Marc Noppen, MD, PhD, FCCP; Grigoris Stratakos, MD; Jan D Haese, MD; Marc Meysman, MD, FCCP; and Walter Vinken, MD, PhD
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1 Removal of Covered Self-Expandable Metallic Airway Stents in Benign Disorders* Indications, Technique, and Outcomes Marc Noppen, MD, PhD, FCCP; Grigoris Stratakos, MD; Jan D Haese, MD; Marc Meysman, MD, FCCP; and Walter Vinken, MD, PhD Study objectives: To describe the technique and outcome of removal of self-expandable metallic airway stents (SEMAS) in a series of patients who underwent stenting for benign airway stenoses. Design and setting: A retrospective cohort analysis of patients with benign airway disorders treated with SEMAS between 1997 and 2003, who presented with an indication for stent removal in a tertiary-care hospital, and referral interventional pulmonology clinic. Patients and methods: During the study period, 49 SEMAS were inserted in 39 patients for treatment of benign airway disorders. Ten of these 39 patients (25.6%), bearing 12 covered stents, presented with an indication for stent removal. Data of these cases were extracted from electronic files kept in our institution archive. Results: Indications for stent removal included excessive or recurrent granuloma formation (five cases), recurrence of stenosis after stent failure (one case), stent fracture (two cases), and accomplishment of treatment (two cases). In all of these cases, covered versions of SEMAS had been placed either in the trachea or in a main bronchus. In contrast to many previous reports, these stents proved to be absolutely retrievable even if some difficulties were encountered. In all cases, however, removal was successful without major complications. All patients resumed normal spontaneous ventilation postoperatively, and follow-up was uneventful. Average duration of stenting before removal was months ( SD) [range, 1 to 60 months]. Conclusions: We conclude that although placement of SEMAS is assumed to be permanent in patients with benign airway disorders, an indication for stent removal is often observed (25.6% in our series). The covered SEMAS can be effectively and safely removed if needed without major sequelae. Nevertheless, new technical improvements in metallic stent design and materials may help reinforce the concept of a retrievable metallic airway stent, which may offer significant clinical advantages. (CHEST 2005; 127: ) Key words: benign tracheobronchial strictures; central airways obstruction; interventional pulmonology; rigid bronchoscopy; self-expandable stents Abbreviations: PITS postintubation stenosis; SEMAS self-expandable metallic airway stents Surgical tracheal sleeve resection and reconstruction remains the gold standard treatment for most benign airway strictures. 1 However, nonsurgical modalities such as laser photocoagulation and *From Interventional Endoscopy Clinic, Respiratory Division, University Hospital AZ-VUB, Free University of Brussels, Brussels, Belgium. Manuscript received January 20, 2004; revision accepted August 27, Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( permissions@chestnet.org). Correspondence to: M. Noppen MD, PhD, Head, Interventional Endoscopy Clinic, Respiratory Division, University Hospital AZ-VUB, Laarbeeklaan 101, B 1090 Brussels, Belgium; marc.noppen@az.vub.ac.be resection, balloon dilatation, and electrocautery have been developed to deal with airway stenosis not amenable to surgery. Endoscopic implantation of airway prostheses (stents) in these patients has gained increasing popularity over the last decade. Currently, various inoperable benign airway disorders are considered indications for airway stenting. 1,2 Postintubation stenosis (PITS), tracheal burn or trauma, tracheobronchomalacia, and extrinsic compression of the trachea are the most common etiologies amenable to stenting. Due to their ease of removal and repositioning, silicone stents have extensively been used in the past when a benign disorder was encountered. 3 5 Their disadvantages 482 Clinical Investigations
2 (high migration rate, small lumen-to-wall thickness ratio, and difficulty to clear secretions), however, prompted endoscopists to use self-expandable metallic airway stents (SEMAS) when silicone prostheses were unsuitable (ie, distal airway) or stent migration probability was judged too high (ie, tracheomalacia). 6 8 Potential advantages of using metallic stents include smaller migration rate, greater cross-sectional airway diameter due to thinner wall construction, better conforming to irregular airways, and epithelialization within the stent allowing for maintenance of mucociliary clearance, not to mention a greater ease of placement, which in some cases may lead to inappropriate use. 9 Disadvantages of this type of stent in benign disorders include difficult repositioning or removal after deployment due to their embedding in the bronchial mucosa and epithelialization of the inner surface. Granuloma formation at the extremities (or within the stent wall if uncovered) is a relatively common inconvenience of both type of stents (silicone or metal) possibly resulting from the radial force applied against the airway wall and the friction exerted. This complication often requires repetitive interventions to treat granulomas or replace the prosthesis, thus making patient management more difficult. 