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Implantation of Ultraflex Nitinol Stents in Malignant Tracheobronchial Stenoses^*

^* From the Department of Pulmonary Medicine (Dr. Miyazawa), Hiroshima City Hospital, Hiroshima; Department of Internal Medicine (Dr. Yamakido), Hiroshima University, Hiroshima; Department of Surgery (Dr. Ikeda), Kyoto Katsura Hospital, Kyoto; Department of Surgery (Dr. Furukawa), Tokyo Medical University, Tokyo; Department of Internal Medicine (Dr. Takiguchi), Chiba University, Chiba; Japan; Department of Surgery (Dr. Tada), Osaka City General Hospital, Osaka; and

Correspondence to: Teruomi Miyazawa, MD, FCCP, Department of Pulmonary Medicine, Hiroshima City Hospital 7–33, Moto-machi, Naka-ku, Hiroshima, 730-8518 Japan; e-mail: ikyoku{at}city-hosp.naka.hiroshima.jp

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Study objective: To assess the uncovered Ultraflex nitinol stent (Boston Scientific; Natick, MA) for its efficacy and safety.

Design, setting, and patients: Between October 1997 and October 1998, we carried out a prospective multicenter study at six hospitals in Japan. Fifty-four Ultraflex stents were inserted in 34 patients with inoperable malignant airway stenosis using a flexible and/or a rigid bronchoscope under fluoroscopic and endoscopic visualization.

Measurements and results: Clinical, endoscopic examination, and pulmonary function on days 1, 30, and 60 after stent implantation showed improvement. In 19 patients (56%), stent implantation was performed as an emergency procedure because of life-threatening tracheobronchial obstruction. Immediate relief of dyspnea was achieved in 82% of the patients. The dyspnea index improved significantly after implantation (before vs days 1, 30, and 60; p < 0.001). Significant improvements were observed in obstruction of airway diameter (81 ± 15% before vs 14 ± 17% on day 1, 12 ± 12% on day 30, and 22 ± 28% on day 60; p < 0.001). Vital capacity (VC), FEV₁, and peak expiratory flow (PEF) increased significantly after stent implantation: before vs immediately after VC (p < 0.01), FEV₁ (p < 0.001), and PEF (p < 0.05). The main complications were tumor ingrowth (24%) and tumor overgrowth (21%). After coagulation with an Nd-YAG laser or argon plasma coagulation, mechanical coring out using the bevel of a rigid bronchoscope was necessary in patients showing tumor ingrowth or overgrowth. Removal and reposition were possible in case of misplacement. There were no problems with migration and retained secretions. The median survival time of patients was 3 months. The 1-year survival rate was 25.4%.

Conclusions: In this study of the Ultraflex nitinol stent, we have demonstrated that patients were relieved from dyspnea, which contributed to improved quality of life, with minimal complications. This stent can be used safely, even in the subglottic region. Owing to its excellent flexibility and biocompatibility, the stent is also indicated in certain complicated situations, eg, narrow stenosis, hourglass stenosis, curvilinear stenosis, bilateral mainstem bronchial stenoses, and long stenosis of varying diameters.

