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(Chest. 2001;120:1894-1899.)
© 2001 American College of Chest Physicians

Interventional Bronchoscopy for the Management of Airway Complications Following Lung Transplantation*

Prashant N. Chhajed, MD, DNB, FCCP; Monique A. Malouf, FRACP; Michael Tamm, MD; Phillip Spratt, FRACS and Allan R. Glanville, MD, FRACP

* From the Heart Lung Transplant Unit, St. Vincent’s Hospital, Sydney, Australia.

Correspondence to: Prashant N. Chhajed, MD, DNB, FCCP, Heart Lung Transplant Unit, St. Vincent’s Hospital, deLacy Building, Level 14, Victoria St, Darlinghurst, NSW 2010, Sydney, Australia; e-mail: chhajed{at}hotmail.com


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To assess the efficacy and complications of different interventional bronchoscopic techniques used to treat airway complications after lung transplantation.

Design: Retrospective study.

Setting: Heart-lung transplant unit of a university hospital.

Patients: From November 1986 to January 2000, interventional bronchoscopy was performed in 41 of 312 lung transplant recipients (13.1%) for tracheobronchial stenosis, bronchomalacia, granuloma formation, and dehiscence.

Interventions: Dilatation, stent placement, laser or forceps excision.

Measurements and results: Mean (± SE) improvement in FEV1 in 26 patients undergoing dilatation for a stenotic or a combined lesion was 93 ± 334 mL or 8 ± 21%. In seven of these patients not proceeding to stent placement, mean improvement in FEV1 was 361 ± 179 mL or 21 ± 9%. Patients needing stent placement after dilatation had a mean change in FEV1 after dilatation of - 5 ± 325 mL or 3 ± 23%, and an improvement of 625 ± 480 mL or 52 ± 43% after stent insertion. Mean improvement in FEV1 for patients treated with stent insertion for bronchomalacia was 673 ± 30 mL or 81 ± 24%. Complications of airway stents were migration (27%), mucous plugging (27%), granuloma formation (36%), stent fracture (3%), and formation of a false passage (6%). Mortality associated with interventional bronchoscopy was 2.4% (1 of 41 patients). For patients with airway complications successfully undergoing interventional bronchoscopy, the overall 1-year, 3-year, and 5-year survival rates were 79%, 45%, and 32%, respectively, vs 87%, 69%, and 56% for those without airway complications (p < 0.05).

Conclusion: Only a small number of patients with airway stenosis after lung transplantation will respond to bronchial dilatation alone. Patients with airway complications after lung transplantation have a higher mortality than patients without airway complications.

Key Words: airway stenosis • bronchomalacia • dilatation • fiberoptic bronchoscopy • interventional bronchoscopy • lung transplantation • stent


   Introduction
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 Abstract
 Introduction
Materials and Methods
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Despite the improvements in surgical technique and immunosuppression strategies, airway stenosis or malacia still remain major complications after lung transplantation, usually as a result of anastomotic ischemia. Rigid bronchoscopy with bougie dilatation for airway stenosis has largely been replaced by flexible bronchoscopy and balloon dilatation. A variety of silicone and expandable metallic tracheobronchial prostheses have been introduced to palliate complications such as stenosis and bronchomalacia. The objective of this study was to assess the efficacy and complications of different interventional bronchoscopic techniques used to treat airway complications after lung transplantation.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
From November 1986 to January 2000, 312 patients aged 41 ± 12 years (mean ± SE; range, 12 to 62 years) underwent lung transplantation at our institution, including 66 heart-lung (HL), 129 bilateral sequential single lung (BL), and 117 single lung (SL) transplants. Hence, there were 375 bronchial and 66 tracheal anastomosis. Forty-one patients (31 male patients, 10 female patients) aged 43 ± 12 years (range, 16 to 58 years) had airway complications that were managed with interventional bronchoscopic procedures. Details of their underlying lung disease and the type of transplant are presented in Table 1 . Interventional bronchoscopic procedures because of airway complications were performed in 46 of the 441 airway anastomoses (2 tracheal and 44 bronchial). The spectrum of airway complications included tracheobronchial stenosis, bronchomalacia, combined lesions (stenosis and bronchomalacia), dehiscence, and formation of granulation tissue.


