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Table of Contents    
Year : 2013  |  Volume : 61  |  Issue : 1  |  Page : 45-50

Application of the Willis covered stent using the telescopic technique for the treatment of fusiform aneurysm in a canine model

Institute of Diagnostic and Interventional Radiology, The Sixth Affiliated People's Hospital, Shanghai Jiao Tong University, Shanghai, China

Date of Submission13-Oct-2012
Date of Decision28-Oct-2012
Date of Acceptance20-Jan-2013
Date of Web Publication4-Mar-2013

Correspondence Address:
Ming-Hua Li
No. 600, Yi Shan Road, Shanghai, 200233
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Source of Support: The National Natural Scientific Fund of China (Contract number: 30970793)., Conflict of Interest: None

DOI: 10.4103/0028-3886.107937

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 » Abstract 

Background: The covered stent is one of the most promising tools for the treatment of intracranial fusiform aneurysms. We developed an in vivo model of fusiform aneurysms and evaluated the effectiveness of double telescoping Willis covered stents for their treatment. Materials and Methods: An external jugular vein graft was anastomosed with the common carotid artery (CCA) to construct the fusiform aneurysm model. After at least 4 weeks, two Willis covered stents were implanted in a telescopic fashion. Angiography follow-up was performed at 2 weeks and 1 and 3 months to examine the grafts. The animals were sacrificed at 1 or 3 months of the follow-up period, and the stents were examined histologically. Results: A total of eight fusiform aneurysms in four canines were created and 16 covered stents were implanted successfully. No technical or device-related difficulties occurred. The angiographic follow-up results showed that six fusiform aneurysms were completely occluded, and a minimal endoleak occurred in two fusiform aneurysms. Histological examination revealed endothelial progress and all aneurysm sacs were filled with thrombi. Conclusion: Vein graft anastomosis with CCA to construct a model of fusiform aneurysm may reproduce the clinical conditions. This study demonstrated that the implantation of two Willis covered stents in a telescoping fashion is an effective way to treat an experimental model of fusiform aneurysm.

Keywords: Animal model, covered stent, canine, fusiform aneurysm

How to cite this article:
Yan L, Shi WY, Wang D, Zhu YQ, Tan HQ, Li MH. Application of the Willis covered stent using the telescopic technique for the treatment of fusiform aneurysm in a canine model. Neurol India 2013;61:45-50

How to cite this URL:
Yan L, Shi WY, Wang D, Zhu YQ, Tan HQ, Li MH. Application of the Willis covered stent using the telescopic technique for the treatment of fusiform aneurysm in a canine model. Neurol India [serial online] 2013 [cited 2021 Jan 26];61:45-50. Available from:

 » Introduction Top

Intracranial fusiform aneurysms are rare, comprising <1% of clinical cases of cerebral aneurysms, and they commonly occur in the internal carotid artery or the vertebrobasilar artery in elderly patients with severe atherosclerosis. [1],[2],[3] These aneurysms may produce severe neurological symptoms, including mass effects, subarachnoid hemorrhage, thromboembolic complications, and/or transient ischemic attacks. [3],[4] Some studies documented that the natural history of these aneurysms is unfavorable with a 23-80% rate of severe morbidity and mortality in a 5-year follow-up period if left untreated; [1],[5],[6] this indicates the necessity for early treatment. Intracranial fusiform aneurysms are defined as the circumferential dilatation of a cerebral artery without any ostium or neck. As a result of their specific anatomical features, the currently available surgical techniques and neuroendovascular devices are inadequate for the effective treatment of these aneurysms and they are at high risk of incomplete occlusion, regrowth, and life-threatening rupture. [7],[8],[9]

The covered stent is a promising device for the treatment of intracranial fusiform aneurysms, which could restore the normal vascular morphology by preventing blood flow into the aneurysm lumen and preserving the parent artery. [10] The Willis covered stent is an endoluminal construct that was specifically designed for intracranial applications. The feasibility of using the stent, including clinical and experimental implantations, has been reported in preliminary studies. [11-13] However, to date, there have been no studies that examined their use for fusiform aneurysms. Furthermore, there is no data regarding the endothelialization process within stents implanted in fusiform aneurysms. In this study, we sutured the external jugular vein pouch to the CCA to create an experimental model of fusiform aneurysm. Using this model, we examined the technique of using two telescoping covered stents for the treatment of fusiform aneurysms. Moreover, we observed the endothelialization of the stent grafts at 1 and 3 months postoperatively.

 » Materials and Methods Top

The protocol in this study was approved by the animal research committee of our institution and was conducted in accordance with the guidelines of the International Council on Animal Care. All animals were maintained with a standard laboratory diet. Four dogs (beagles, Agronomic School of Shanghai Jiaotong University, Shanghai, China) of both genders weighing 15-25 kg were used.