Key Words: malignant tracheobronchial stenosis • nitinol stent • Ultraflex stent

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Inoperable central airway stenosis due to a malignant tumor is a relatively common condition and may be life threatening. Because of the poor prognosis, palliative methods are needed to maintain airway patency. Development and improvement of various airway stents and increased experience have led to an increasing variety of indications and number of procedures every year.^{1 2 3 4 5} Therefore, stenting has become a new valuable therapeutic strategy for patients with malignant tracheobronchial stenosis, although there is controversy as to which of the various airway stents available today give the best results. Worldwide, the Dumon silicon stent (Novatech; Aubagne, France) has become the "gold standard" during the past decade. Several thousand placements have been performed and have proven to be safe and effective. It can even be removed when the patient responds to radiotherapy/chemotherapy and does not need the stent any longer.^{4 5 6 7} Expandable metallic stents present the advantages of having thin walls and excellent adaptability to varying airway diameters. The first expandable models, such as the Gianturco Z-stent (Cook; Bloomington, IN), which is made of stainless steel, were used frequently because placement is easy. However, this metallic stent is difficult to extract because it is anchored firmly to the bronchial wall by hooks. In addition, due to its high expanding force, it tends to penetrate the wall and bears the risk of causing a fatal hemorrhage.^{8 9} To reduce these disadvantages, nitinol with its shape memory effect might well become an important alloy for designing stents.^{10 11 12 13 14} Recently, Becker¹ investigated a self-expanding device made of nitinol, the Ultraflex stent (Boston Scientific; Natick, MA), which is more flexible and resembles the physical properties of the cartilages. For easy insertion, he developed a new crochet knotting device. This stent can be easily removed before it is completely epithelialized. He reported that treatment of different kinds of central airway stenoses, even if complicated, has been successful and the complication rate is low.^{1 15 16} Although the ideal stent has yet to be designed, of all the commercially available expandable metallic stents, the Ultraflex stent looks most promising. Thus, this prospective multicenter study was undertaken to assess the uncovered Ultraflex stent for its efficacy and safety.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Between October 1997 and October 1998, we carried out a prospective multicenter study at six centers in Japan, which was approved by the Committee on Human Research of each institution. Informed consent was obtained from all patients and their families. Fifty-four Ultraflex stents were inserted in 34 patients with inoperable central airway stenosis due to a malignant tumor (25 patients with stage III B/IV bronchogenic carcinomas, 4 with esophageal carcinomas, 3 with mediastinal tumors, and 2 patients with metastatic pulmonary lesions). There were 30 men and 4 women (average age, 63 years; Table 1 ). Histopathologically, there were 25 cases of primary bronchogenic carcinoma; among them, there were 5 cases of recurrence of small cell carcinoma after chemotherapy and/or radiotherapy. Most of the patients who had already undergone treatment had end-stage disease. Therapies prior to stent implantation included surgery in 5 patients, chemotherapy in 8, and radiotherapy in 10 patients. In 11 of the 22 patients with an intraluminal tumor, debulking was performed using Nd-YAG laser and/or mechanical coring out using the bevel of a rigid bronchoscope. Ten of 12 patients with predominantly extrinsic compression of the central airways underwent dilatation using a high-pressure balloon catheter. After reopening the airway, if there was residual stenosis of > 50% detected in the tracheobronchial region, we used a guidewire-introduced Ultraflex stent. The Ultraflex stent is folded down and fixed onto an introducing catheter by a new crochet knotting technique. After introduction, it is released by pulling the thread under fluoroscopic and endoscopic visualization. Patients were endoscopically examined before and after stent implantation on days 1, 30, and 60 to check the stent position and patency. The dyspnea index was used to assess pulmonary function before treatment and on days 1, 30, and 60 after implantation. Dyspnea index grades are as follows: grade 0, asymptomatic while climbing stairs; grade I, symptomatic climbing stairs; grade II, symptomatic after walking 100 m on flat ground; grade III, symptomatic with the least effort (talking, getting dressed); and grade IV, symptomatic in bed, at rest.