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  		Table 1.. Underlying Lung Disease and Type of Transplant in 41 Patients With Airway Complications Treated With Interventional Bronchoscopy*

 
HL, SL, and BL transplantation were performed with the use of standard methods.1 2 3 In the first five patients, anastomoses were performed with omental pedicle wrap using interrupted sutures. The next 20 patients underwent telescopic anastomosis, and since then all patients have undergone end-to-end anastomosis with continuous sutures. No revascularization procedures were performed. All patients were treated with triple-drug immunosuppression (cyclosporine, azathioprine, and prednisolone) and sulfamethoxazole-trimethoprim combination. Patients received antibiotics according to the sensitivity of organisms grown from the donor or the recipient in the perioperative period. Nebulized amphotericin B treatment was commenced immediately postoperatively and continued after discharge only in those patients with positive fungal culture findings.

Flexible bronchoscopy was performed immediately after surgery and subsequently on postoperative days 2 and 7. Surveillance bronchoscopy and transbronchial biopsy was performed at 3 weeks and 6 weeks, and at 3 months, 6 months, and 12 months after transplantation. Bronchoscopy was also performed for clinical symptoms, a fall in lung function, or development of an infiltrate on chest radiograph. The indications for dilatation in patients with a stenotic lesion were as follows: increased shortness of breath, stridor, drop in lung function, a terminal plateau of the expiratory component on the flow volume loop, significant narrowing of the airway (endoscopically > 50% of predicted airway diameter or inability to pass the bronchoscope through a stenotic lesion in the main bronchi or bronchus intermedius), and inability to clear secretions beyond the stenosis with increased frequency of lower respiratory tract infections. The indications for stent placement were stenotic or combined lesions not improving with repeated dilatation, significant bronchomalacia (subtotal occlusion of the airway visualized at bronchoscopy during expiration associated with retention of secretions), or anastomotic dehiscence (in patients not suitable for open surgery). In stenotic lesions with significant inflammation, metallic stent placement was undertaken after dilatation after the lesion had matured into a fibrous stricture. Flexible bronchoscopy was performed with a 6.2-mm diameter bronchoscope. All patients received IM atropine, 0.01 mg/kg, and morphine, 2.5 to 5 mg. Sedation was achieved with IV midazolam, 0.1 to 0.2 mg/kg, and fentanyl, 1 to 2 µg/kg. Rigid bronchoscopy was performed with the Dumon-Harrell Universal Bronchoscope (Efer la Ciotat; France) under general anesthesia.4

In the earlier years, dilatation was achieved with the use of rigid bronchoscopes of increasing diameter (eight patients). Balloon dilatation (Schneider GmbH; Bulach, Switzerland) was performed under fluoroscopy guidance using a radiopaque solution (urograffin, 10 mL, plus normal saline solution, 10 mL; n = 23 patients). Inflation of the balloon (Bard; Billerica, MA) was maintained for 1 min. If necessary, the procedure was repeated either with the same balloon or a larger-diameter balloon. Various stents (Dumon, Bryan, Woburn, MA; Gianturco, Cook, Bloomington, IN; Wallstent, Schneider, Minneapolis, MN; and Ultraflex, Boston Scientific, Watertown, MA) used for stenosis and bronchomalacia were the result of stent evolution and availability. In all, 10 patients had anastomotic dehiscence postoperatively. Reoperation was performed in two patients, interventional bronchoscopy was performed in two patients, and in six patients neither procedure was undertaken. We chose covered Wallstents for the two patients with postoperative anastomotic dehiscence in an attempt to seal the defect, and in one patient with combined lesion having anastomotic bleeding. Nd-YAG laser was used in one patient for the resection of excessive granulation tissue and in another patient with web formation. Patients surviving 30 days postprocedure were considered to have a successful interventional bronchoscopic procedure.