Under sterile conditions, the animal was fixed in a supine position. A midline skin incision of approximately 10 cm was made on the anteroinferior neck. A 4-cm long segment of the left external jugular vein was exposed and resected and two 0.8- to 1.2-cm long venous pouches without branches were harvested. They were kept in heparinized saline (a mixture of 1,000 IU heparin in 30-ml 0.9% saline). The left common carotid artery (CCA) was exposed and approximately 10 cm was freed. The artery was temporarily clipped proximally and distally with two atraumatic hemostatic clamps and divided in the middle; then, the vein sample was engrafted using end-to-end anastomosis. The vascular clips were released and the bleeding points of the anastomotic stoma were repaired to prevent leakage. The same procedure was performed in the right CCA of each dog.

Stent implantation was performed 4 weeks or more after aneurysm construction, and all animals received oral aspirin (100 mg/d) and Ticlid (75 mg/d) for consecutive 3 days before endovascular treatment. The construction and implantation of the Willis covered stents (MicroPort, Shanghai, China) [Figure 1]a and b] has been reported in our previous report. [12] In this study, two covered stents were implanted in a telescopic fashion in each fusiform aneurysm. After an angiographic examination, the stents were selected and implanted. We usually chose the first stent that was a little larger in diameter than the parent artery; the second stent had a diameter that was the same or 0.5-mm wider than the first. To ensure a complete permanent reconstruction from the distal to proximal parent artery, the stents were implanted with a landing zone of at least 3 mm on either side of the aneurysm. The first stent was deployed in the distal parent artery and the second stent was then advanced into the proximal parent artery and deployed within the previous stent. There was an overlap of at least 3 mm at the junction of the stents. Anti-platelet treatment in the form of aspirin (100 mg/d) and Ticlid (75 mg/d) was continued after the stent implantation. In addition, low molecular heparin sodium (4,000 U/d) was injected subcutaneously and benzylpenicillin potassium (1,200,000 U/d) was injected intramuscularly for 3 days after stenting.
Figure 1: Photograph of the Willis covered stent in its constricted form (a) and completely expanded and deployed in vitro (b)

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All animals underwent digital subtraction angiography using standard techniques via a transfemoral approach under general anesthesia. Immediate angiography prior to stent deployment was performed to assess the gross morphological characteristics (i.e., fusiform dilation, patency of the parent artery). Follow-up angiography was performed immediately after, and then at 2 weeks, 1 month, and 3 months after stent implantation. The isolation of the fusiform aneurysm, parent artery restenosis, and the presence of an endoleak were evaluated.

Eight fusiform aneurysm models were sacrificed for histological examination at 1 and 3 months of follow-up (n =4 at each period). Light microscopy (n =4) and scanning electron microscopy (n =4) were performed after the stented arteries were removed from the living models. The sections were harvested from the aneurysm core with the cutting plane perpendicular to the longitudinal axis of the parent artery, with thickness ranging from 30 to 50 μm. Fusiform aneurysm sac thrombosis and stent tissue coverage were analyzed by using light microscopy after sections were stained with hematoxylin and eosin. The stented aneurysm models were longitudinally incised and carefully spread apart. Five samples were taken from different sites in each specimen (from proximal to distal of the two stents, samples were gathered at an average distance among five points) and prepared for the examination. Four samples were fixed on scanning electron microscopy stubs, sputter-coated with gold, and examined in a high-vacuum mode with accelerating voltages of between 2 and 10 kV. Two photos were taken from each sample and the degree of endothelial progression was analyzed by two pathologists.

 » Results Top

All surgical and endovascular procedures were well-tolerated in four dogs, and no complications related to the surgery occurred. A total of eight fusiform aneurysms were created. Angiography performed at 4 weeks or more after surgery demonstrated well-opened fusiform aneurysms with apparent fusiform dilation and a good degree of patency of the parent arteries.

All stents were implanted successfully without technical or device-related difficulties. No arterial perforations occurred during the implantation procedure and there was no formation of thrombosis. There was no instance of distal end of the graft retracting and prolapsing back into the aneurysm. The angiography immediately after implantation revealed complete resolution of the fusiform aneurysm with no endoleak in seven models, and one aneurysm with a mild endoleak that appeared at the junction of the two stents [Figure 2]a-d. Follow-up conventional angiography was performed at 2 weeks, 1 month, and 3 months post-stent implantation. The first at 2 weeks into the follow-up period depicted another mild endoleak [Figure 3]a-d that appeared between the stent and distal parent artery. Six fusiform aneurysms were completely occluded and a mild endoleak into the aneurysm sac persisted in two aneurysms. These decreased gradually over the following 3-month follow-up period. All of the constructs were found to be stable and no parent artery stenosis or occlusion was observed. The fusiform aneurysm characteristics, endovascular treatments, and angiography follow-up are summarized in [Table 1].
Figure 2: Angiography was performed at 8 weeks after the creation of a fusiform aneurysm (arrow) (a) Immediate angiography after implantation revealed a mild endoleak (arrow) at the junction of the two stents (b) Angiography at 1 and 3 months post-stent insertion showed that the mild endoleak (arrow) still existed, but was gradually decreasing (c and d)