Statistical Analysis
All analyses were performed using SAS software (Release 6.11; SAS Institute; Cary, NC). The survival rate was compared using the Kaplan-Meier life-table analysis and the log-rank test. Continuous variables were tested by paired t test. A p value < 0.05 was considered to be significant. All results were presented as the mean ± SD.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Fifty-four Ultraflex stents were implanted in 34 patients (Fig 1 ). In 19 patients (56%), stents were implanted as an emergency procedure because of life-threatening tracheobronchial obstruction. Immediate relief of dyspnea was achieved in 82% of the patients. For stent insertion, a flexible bronchoscope was used in 24 instances, and a rigid bronchoscope was used in 10. The number and sites of stent implantation were as follows: 7 stents in the trachea, 19 in the left mainstem bronchus, 10 in the right mainstem bronchus, 10 in the bronchus intermedius, and 3 in lobar bronchi. The sizes of the implanted stents are shown in Table 2 . Due to long stenosis of varying diameters, in two patients three stents had to be implanted and in five patients two stents were implanted (Fig 2 ). Due to bilateral stenosis of the mainstem bronchi, three patients needed three stents and one patient needed two stents. Eight patients were subjected to additional radiotherapy/chemotherapy after stent implantation. Clinical, endoscopic examination, and pulmonary function on days 1, 30, and 60 after stent implantation showed improvement. Response to treatment as indicated by changes in the dyspnea index is shown in Table 3 . Following treatment, a shift to a lesser degree of dyspnea was noted. The dyspnea index improved significantly after implantation (before vs days 1, 30, and 60; p < 0.001). Significant improvement was also observed in obstruction of airway diameter (81 ± 15% before vs 14 ± 17% on day 1, 12 ± 12% on day 30, and 22 ± 28% on day 60; p < 0.001; Fig 3 ). The results of pulmonary function tests in 16 patients before and immediately after stent implantation are shown in Table 4 . Vital capacity (VC), FEV₁, and peak expiratory flow (PEF) increased significantly after stent implantation: before vs immediately after, VC (p < 0.01), FEV₁ (p < 0.001), and PEF (p < 0.05). The flow volume loop after implantation of the stent showed immediate improvement of flow limitation (Fig 4 ). The main complications that arose in the 2-month follow-up period were tumor ingrowth (24%) and tumor overgrowth (21%; Table 5 ). After coagulation with Nd-YAG laser or argon plasma coagulation (Erbe USA; Marietta, GA), mechanical coring out using the bevel of a rigid bronchoscope was necessary in cases of tumor ingrowth and overgrowth. Repositioning or removal was possible in case of misplacement. Follow-up investigations revealed retention of mucus secretion within the stent area in only 9% of the patients. Granulation tissue ingrowth was observed in only one patient, but it did not affect stent patency. Migration of the stent was not observed during follow-up. The causes of death were as follows: 15 cases of cachexia, 5 cases of bleeding, and 1 case of respiratory insufficiency. None of the patients died of suffocation. Death was not attributed to stent-related complications in any patients. Survival curves after stent placement are shown in Figure 5 . The median survival time of patients was 3 months. The 1-year survival rate was 25.4%.

View larger version (73K): [in this window] [in a new window] [Download PPT slide]   Figure 1.. Bronchoscopic images before and after implantation of the Ultraflex stent. Left: extrinsic compression of the trachea. Right: uncovered Ultraflex stent (diameter/length, 16/60 mm) in place.

View larger version (65K): [in this window] [in a new window] [Download PPT slide]   Figure 2.. Three-dimensional CT images before and after implantation of Ultraflex stents. Left: extrinsic compression of the trachea and left mainstem bronchus. Right: uncovered Ultraflex stents in place (diameter/length, 16/80 mm and 12/40 mm, respectively). Both lumina were patent.

View larger version (9K): [in this window] [in a new window] [Download PPT slide]   Figure 3.. Degree of tracheobronchial obstruction before and after implantation of the Ultraflex stent. * = p<0.001 before vs day 1, day 30, and day 60.

View larger version (12K): [in this window] [in a new window] [Download PPT slide]   Figure 4.. Flow volume loop before and after implantation of the Ultraflex stent. Left: before implantation. Right: immediate improvement of flow limitation after implantation is shown.