10,11 Existing published experience with second-generation SEMAS (Wallstent and Ultraflex; Boston Scientific; Galway, Ireland) is quite limited and almost uniformly describes them as permanent or as difficult to remove In several cases however, stent removal or replacement is imposed by the presence of various complications, disease relapse, or treatment failure or even treatment accomplishment. Pediatric patients represent another common indication for stent removal or replacement. 15 In this study, we evaluated retrospectively metallic stent removal in patients with benign disorders treated in our institution during the last 7 years. We report on the indications, technique, outcomes, and complications of these stent removals. Table 1 Benign Indications for Placement of SEMAS Indication Patients, No. Stents, No. PITS Tracheo/bronchomalacia 5 7 Thyroid goiter 5 5 Postlobectomy or pneumonectomy 5 8 syndrome Tracheoesophageal or bronchopleural 2 2 fistulas Tracheal burn 2 4 Relapsing polychondritis 1 2 Miscellaneous (trauma, Wegener 4 5 disease, tracheal hamartoma, aortic aneurysm) Total candidates due to contraindications to surgery (ie, critically ill or with severe comorbidities or presenting very long, malacic, and complex stenoses), or because patients declined surgery after extensive multidisciplinary counseling. In most cases, SEMAS were preferred because of the presence of a malacic portion of the trachea and/or major bronchi, or when an irregular and small airway was involved making the use of Dumon silicon stents unsuitable. Since published experience of metallic autoexpandable stent removal was quite limited and these stents generally have been described as nonretrievable, their deployment was initially considered permanent. After stent placement, patients had to quit smoking and were prescribed normal saline solution nebulizations twice daily. Technique Description When indicated and after informed consent by the patient, removal of stents was performed with rigid bronchoscopy (Karl Storz; Tutlingen, Germany) in a fully equipped operating theater under total IV anesthesia (IV propofol, alfentanil, and atracurium). Ventilation and oxygenation were ensured by highfrequency jet ventilation with variable fractional inspiratory oxygen concentrations delivered by a side port of the bronchoscope. Materials and Methods We retrospectively analyzed data on all patients with benign disorders who received SEMAS between 1997 and Data were extracted from electronic files of our institution archive. Forty-nine SEMAS (41 covered Ultraflex stents, 6 uncovered Ultraflex stents, and 2 Wallstents) were inserted by rigid bronchoscopy in the central airways of 39 patients hospitalized for benign airway disorders in our institution. There were 24 male and 15 female patients (mean age, years [ SD]; range, 16 to 95 years). All patients were admitted for severe dyspnea caused by central airway obstruction as confirmed by fiberbronchoscopy. Indications are listed in Table 1. All patients were nonsurgical Figure 1. Two covered Ultraflex stents endoscopically removed 2 years after placement (patient 10). Granuloma formation can be seen on the proximal edge of one of the stents (arrows). CHEST / 127 / 2/ FEBRUARY,
3 Removal was performed by grasping the circular extraction loop or if impossible, one of the metallic loops of the proximal edge of the stent with a rigid alligator forceps. Meanwhile, the beveled edge of the rigid scope was advanced coaxially until the proximal edge of the stent was introduced in the inner lumen of the scope, thus creating a space between the stent wall and the airway mucosa. Immediately after that, pulling the stent extremity with the forceps together with a turning movement of the rigid bronchoscope allowed for successful removal of the stent, which in many cases was retrieved intact (Fig 1). Although successful at the end, this procedure proved demanding in both bronchoscopic skills and operating time. If the stent broke during this process, the remaining threads would be removed piecemeal with the forceps through the rigid bronchoscope. Results Ten of the 39 patients (25.6%), all of them bearing covered versions of SEMAS, presented with an indication for stent removal during the follow-up period (5 male and 5 female patients; mean age, years; range, 16 to 62 years). Indications for removal included restenosis due to excessive or recurrent granuloma formation impossible