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Figure 3: Another angiography was obtained 4 weeks after surgery. This illustrated a well-opened fusiform aneurysm (arrow) (a) Immediate angiography after stenting (arrow) revealed absolute arterial occlusion (b) Angiography at 2 weeks showed that a mild endoleak (arrow) had appeared between the stent and distal parent artery (c) the endoleak (arrow) still existed, but had decreased in size at 3 months (d)

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Table 1: Summary of treatment with two Willis covered stents in 4 dogs with 8 experimental fusiform aneurysms

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Thrombus was observed in the sac of all studied aneurysms and most were becoming organized. The stents were well inlaid in the wall of the parent arteries and the surface of the stents was covered with a neointima with no significant in-stent narrowing. A thicker layer was observed at 3 months than at the 1 month angiographic examination [Figure 4]a. Endothelialization in the Willis covered stent was first found at the proximal and distal edge and arranged along the longitudinal axis of the stents. Endothelial cells were found at 1 month after stent insertion, which was loosely arranged with "oval" appearing cells covering the entire stent area. Endothelial progress was almost complete in most mesh areas at 3 months, and the stent struts were covered with regularly arranged endothelial cells [Figure 4]b-d.
Figure 4: Light microscopy examination at 3 months follow-up showed the grafts (short allow), neointimal formation (long arrow), and thrombus (double arrows) (a) Scanning electron microscopy examination at 1 month (b) and 3 months (c and d) of follow-up showed the progressive endothelialization

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 » Discussion Top

Although there have been some reported models of fusiform aneurysm in the carotid artery or abdominal aorta induced by porcine pancreatic elastase, to our knowledge, this has not yet been successfully duplicated in large animals. [14],[15] Fukui et al. [16] initially constructed fusiform aneurysms in rats by surgical venous grafting and the pathological findings were similar to those observed in human intracranial aneurysms. This technique has since been applied in large animals, including dogs and swine among others. These models have been used for the testing and refinement of endovascular devices and techniques. [17],[18] Adult dogs have a long CCA (10-12 cm) and the caliber, a constant diameter of 4-5 mm, is comparable to that of the human internal carotid artery and vertebrobasilar artery. [19] This vessel also provides a sufficient length to construct an aneurysm model and permit the replication of conditions that are similar to those encountered in humans. Moreover, the blood supply of the intracranial arterial system in dogs is mostly obtained through the vertebrobasilar system, where abundant anastomoses exist between each network of the internal carotid artery, the external carotid artery, and the vertebrobasilar artery. [20] This helps prevent death during the operative procedure and enables long-term follow-up. Finally, the number of cells, their composition, and the accompanying proteoglycan matrices of the artery in canine models are essentially the same as in humans. [21] These attributes indicate that the canine model may accurately predict the human biological response to endovascular device implantation.

Compared with saccular aneurysms, fusiform aneurysms involve a much longer segment of the parent artery and may need two or more stents to reconstruct the parent artery. Therefore, we specifically designed the model to test telescopic stents in a context that is more closely related to their clinical use. Gross morphological features and angiographic images depicted apparent fusiform dilation, which was similar to the majority of human intracranial fusiform aneurysms and were suitable for the study of treatment with telescopic covered stents. This model reproduced the difficult-to-treat situation, where a long segment of the parent artery is not in contact with the stents. It has a high surgical success rate and a high rate of fusiform aneurysm formation, without any significant complications related to the procedure, despite its relative complexity.

Intracranial fusiform aneurysm has a variable shape and large size, and its treatment remains a therapeutic challenge despite dramatic progress in microsurgical techniques and endovascular therapies. [7],[8] Endovascular flow diverters (FDs) have been developed recently to treat such aneurysms and have rejuvenated enthusiasm in endovascular treatment. [22],[23] However, complications have been reported in recent studies, and FDs have been shown to fail to occlude in vivo experimental fusiform aneurysms. [9],[24],[25] In treating fusiform aneurysms with stents, the segment of the stents that bridge the aneurysm is not in contact with the vessel wall. Self-expanding stents have a tendency to prolapse back into the aneurysm immediately upon deployment or after a period of time if the landing zone on either side of the aneurysm is insufficient, and it is difficult to estimate how long the stent should be deployed. Thus, multiple stents often have to be used in endovascular treatment, which may increase the incidence of parent artery thrombotic complications or vessel stenosis, especially in the middle cerebral or vertebrobasilar artery.