View larger version (8K): [in this window] [in a new window] [Download PPT slide]   Figure 5.. Survival curves after implantation of the Ultraflex stent. The median survival time of patients was 3 months. The 1-year survival rate was 25.4%.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

Nitinol is a nickel and titanium alloy that has various excellent properties, including superelasticity, biocompatibility, kink resistance, constancy of stress, physiologic compatibility, shape memory deployment, dynamic interference, and fatigue resistance.^{10 11 12 13 14} The elasticity of this alloy, which is 11%, biodynamically resembles that of the tracheobronchial tree most closely, and it is much greater as compared to stainless steel (0.5%).¹⁰

In stress-strain tests, biological tissues show a nonlinear behavior unlike artificial materials, called a hysteresis curve, because of biodynamic involvement of a time factor.¹³ That is, since biological materials show both viscous and elastic plasticity, expansion and returning to the starting point are somewhat delayed. Of all materials currently in use for tracheobronchial stenting, only nitinol shows a hysteresis curve that is very similar to elastic tissue such as the cartilages. By this property, the force exerted onto the airway wall by the stent does not increase even when coughing increases the compression power. This property of nitinol prevents damage of the mucosa. The Ultraflex stent thus may be considered a highly bioadaptable alloy because of its low resistance to cough but sufficient resistance to compression by tumors, thereby preventing reocclusion. In experiments of the stress-strain study performed by Freitag et al,¹⁴ the Gianturco stent,^{8 9} which is made of stainless steel, in contrast shows an exponential increase in power at a nonlinear slope. Therefore, this stent may perforate the airway wall and vessels due to its excessive force of expansion. Another metallic device, the Wallstent,¹⁷ which is made of a cobalt steel alloy, increases in length at both ends by 3 to 4 mm when compressed on coughing. Thus the sharp spikes at both ends of the stent almost regularly damage the mucosa and induce the formation of granulation tissue. The Strecker tantalum stent¹⁸ shows a plastic deformation at the nonlinear slope when pressure is strong. Also the Palmaz stent,¹⁹ which is made of stainless steel, shows a nonlinear and irregular slope and plastic deformation when a lateral strong pressure is applied. Thus both the Strecker and Palmaz stents are liable to collapse and are not suitable to maintain airway patency. In contrast, the Ultraflex stent has the least risk of perforation unlike the Gianturco stent, its length does not change as in the case of the Wallstent, and it does not collapse like the Strecker stent and Palmaz stent. Thus, the above complications are rare for the Ultraflex stent, compared with other metal stents.^{1 14}

The strain of the Dumon stent,^{5 6 7} which is made of silicon, increases linearly following Hooke’s law; therefore, the expansion power depends on the stiffness of the material. The Dumon stent is known as the "gold standard" because it is economical, readjustment is simple, and removal or replacement is always possible. However, the Dumon stent shows complications such as stent migration and retained secretion inside the stent. Since the Ultraflex stent scarcely migrates, it can be used safely even if it has to be implanted in the subglottic region, where fixation of a Dumon stent is usually difficult. Compared to the Dumon stent, the Ultraflex stent is more flexible and the retention of secretions inside the stent is insignificant. As the walls are much thinner, more space is left for the lumen. Moreover, the uncovered Ultraflex stent may become epithelialized, potentially improving mucociliary clearance. Several weeks after stent implantation, the stent is covered by reactive metaplastic epithelial cells of squamous differentiation. Finally, the whole stent may become covered by a continuous layer of ciliated epithelium that provides an almost regular transport of the mucus.²⁰ Thus, this stent can be implanted even in a long stenosis without minor risk of retention of secretions. As the wire mesh of the Ultraflex stent is flexible and expands actively, it fits advantageously to complex shapes such as narrow and curvilinear stenosis. For example, the stent fits even to the lumen of an hourglass-shaped stenosis to which the Dumon stent cannot fit due to tilting. The Ultraflex stent adapts better to bends and curvatures. In fact, in the present study, these stents could be implanted in complicated situations, such as long stenoses of varying diameters and bilateral bronchial stenoses. Consequently, most of the patients showed significant airway recanalization and improvement of dyspnea at a low complication rate.