to manage with other treatment modalities (five cases), relapse of stenosis after initial treatment due to material fatigue (one case), stent fracture (two cases), and accomplishment of treatment (two cases) [Table 2]. Presenting symptoms were recurrence of dyspnea in six cases, foul breath and purulent expectoration in two cases, while the remaining two patients were asymptomatic and indication for removal of prosthesis was documented by follow-up fiberbronchoscopy. Average duration of stenting before indication for removal was months (range, 1 to 60 months). We were able to remove all 12 stents in the 10 patients (11 from the trachea and 1 from the left main bronchus, all covered Ultraflex stents). Significant oozing and tracheal mucosa dehiscence occurred in only two patients and could be controlled by bronchoscopic techniques (tamponade by means of the shaft of the bronchoscope). Small pieces of metallic wire totally embedded in the Table 2 Clinical Characteristics of Patients Who Presented With an Indication for Stent Removal* Patient, No. Gender Age, yr Indication for Stenting Type/Size, mm Duration of Stenting, mo Reinterventions Prior to Stent Removal, No. Indication for Removal Long-term Outcome 1 Male 16 PITS, malacic trachea/ UF Female 39 PITS, obesity, malacic trachea/uf and UF Male 37 Malacia, tracheal reconstruction/ UF Female 61 Goiter, extrinsic compression/ UF Female 61 Postpneumonectomy syndrome, tracheomalacia/ UF Female 45 PITS, relapse after reconstruction surgery/ UF Male 47 Tracheo-bronchomalacia in the left main bronchus/uf Female 57 Transplantation, stenosis of anastomosis/ UF Male 62 Relapsing polychondritis/ UF Male 58 Tracheomalacia, obesity/ UF and UF *UF Ultraflex stent Treatment accomplishment 24 3 Extensive granuloma formation (two stents removed) 1 4 Extensive granuloma formation and keloids 18 1 Treatment accomplishment Uneventful follow up Tracheostomy was performed; patient died 4 wk later from pulmonary embolism New stenting was imposed by recurrent granulation and stenosis Uneventful follow-up 6 2 Rupture of stent Replaced by a new stent; 2 mo later a second stent was added 1 1 Extensive granuloma formation 11 3 Extensive granuloma formation 12 2 Extensive granuloma formation Tracheostomy was performed; no major complications Brachytherapy followed with excellent results Replaced by a silicone Dumon stent of same size; uneventful followup 5 1 Rupture of tracheal stent Replaced by a new stent; uneventful follow-up 24 2 Relapse of stenosis due to Replaced by new stents; fatigue of stent (two repositioned next day stents removed) due to migration; uneventful follow-up 484 Clinical Investigations
4 tracheal or bronchial mucosa remained in place in three cases, as it was impossible to remove them without causing major trauma to the airway mucosa. These small metallic threads have been followed up bronchoscopically (Fig 2). They have remained stable and have not caused any complications. However, a longer follow-up period is required to exclude long-term sequelae. No other complications were observed. All patients resumed normal spontaneous ventilation postoperatively, and no late complications related to the procedure occurred. All five patients with stent-related granuloma formation had undergone multiple interventional bronchoscopic treatment trials including cryotherapy, mechanical excision, or balloon dilatation prior to the decision for stent removal (Table 2). In two of these patients, tracheostomy had to be performed after removal of airway prostheses, due to their critical health status considered not amenable to other interventional or conservative treatment. One patient with tracheomalacia who presented a marked tendency for granulomas and keloids received brachytherapy treatment, 16,17 with excellent results. In the remaining two patients of this subgroup, new stents had to be deployed due to continuing need for airway wall support. Stent replacement was also necessary in the two cases of stent rupture as well as in the case of stent failure due to material fatigue 2 Figure 2. Bronchoscopic view of the trachea 2 months after removal of the self-expandable metallic stents. Healing of the mucosa is evident, although the imprints of the mesh are still recognizable. A small peace of embedded metallic thread is still visible (arrow), but has not caused complications during follow-up. years after first placement. In two patients in whom treatment was judged accomplished, the presence of stents was no longer indicated; they were dismissed after stent removal without any other treatment and follow-up was uneventful. Discussion The management of patients with tracheobronchial strictures of benign etiology can be quite challenging. There are a large number of patients with lesions not amenable to surgery, or who are considered medically inoperable. 