Lung volumes (FEV1) were measured before and after interventional bronchoscopic procedures. FEV1 was measured as recommended by the American Thoracic Society guidelines at the following time points as applicable: predilatation, postdilatation, postdilatation prior to stent insertion, before stent insertion (for patients having only stent placement), and after stent insertion. The functional outcome for all patients who underwent dilatation was assessed comparing predilatation and postdilatation FEV1. For patients who underwent stent insertion following a dilatation procedure, the final outcome of both these procedures were measured using FEV1 predilatation and after stent insertion. The functional outcome of dilatation only, in patients who underwent stent placement following a dilatation procedure, was also assessed using the predilatation FEV1 and comparing it with the FEV1 measured prior to stent insertion. The functional outcome of only stent insertion was assessed using FEV1 before stent insertion and after stent insertion. The Cox-Mantel log-rank statistic was used to compare the survival in recipients with airway complications treated with successful interventional bronchoscopy and those without airway complications.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Airway complications were managed with interventional bronchoscopy in 41 of 312 lung transplant recipients (13.1%). These were present in 46 of the 441 anastomosed airways (10.4%), which included 2 of 66 tracheal anastomoses (3%) and 44 of 375 bronchial anastomoses (11.7%). When compared to the number of transplants based on anastomosis, these complications were observed in 19.7% with SL transplantation and 8.1% with BL transplantation ({chi}2, 9.23; p < 0.05). There was no association of the complications with the age of the patient or the experience of the surgeon. The frequency of the complications did not change over time. The mean duration from transplantation to the diagnosis and treatment of airway complications was 97 ± 68.3 days (range, 17 to 291 days). Twenty-eight patients had pure stenotic lesions in 31 anastomosed airways (3 patients with BL transplantation had bilateral bronchial stenosis). Five patients had bronchomalacia, seven patients had combined lesions, and two patients had anastomotic dehiscence. Of these, one patient with BL transplantation had a combined lesion in the left main bronchus and bronchomalacia in the right main bronchus. All 24 lesions of the left side were located in the main bronchus, whereas 10 of 20 lesions on the right side were located beyond the main bronchus.

Thirty-one patients underwent dilatation for stenotic or combined lesions; of these, 23 patients (74%) underwent stent placement following dilatation (including 3 patients with BL transplantation having bilateral bronchial stenosis). The mean time interval between dilatation and stent insertion was 34.9 ± 30.1 days (range, 3 to 111 days). Three patients underwent dilatation and stent placement in the same sitting. Eight patients (26%) underwent only dilatation for stenotic or combined lesions. Stent placement without dilatation was performed in 10 patients: bronchomalacia (n = 4), stenosis (n = 3), combined lesion (n = 1), dehiscence (n = 2). One patient with bilateral dehiscence underwent placement of two overlapping covered Wallstents in each main bronchus. The functional outcome of dilatation and/or stent placement measured as a change in FEV1 is presented in Table 2 . Patients who underwent dilatation alone were followed up for a mean of 207 ± 211 days (range, 33 to 625 days). In five patients, the FEV1 at follow-up was greater than the postdilatation FEV1. One patient had a fall in FEV1 of 160 mL, and another patient had a fall in FEV1 of 580 mL. The fall in lung function in these patients was not attributed to restenosis as evidenced by bronchoscopy.


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  		Table 2.. Functional Outcomes of Interventional Bronchoscopy Measured as Change in FEV1*

 
There were no complications following dilatation. The complications following stent insertion are presented in Table 3 . Following migration, stents were either replaced (n = 5), repositioned (n = 1), removed (n = 1), or left in situ (n = 2). Stent removal secondary to recurrent mucous plugging was necessitated in two patients with Dumon stents. The modalities used to treat patients having formation of granulation tissue and stenosis were laser excision (n = 2), forceps excision (n = 5), and stent placement (n = 6).


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  		Table 3.. Complications Associated With Various Stent Types in 33 Patients

 
The mortality rate associated with interventional bronchoscopy was 2.4% (1 of 41 patients). The overall survival rate for patients with airway complications successfully undergoing interventional bronchoscopy (36 patients) was significantly lower compared to those patients without airway complications (263 patients). The 1-year, 3-year, and 5-year survival rates (mean ±SE) were 79 ± 7.0%, 45 ± 9.3%, and 32 ± 12.7%, respectively, for patients with airway complications and treated successfully with interventional bronchoscopy vs 87 ± 2.2%, 69 ± 3.1%, and 56 ± 3.7% for those without airway complications (p < 0.05; Fig 1 ). In total, 19 of 36 patients who successfully underwent interventional bronchoscopy died: 1 of 19 patients (5.3%) due to recurrent bronchial stenosis, 14 of 19 patients (73.7%) due to infection, and 4 of 19 patients (21%) due to bronchiolitis obliterans. Five patients died within 30 days postprocedure: anastomotic dehiscence (n = 2), procedure related (n = 1), anastomotic bleeding (n = 1), and tracheal stenosis (n = 1). No bronchoscopic intervention was undertaken in eight patients with postoperative anastomotic dehiscence. The causes of death in the remaining patients (97 of 258 patients) included infection (28.9%), bronchiolitis obliterans (30.9%), graft failure (7.2%), malignancy (14.1%), cerebrovascular accident (5.2%), and others (13.4%). Infection as a cause of death was significantly higher in patients with airway complications (p < 0.05).