Unlike coil embolization, coil supportive intracranial stents and FD reconstruction, the curative reconstruction of the covered stent is immediate, as the graft can simultaneously reconstruct the vascular morphology and occlude blood flow into the aneurysm lumen. [10] In addition to supporting the aneurysm packing and flow redirection, the stent provides a physical matrix for endothelial re-growth. Balloon-expanding covered stents have many advantages in treating intracranial aneurysms. First, compared with self-expanding stents, balloon-expanding stents are more stable and easier to control during the treatment of fusiform aneurysms. Second, covered stents confer significantly reduced recurrence rates compared to other devices. Furthermore, this strategy is conducted within the parent artery and avoids aneurysm rupture. Finally, in treating large or giant aneurysms, the mass effect induced by aneurysms could obviously be reduced after the implantation of covered stents.

The Willis covered stent is a new neurovascular balloon-expanding construct designed for intracranial implantation to exclude aneurysms from the parent artery. In this study, to reproduce the potential clinical difficulties of treating fusiform aneurysms with stents, the fusiform aneurysm models were produced and two covered stents were implanted in a telescopic fashion. The stents were used to bridge the aneurysms with a landing zone that was approximately 3 mm on either side of the aneurysm. There was also an overlap of at least 3 mm at the junction of the stents. The results of angiographic follow-up showed a 75% rate of curative exclusion of the aneurysms. All of these constructs were found to be stable, and no stent had retracted and prolapsed back into the aneurysm. The follow-up angiograms demonstrated that a mild endoleak had occurred in two aneurysms, which decreased gradually in volume at 1 and 3 months post-insertion.

The endothelialization of the Willis covered stent within the vessel has been reported in our previous study [12] in both straight and curved arteries. The results of the histopathological examinations in this study were almost the same as previous studies regarding the endothelial progress of ePTFE-covered stents in straight vessels, but these were mainly concerning models of saccular aneurysms. In this study, thrombus was observed in the aneurysm sacs and around the stent, and most were becoming organized. Light microscopy inspection showed that the stents were inlaid in the vessel wall and covered with a new intimal layer, which was thicker at 3 months compared to 1 month after stent insertion. There was no significant in-stent narrowing at both 1 and 3 months of follow-up. Scanning electron microscopy determined that endothelialization was found at the proximal and distal edges of the stents and arranged along the longitudinal axis at 1 month of follow-up, with endothelial cells loosely arranged with an "oval" appearance covering the entire area of the stent. Endothelial cells were regularly arranged at the surface of the stents and endothelialization was almost complete in most mesh areas at 3 months. However, the endothelial cells were not mature or arranged tightly by this stage.

Some limitations of this study should be mentioned. First, the number of experimental model animals used in this initial study was small, and thus the results cannot be used to support generalizations or show statistical significance. Second, preliminary experience about endovascular stent implantation in animal models has shown that double anti-platelet therapy is necessary to prevent thrombosis, but the data is inconclusive. Therefore, the drugs and dosages we used in this experiment were arbitrary and were judged by clinical experience. Third, the 3-month end-point was relatively short, and it was therefore difficult to estimate the possibility of aneurysm recanalization and parent artery stenosis. Moreover, the model used in this study could not absolutely reproduce the pathological changes of human fusiform aneurysms. Finally, this study did not reproduce the problem of side branch coverage, which may be encountered clinically.

The fusiform aneurysm model used in this experiment successfully reproduced the morphological features and clinical situation of most human intracranial fusiform aneurysms. These results indicate that the experimental fusiform aneurysms may be treated with telescoping Willis covered stents with a favorable angiographic outcome, although further large series with long-term follow-up are necessary to determine the durability of these promising results.

 » References Top

1.1. Drake CG, Peerless SJ. Giant fusiform intracranial aneurysms: Review of 120 patients treated surgically from 1965 to 1992. J Neurosurg 1997;87:141-62.  Back to cited text no. 1
2.2. Mizutani T, Miki Y, Kojima H, Suzuki H. Proposed classification of nonatherosclerotic cerebral fusiform and dissecting aneurysms. Neurosurgery 1999;45:253-9.  Back to cited text no. 2
3.3. Biondi A. Trunkal intracranial aneurysms: Dissecting and fusiform aneurysms. Neuroimaging Clin N Am 2006;16:453-65.  Back to cited text no. 3
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1]

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