2 In these patients, airway stenting may represent the only possible treatment. Silicone prostheses are considered the first choice in benign diseases except in cases where they are judged unsuitable because of airway wall malacia or distal and/or angular stenosis. In such cases, SEMAS are generally indicated. 1,6 8 Although SEMAS have systematically been used during the last decade to manage benign tracheobronchial strictures with well-documented positive results, their use for this indication is still debated. 11,14 Despite their more advantageous internal/external diameter and decreased risk of migration, the major drawback for placement of the currently used SE- MAS in benign situations is their difficult repositioning and removal in case of complications. Reports on these removals are scarce in the literature, 13 15,18 and the overall impression is that placement should be considered permanent and therefore restricted to patients with a short life expectancy. 2,18 In our series of 39 patients treated with SEMAS of second generation (Wallstent and Ultraflex), 10 patients (25.6%) presented with an indication for removal. In all of the cases, it was the polyurethanecovered expandable Ultraflex stent that had to be removed. It is possible that if patients with the uncovered version of the same stent had presented with an indication for stent removal, results would have been different. Five of the 10 patients had excessive and recurrent granuloma formation for which other means of treatment were exhausted. Granuloma formation is a common complication of airway stents. The constant friction of stents and the highly localized pressures they exert against the mucosa possibly promotes the development of granulation tissue. Ideally, a stent should fit tightly and should not move to avoid friction. An undersized stent would exert excessive friction of the metal against the airway wall, while an oversized one would exert excessive radial pressure alongside the bronchial mucosa and impair microcirculation. 1,19 It is therefore of cardinal importance to select the proper size of stent and make sure its edges are smooth. CHEST / 127 / 2/ FEBRUARY,
5 In our series of SEMAS placed for benign tracheobronchial strictures (39 patients) during a follow-up period of up to 6 years, we observed granuloma formation over the edges of the stent or through its metallic meshes in 17 patients (43%) requiring several interventional bronchoscopy procedures including cryotherapy, balloon dilatation, or mechanical excision. Only 5 of those patients (or 12.8% in our series), however, had to have their stents removed. As life expectancy of patients with stents is getting longer and more benign indications are recognized for airway stent insertion, the high rate of granuloma formation over the stent will become more of concern and a major limitation. The mesh of the Ultraflex stent is made of Nitinol, a highly bioadaptable nickel-titanium alloy exhibiting low resistance to cough yet adequate resistance to airway compression. Stent fracture or failure due to metal fatigue after some years of continuous strain may develop in a number of patients and call for stent removal (three cases or 7.7% in our series). Metal fatigue of the mesh and spontaneous expulsion of wire stent fragments (metalloptysis) have been previously reported. 19,20 No specific contributing factors (trauma, emergency intubation, recurrent infections, or persistent cough) could be identified in our patients; the short duration of treatment (5 months and 6 months, respectively) also is unlikely to contribute to the rupture or fatigue of the stent. Strengthening of the airway wall can be observed after some years of stenting, making further mechanical support unnecessary. For silicone stents, several studies 4,21 have reported 18 months as a proper duration of stenting before removal is attempted, but no data on SEMAS are available. In our series, we postulated treatment accomplishment in two cases (5.1%), one with a PITS, and another with a malacic stricture resulting from external compression of trachea by a large goiter. Durations of stent treatment were 5 years and 1.5 years, respectively. Stability of the bronchoscopic appearance and the informed patient request were the major criteria for attempting removal in these two patients. No recurrence or other complication followed stent removal, and both patients could be dismissed from hospital without further treatment. We were able to remove all 12 covered Ultraflex stents from our patients. To our knowledge, there is no other published report of a similar series of stent removal. No major complications occurred during the removal procedure. In two cases, oozing occurred, which could be easily controlled after tamponade with the shaft of the bronchoscope. This is in accordance with previous scarce case reports 10,12 14,19 of stent removal, where only minor bleeding was observed. Dehiscence or laceration of the tracheal mucosa was amazingly self-healing, and in both patients in whom we observed this phenomenon, no sign of scar or trauma was seen 2 months after intervention (Fig 2). Conclusion Although placement of SEMAS is assumed to be permanent in patients with benign airway disorders, an indication for stent removal is often observed (25.6% in our series). The results obtained in our study suggest that covered SEMAS can be both effectively and safely removed if needed without major sequelae. However, removal can be cumbersome in inexperienced hands. Efforts are ongoing to produce better-designed, technically improved, removable airway stents that may be more suitable for pediatric use and for patients with long life expectancy. 