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  		Figure 1.. Kaplan-Meier overall survival curves in lung transplant recipients. A: patients with no airway complications (n = 263). B: patients with airway complications successfully undergoing interventional bronchoscopy. C: patients with anastomotic dehiscence with no bronchoscopic intervention (n = 8), plus patients dying < 30 days after interventional bronchoscopy (n = 5).

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Airway complications are a continuing problem in patients undergoing lung transplantation and are reported in 7 to 14% of patients.5 6 7 Overall, 13% of our lung transplant recipients required treatment for airway complications with interventional bronchoscopy. Based on the number of anastomosis at risk, these complications were significantly higher in SL transplant recipients compared to BL transplant recipients. To our knowledge, this observation has not been reported earlier. In SL transplant recipients for emphysema, telescoped anastomotic anastomoses have been reported to be associated with a higher incidence of bronchial anastomotic complications than end-to-end anastomoses.8

A mean gain in FEV1 of 24% after balloon dilatation and an increase in FEV1 ranging from 56 to 117% (maximum, 900 mL) have been reported in the interval before stent insertion and after stent insertion.9 10 11 In our study, the mean improvement in FEV1 was 21% in patients who did not need stent placement postdilatation. The other patients who did not show this improvement in FEV1 benefited by stent placement, with a mean improvement in FEV1 of 52%. Patients with bronchomalacia had a mean improvement in FEV1 of 81% after stent placement. All of these patients have done well, and we believe that stent placement offers a satisfactory outcome for patients with bronchomalacia. Placement of covered Wallstents did not help control the air leak in two patients with anastomotic dehiscence due to ischemia. In four patients with a stenotic lesion, stent placement was attempted without a prior dilatation procedure; of these, one patient (25%) succumbed due to the formation of a false passage and rupture of the left pulmonary artery. Dilatation of airway stenosis before stent placement allows the assessment of the extent of the lesion, the degree of inflammation, and the status of the bronchial tree beyond the lesion. Furthermore, 20% of patients may not need subsequent stent placement. Following the single negative experience with the Gianturco stent, we believe that dilatation may contribute to the safety of subsequent stent placement. Exuberant granulation tissue from an inflammatory stricture may occlude the lumen of a metallic stent. Consequently, as a further advantage, balloon dilatation in this situation allows time for the inflammatory lesion to mature into a fibrous stricture, which is more suitable for metallic stent placement.9 For stenotic lesions, we would recommend the use of balloon dilatation on two occasions prior to stent insertion or more than two occasions if required in presence of significant inflammation.

Bolot et al12 opine that predilatation of a stenosis may not be necessary with the Gianturco stent, as it is a self-expanding device. We had a procedure-related death in one of our patients in whom the insertion of the stent was undertaken without prior dilatation. We had three patients who underwent dilatation and stent placement in the same sitting. All these patients had severe near-total stenosis involving the left main bronchus. We have not used this approach for > 4 years now, during which time balloon dilatation has been employed in all patients with a stenotic lesion prior to stent placement. The other advantages of balloon dilatation are that it may be performed via flexible bronchoscopy, it can be closely monitored under fluoroscopy guidance, it may be repeated, and it is a safe procedure. Formation of granulation tissue is a common complication following Wallstent insertion in lung transplant recipients13 14 ; in our series, it was noted in 27% patients with uncovered Wallstents. The Ultraflex stent, consisting of nitinol,15 has smooth proximal and distal ends and potentially invokes less granulation response. So far, we have not noted complications with our single use of the Ultraflex stent. Mucous plugging following insertion of Wallstents for lung transplant recipients was not a feature in some studies,13 14 and has been reported with the use of covered Wallstents in malignant lesions.16 17 The mucous plugging noted in our group of patients with uncovered Wallstents could be explained by the partial neoepithelialization that may occur with this stent, as opposed to the complete neoepithelialization that occurs with the Gianturco stent, which is designed as a broad metal lattice.

