —Case from 4-week follow-up group. On gross examination, dark brown hematoma was present in this distal portion of stent-graft.

 

Figure 14
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  		Fig. 4E —Case from 4-week follow-up group. Microscopic examination at site of focal hematoma shows thin intimal cell layer, subintimal hematoma, and proliferation of smooth-muscle cells. In other portion, thin regular neointimal cell layer and smooth-muscle cell layer were observed.

 


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
Treatment paradigms for aortic aneurysm and dissection have evolved with the development of endovascular techniques and with our improved understanding of the pathophysiology of these diseases. In the case of thoracic aortic dissection, primary treatment is usually medical therapy consisting of ß-blockade, antihypertensive therapy, and general supportive measures. Surgical intervention with graft interposition has been a traditional treatment for most patients with diseases of the descending aorta [18], and endoluminal aortic stent-graft placement was recently introduced for abdominal and thoracic aneurysm repair [19-21]. Endoluminal repair is also a new therapeutic alternative that is yielding encouraging results in the high-risk setting of aortic dissection [15, 16, 18-22].

Treatment strategies for type B aortic dissection involve the exclusion of the primary entry tear to induce thrombosis and retraction of the thoracic false lumen. Placement of a stent-graft across the primary entry tear could provide an effective single-step treatment that might be more efficient than endovascular techniques for the relief of ischemic complications and would be less invasive than aortic graft replacement at thoracotomy [15, 22, 23]. Furthermore, stent-graft placement caused aortic remodeling by expanding the true lumen and thrombosis and retraction of the false lumen, which mimics the natural aortic healing process [15]. Thus, stent-grafting techniques hold tremendous promise for high-risk patients with aortic aneurysm or dissection, but several limitations should be discussed—that is, the biocompatibility of the materials used, proper device fixation, healing performance, stent-graft migration, and alterations in graft shape and structure.

The technical feasibility and the biocompatibility of a device have important roles in the technical and clinical success of endoluminal repair. In our study, the transfemoral deployment of a separating stent-graft was successful in all nine dogs without any complications such as artery rupture, stent migration, or incorrect stent deployment. We found that stents can be introduced reliably into the thoracic aorta and deployed in a manner that is familiar to most interventionists. Using a 12-French sheath, the 10-French introducing system was advanced easily to the thoracic aorta, and the mean time required to place the separating stent-graft was acceptable.

The devised separating stent-graft offers several advantages: First, surgical aortotomy may not needed because of the stent's low profile; second, blood pressure control is not required during deployment; third, the stent-graft does not migrate during deployment; and, fourth, the procedure time is relatively short (~ 20 min in this study). Once deployed, the self-expanding polyester-covered stents did not recoil, nor did they appear to induce acute thrombus formation or trauma to vessel walls. Furthermore, the 12-French sheath and the 10-French introducing system are more flexible than a larger sheath or introducing system. Therefore, the separating stent-graft is likely to be more easily used in patients with tortuous or narrow iliac vessels. In the present study, the gold markers attached at both ends of the stents facilitated fluoroscopic visualization and precise stent-graft deployment.

Structurally, the stent-grafts showed no signs of instability or disintegration, such as suture breaks, knitted wire element displacement, wire fractures, or tears in the polyester sleeve over the 12 weeks of implantation. Successful endovascular treatment of aortic diseases requires good proximal fixation to avoid migration and proximal graft-related endoleaks. A number of factors come into play—namely, environmental factors such as the shape and length of a proximal neck; the morphology of the aortic wall; the presence of thrombus; and the characteristics of the stent-graft itself, such as the radial force applied by and the size of the stent-graft, the type of device (self-expanding vs balloon expandable), and the presence of proximal hooks or barbs. In our device, the use of an inner bare stent as a supporting skeleton positioned after graft deployment allowed the profile of the stent-graft to be further reduced, allowing patients with smaller iliac arteries to be considered for treatment. Such a sequentially constructed stent-graft system can provide the lower profile and strength required. It also provides excellent longitudinal flexibility, enabling the system to pass through an extremely tortuous iliac artery, thus increasing the technical success rate. The radial force generated by a modular stent-graft system such as ours is attributed to the flexible and powerful inner stent. Our device has two design features that limit migration potential: barbs on the proximal stent and a 0.5-cm gap between the proximal stent and the polyester Dacron fabric (DuPont) graft used for the diseased part of the aorta. Antegrade aortic flow is also maintained through the gap between the stent and aorta during stent-graft deployment and blood pressure control is not required during deployment.