22,23 Newer improvements in organic materials (poly-l-lactide) have also led to experimental studies in animals, testing bioabsorbable airway stents, which would not have to be retrieved at all. 24,25 These new technical improvements in self-expandable stent design and materials may offer considerable clinical benefits in the future. References 1 Freitag L. Tracheobronchial stents. In Bolliger CT, Mathur PN, eds. Interventional bronchoscopy: Progress in Respiratory Research (Vol 30). Prog Respir Res Basel, Switzerland: Karger, 2000; Wood DE, Liu YH, Vallières E, et al. Airway stenting for malignant and benign tracheobronchial stenosis. Ann Thorac Surg 2003; 76: Vergnon JM, Costes F, Bayon MC, et al. Efficacy of tracheal and bronchial stent placement on respiratory functional tests. Chest 1995; 102: Martinez-Ballarin JL, Diaz-Jimenez JP, Castro MJ, et al. Silicone stents in the management of benign tracheobronchial stenoses: tolerance and early results in 63 patients. Chest 1996; 109: Dumon JF, Cavaliere S, Diaz-Jimenez JP, et al. Seven years experience with the Dumon prosthesis. J Bronchol 1996; 3: Nashef SA, Dromer C, Velly JF, et al. Expanding wire stents in benign tracheobronchial disease: indications and complications. Ann Thorac Surg 1992; 54: Rousseau H, Dahan M, Lauque D, et al. Self-expandable prostheses in the tracheobronchial tree. Radiology 1993; 188: Nesbitt JC, Carrasco H. Expandable stents. Chest Surg Clin N Am 1996; 6: Noppen M, Van Renterghem D, Vanderstraeten P. The wrong stent at the wrong time: a cautionary tale. Respiration 2003; 70: Gaissert HA, Grillo HC, Wright CD, et al. Complication of benign tracheobronchial strictures by self-expanding metal stents. J Thorac Cardiovasc Surg 2003; 126: Jantz MA, Silvestri GA. Silicone stents versus metal stents for 486 Clinical Investigations
6 management of benign tracheobronchial disease: pro; metal stents. J Bronchol 2000; 7: Rafanah AL, Mehta AC. Stenting of the tracheobronchial tree. Radiol Clin North Am 2000; 38: Sonett JR, Conte JV, Orens J, et al. Removal and repositioning of permanent expandable wire stents in bronchial airway stenosis after lung transplantation. J Heart Lung Transplant 1998; 17: Rodriguez AN, Jimenez JP, Edell ES. Silicone stents versus metal stents for management of benign tracheobronchial disease: con; metal stents. J Bronchol 2000; 7: Prasad M, Bent JP, Ward RF, et al. Endoscopically placed nitinol stents for pediatric tracheal obstruction. Int J Pediatr Otorhinolaryngol 2002; 66: Kennedy AS, Sonett JR, Orens JB, et al. High dose brachytherapy to prevent recurrent benign hyperplasia in lung transplant bronchi: theoretical and clinical consideration. J Heart Lung Transplant 2000; 19: Brenner B, Kramer MR, Katz A, et al. High dose rate brachytherapy for nonmalignant airway obstruction: new treatment option. Chest 2003; 124: De Mello-Filho FV, Antonio SM, Carrau RL. Endoscopically placed expandable metal tracheal stents for the management of complicated tracheal stenosis. Am J Otolaryngol 2003; 24: Saad CP, Murthy S, Krizmanich G, et al. Self-expandable metallic airway stents and flexible bronchoscopy: long-term outcomes analysis. Chest 2003; 124: Aggarwal A, Dasgupta A, Mehta AC. Metalloptysis expulsion of wire stent fragments. Chest 1999; 115: Brichet A, Verkindre C, Dupont J, et al. Multidisciplinary approach to management of postintubation tracheal stenoses. Eur Respir J 1999; 13: Song HY, Shim TS, Kang SG, et al. Tracheobronchial strictures: treatment with a polyurethane-covered retrievable expandable nitinol stent. Initial experience. Radiology 1999; 213: Hwang JC, Song HY, Kang SG, et al. Covered retrievable tracheobronchial hinged stent: an experimental study in dogs. J Vasc Interv Radiol 2001; 12: Saito Y, Minami K, Kobayashi M, et al. New tubular bioabsorbable knitted airway stent: biocompatibility and mechanical strength. J Thorac Cardiovasc Surg 2002; 123: Korpela A, Aarnio P, Sariola H, et al. Bioabsorbable self reinforced poly-l-lactide metallic and silicone stents in the management of experimental tracheal stenosis. Chest 1999; 115: CHEST / 127 / 2/ FEBRUARY,
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