Apart from the material and design of the Ultraflex stent, easy manipulation for implantation is another characteristic of this stent. Because of its new crochet knotting device, the Ultraflex stent can be implanted easily, not only using a rigid bronchoscope under general anesthesia like the Dumon stent, but also using a flexible bronchoscope under local anesthesia like that used for implantation of the Strecker stent and the Wallstent.^{18 21 22 23} If the stenosis is inaccessible to the rigid bronchoscope, the Ultraflex stent can be implanted using a flexible bronchoscope. As many pulmonologists using the flexible bronchoscope only are not trained with the rigid bronchoscope, this means that stent implantation can be added as an option in endobronchial treatment. As in this study, many serious cases were included; rigid bronchoscopes were used under general anesthesia to avoid risks in those patients. It is noteworthy, however, that stents were implanted using only a flexible bronchoscope in 60% of the cases studied. This stent can be released by pulling the thread. Unlike other expandable metal stents, this stent does not fully expand immediately after release, allowing time to readjust the position of the stent, if necessary. When the nylon thread at the distal end of the stent is pulled forward with a forceps, the distal end withers like the opening of a purse and can be positioned more distally. Similarly, the proximal end can be pulled up. Moreover, the stent can be easily removed before epithelialization has occurred. Other metal stents are very difficult if not impossible to extract in case of complications, even if they have not yet been covered by the mucosa. Although the Ultraflex stent is not clearly visible under fluoroscopy, it can be safely inserted by endoscopic control. Problems such as malfunction of the release mechanism or misplacement according to the markers rarely occurred in insertion without prior dilatation or laser resection of a stenosis. Positioning of the markers on the introducer catheter requires some improvement for stent placement under fluoroscopy. As recommended by Becker,¹⁶ however, there are fewer problems if after insertion using a guidewire, the position of the stent is adjusted before its complete release under direct visual monitoring through the flexible bronchoscope, which can be easily introduced parallel to the implantation device. Although the implanted stent is not clearly visualized by chest radiograph, it is possible, however, to check the stent position during follow-up. Furthermore, this stent is advantageous, in that it shows neither artifacts in CT nor problems with MRI, unlike the Gianturco stent and the Wallstent.²⁴ However, although the gaps of the wire meshes are smaller than those of the Gianturco stent, tumor ingrowth can also occur through the meshes of the uncovered nitinol stent. Thus after coagulation with Nd-YAG laser or argon plasma coagulation, mechanical coring out using the bevel of a rigid bronchoscope was necessary in cases of tumor ingrowth or overgrowth. By applying covered Ultraflex stents that are now available for treatment in cases of exophytic tumor growth, granulation tissue, and fistulas, this complication can be prevented.

Implantation of the Ultraflex stent for palliative treatment of malignant airway stenoses should be considered when it has become clear from the endoscopic observation that this is feasible. In therapeutic bronchoscopy, we should use the type of stent that is best indicated for a specific situation. With this regard, the nitinol stent can be used in all localizations, even in the subglottic region, without risk of migration. Owing to its excellent flexibility and biocompatibility, this stent is also indicated in certain complicated situations, eg, narrow stenosis, hourglass stenosis, curvilinear stenosis, bilateral mainstem bronchial stenoses, and long stenosis of varying diameters. In this prospective multicenter study of this nitinol stent, we have demonstrated that patients were relieved from dyspnea, which contributed to improve their quality of life, with minimal complications.

	Acknowledgements

 
The authors thank Dr. Heinrich D. Becker (Thoraxklinik; Heidelberg, Germany) for valuable advice and comments on this article.

	Footnotes

 
Abbreviations: PEF = peak expiratory flow; VC = vital capacity

Department of Surgery (Dr. Shirakusa), Fukuoka University, Fukuoka, Japan.

Received for publication October 20, 1999. Accepted for publication April 20, 2000.

	References

TOP Abstract Introduction Materials and Methods Results Discussion References

 

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