Histologically, the ultrathin polyester fabric-covered stents showed predictable healing. By pathologic examination, endothelialization of the stent-graft surface occurred from 4 weeks and surfaces were completely covered at 12 weeks by neointima. The new endoluminal surface was covered by a confluent thin (< 1 mm) monolayer of mature endothelial cells. The healing of the luminal surface gave way to the development of a neointima—a thin internal collagenous capsule with a continuous endothelial lining. Contact between either the polyester sleeve or the nitinol stent and the aortic wall induced no tissue necrosis, and the nitinol wire was well incorporated within the collagenous tissue. Overall inflammatory response was minimal, with no evidence of histiocytes within neointima, media, or adventitia. After 12 weeks, no inflammatory cells were observed in contact with the nitinol stent. In general, these findings illustrate a favorable biocompatibility that is typical of this foreign material [24-27].

Although endothelialization of the graft area is slightly slower than that at the stent area for ultrathin polyester, the degree and nature of the intimal thickening observed in our study and in others indicate that covered stents provide a stronger barrier than non-covered stents in terms of blocking the migration, proliferation, or both of the intimal and medial cells associated with hyperplasia and stenosis of stents [28-33]. In one case more intima proliferation at the periphery of the distal stent was detected at the 4-week follow-up, but no hyperproliferation capable of disturbing aortic flow was seen in any case. One animal had a small focal hemorrhage at the aortic wall at the junction between the graft and the distal stent in the 4-week group (Figs. 4A, 4B, 4C, 4D, and 4E). The mechanism of endothelial injury during stent expansion is unclear contributing factors may include the following: balloon-vessel contact between struts, pressure imposed by blood confined to the closed space between balloon, stent struts, and vessel wall during expansion; inhomogeneous circumferential strain applied to the vessel wall during dilation; or acute alterations in flow. The reproducible localization of endothelial cell loss to stent interstices also implies that factors such as balloon pressure and compliance, strut thickness and configuration, speed of inflation, and vessel oversizing may all be important determinants of endothelial loss [34].

Many authors have reported results of various stent-graft systems in animals, but to our knowledge, this report is the first of an animal study involving an ultrathin Dacron graft. This animal study also provides details of the healing process associated with ultrathin polyester fabric and a nitinol stent. The limitations of our study are that the follow-up was only 12 weeks and separating stent-grafts were placed in only nine canine aortas. Moreover, the healing process and pattern of endothelialization of aneurysmal or dissection models differ from the normal thoracic aorta. Hence, additional studies in aneurysm or dissection models are required to elucidate the healing process in nitinol ultrathin Dacron devices in the diseased aorta for multiple-year follow-up.


Conclusion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
The technique of endoluminal aortic stent-graft placement has recently been introduced for the repair of thoracic aneurysms. Endoluminal repair is a new therapeutic alternative that is yielding encouraging results in the high-risk setting of aortic dissection.

The described separating type of stent-graft can be easily deployed without the need for blood pressure reduction and achieves accurate deployment without migration in the normal thoracic aorta of a canine model. Because of its low profile, the separating stent-graft can be used more easily in patients who have tortuous or narrow iliac vessels. This animal study provides an examination of the healing process associated with the use of ultrathin polyester fabric nitinol stents and shows their predictable healing characteristics in the normal thoracic aorta.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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