Excessive granulation tissue is removed either with forceps or laser, and often the associated stenosis needs to be treated with stent placement. Mucous plugging is treated using normal saline solution and/or n-acetylcysteine nebulization and physiotherapy. Patients who have difficulty in clearing secretions may need to receive these treatments on a long-term basis. Stents that migrate should be removed and replaced. Stents with minimal migration may be left in situ if they are not occluding any part of the airway and if they are functioning properly. A potential surgical problem could arise with the use of metallic stents if a patient needed retransplantation, as these stents become either partially or completely embedded in the airway wall. Tracheobronchial prostheses are clearly useful for short-term to medium-term gains. Complications associated with the Gianturco stent have led to caution in its use. Our experience enumerates the various problems associated with stent placement and highlights the fact that stent technology is still evolving. In our series, the survival of patients with airway complications needing intervention was lower than survival in patients who did not need intervention. Those who survived 30 days from intervention had a survival rate that was comparable to recent survival rates from the International Society for Heart and Lung Transplantation registry.18

In conclusion, only a small number of patients with airway stenosis after lung transplantation will respond to bronchial dilatation alone. Patients with airway complications after lung transplantation have a higher mortality than patients without airway complications.


   Footnotes
 
Abbreviations: BL = bilateral sequential single lung; HL = heart-lung; SL = single lung

Received for publication June 28, 2000. Accepted for publication June 4, 2001.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Mal, H, Andreassian, B, Pamela, F, et al (1989) Unilateral lung transplantation in end-stage pulmonary emphysema. Am Rev Respir Dis 140,797-802[ISI][Medline]
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  3. Pasque, MK, Cooper, JD, Kaiser, LR, et al (1990) Improved technique for bilateral lung transplantation: rationale and initial clinical experience. Ann Thorac Surg 49,785-791[Abstract]
  4. Dumon, JF (1990) A dedicated tracheobronchial stent. Chest 97,328-332[Abstract/Free Full Text]
  5. Griffith, BP, Hardesty, RL, Armitage, JM, et al (1993) A decade of lung transplantation. Ann Surg 218,310-318[ISI][Medline]
  6. Shennib, H, Massard, G (1994) Airway complications in lung transplantation. Ann Thorac Surg 57,506-511[Abstract]
  7. Schafers, HJ, Haydock, DA, Cooper, JD (1991) The prevalence and management of bronchial anastomotic complications in lung transplantation. Ann Thorac Surg 101,1044-1052
  8. Garfein, ES, Ginsberg, ME, Gorenstein, L, et al (2001) Superiority of end-to-end versus telescoped bronchial anastomosis in single lung transplantation for pulmonary emphysema. Thorac Cardiovasc Surg 121,149-154[CrossRef]
  9. Carre, P, Rousseau, H, Lombart, L, et al (1994) Balloon dilatation and self-expanding metal Wallstent insertion. Chest 105,343-348[Abstract/Free Full Text]
  10. Higgins, R, McNeil, K, Dennis, C, et al (1994) Airway stenoses after lung transplantation: management with expanding metal stents. J Heart Lung Transplant 13,774-778[ISI][Medline]
  11. Lonchyna, VA, Arcidi, JM, Jr, Garrity, ER, Jr, et al (1999) Refractory post-transplant airway strictures: successful management with wire stents. Eur J Cardiothorac Surg 15,842-850[Abstract/Free Full Text]
  12. Bolot, G, Poupart, M, Pignat, JC, et al (1998) Self-expanding metal stents for the management of bronchial stenosis and bronchomalacia after lung transplantation. Laryngoscope 108,1230-1233[CrossRef][ISI][Medline]
  13. Kshettry, VR, Kroshus, TJ, Hertz, MI, et al (1997) Early and late airway complications after lung transplantation: incidence and management. Ann Thorac Surg 63,1576-1583[Abstract/Free Full Text]
  14. Brichon, PY, Blanc-Jouvan, F, Rousseau, H, et al (1992) Endovascular stents for bronchial stenosis after lung transplantation. Transplant Proc 24,2656-2659[ISI][Medline]
  15. Vinnograd, I, Klin, B, Brosh, T, et al (1994) A new intratracheal stent made from nitinol, an alloy with "shape memory effect." Thorac Cardiovasc Surg 107,1255-1261
  16. Bolliger, CT, Heitz, M, Hauser, R, et al (1996) An airway Wallstent for the treatment of tracheobronchial malignancies. Thorax 51,1127-1129[Abstract]
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