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Ann Thorac Surg 2007;84:401-409
© 2007 The Society of Thoracic Surgeons

---

Original Articles: General Thoracic

Impact of Anastomotic Airway Complications After Lung Transplantation

^a Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, Cleveland, Ohio
^b Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, Ohio
^c Department of Pulmonary, Allergy, and Critical Care Medicine, Cleveland Clinic, Cleveland, Ohio

Accepted for publication May 4, 2007.

^_* Address correspondence to Dr Murthy, Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, 9500 Euclid Ave, Desk F24, Cleveland, OH 44195 (Email: murthys1{at}ccf.org).

General thoracic surgery: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Background: Because improper airway healing continues as a source of morbidity after lung transplantation, we determined prevalence and risk factors for anastomotic complications and examined their impact on survival.

Methods: From January 1997 to January 2004, 272 patients undergoing pulmonary transplantation were studied for anastomotic airway complications. Complications were categorized as necrosis or obstruction and treatment as none, endoscopic (stenting, bronchoplasty, ablation), or open repair. Survival impact was assessed by follow-up (mean, 3.0 ± 2.2 years) using competing-risks nonproportional hazards methodology in the context of repeated events.

Results: By 24 months, 94 anastomotic airway complications (26 necrotic, 67 obstructive, 1 torsion) had developed in 48 patients (18%), and 23 (8.5% overall; 48% of affected patients) underwent intervention. Risk of necrotic complications preceded obstruction. Risk factors were telescoping anastomosis (p < 0.0001), more recent transplant (p < 0.0001), donor–recipient size mismatch (p = 0.008), and previously treated anastomotic airway complication (p < 0.0001). Seventy-eight interventions were performed for 60 of the 94 complications. Compared with patients experiencing no anastomotic airway complications, those with treated complications had equivalent early survival (82% versus 80% at 12 months, p = 0.9) but worse late survival (60% versus 27% at 48 months, p = 0.03), and those with untreated complications had worse early survival (82% versus 62% at 12 months, p = 0.004) but equivalent late survival (p = 0.4).

Conclusions: Anastomotic airway complications occur in about one fifth of patients after lung transplantation and are formidable and persistent problems. Early complications are necrosis, followed by obstruction. Few risk factors are modifiable. Because these complications importantly affect survival, improving efficacy of intervention strategies should improve outcome.

Dr Mehta discloses a financial relationship with Alveolus Corp.

 

Survival after orthotopic lung transplantation has steadily improved [1]. Nevertheless, improper airway healing continues to be a source of morbidity and perhaps mortality. Although thoughtful discourse regarding the etiology of anastomotic airway complications has been published [2–7], information on their long-term impact is limited, especially in light of improved posttransplant survival. Therefore, objectives of this study were to (1) determine prevalence of and risk factors for these complications, (2) review management strategies, and (3) examine their impact on survival.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Patients
The lung transplantation program at Cleveland Clinic began in February 1990. Between its inception and July 2004, 386 patients underwent transplantation. Since January 1997, 272 of 276 patients had systematic recording of anastomotic airway complications in the Unified Transplant Database (UTD). Their characteristics, indications for transplant, and immunosuppression are presented in Table 1, Appendix Figure 1 _^*, and Appendix 1 _^*. Notably, no patient received sirolimus-based immunosuppression as induction therapy or early posttransplant [8].

View larger version (28K): [in this window] [in a new window]   Appendix Fig 1. Indication for transplant.

View larger version (76K): [in this window] [in a new window]   Appendix Fig 2. Bronchoscopic images of anastomotic airway complications: partial or full-thickness necrosis. (A) Necrosis of right single lung transplant airway. (B) Suspected early dehiscence with suture eroding into airway.

View larger version (58K): [in this window] [in a new window]   Appendix Fig 3. Bronchoscopic images of anastomotic airway complication: obstruction. (A) Obstruction from eccentric granulation tissue stenosis. (B) Obstruction from cicatricial fibrosis. (C) Obstruction from bronchomalacia.

Systematic follow-up was performed yearly for vital status and to identify complications diagnosed and treated elsewhere. Follow-up was 100% complete. Mean follow-up among 147 survivors was 4.0 ± 2.1 years. Follow-up was approved by the Institutional Review Board (IRB), with written consent from patients or surviving family members.

Anastomotic Airway Techniques
Airway anastomoses were performed by telescoping or end-to-end techniques. Permanent, absorbable, or mixed sutures were used in an interrupted or running (continuous) fashion. Buttressing of anastomoses was predominantly performed with pedicled thymic pericardial fat (Table 1).

Data
Procedure summaries of all posttransplant bronchoscopies were reviewed to identify and record any anastomotic airway complication. Additional medical record review provided information about presenting symptoms and management of airway complications. Data from this review and the UTD were approved for use in research by the IRB, with patient consent waived.

Data Analysis
Anastomotic airway complications
Anastomotic airway complications were analyzed as time-related repeating events. A complication was considered a new event if it was of a different type (necrosis versus obstruction), recurred after treatment, or occurred on the contralateral side in a bilateral lung transplant. Unit of study was the patient, not anastomosis, with single versus bilateral lung transplantation (including sidedness) considered a potential risk factor (Appendix 2 _^*). Nelson’s cumulative event methodology provided nonparametric estimates [10], and a multiphase hazard methodology provided parametric estimates [11].

Because the temporal pattern of risk for each additional complication was similar, we used modulated renewal process methodology [12, 13]. For this, patients experiencing a first event are restarted at a new time 0 and tracked to a second one, and so forth, for each successive event [12].

Risk factors were identified by bootstrap bagging variable selection [14] using 500 resampled data sets, automated analysis with p = 0.05 for variable inclusion, and retention of variables or clusters of highly related variables appearing in 50% or more of analyses.

Impact on survival
Impact of anastomotic airway complications on survival was estimated within the same modulated renewal context as repeated complications, treating death as a competing risk [15]. This allowed us to include occurrences of preceding events and their timing, number, type, treatment, and interaction of complication type and treatment as potential risk factors for death. Nonproportionality of risk was accommodated by multiphase hazard methodology [11].

	Results

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Prevalence
By the end of follow-up, 48 patients experienced anastomotic airway complications, an occurrence of 18% within 24 months. In 20 patients the first complication occurred after transplantation but before hospital discharge, and their postoperative length of stay was considerably longer than those whose first complication became evident after discharge (median, 26 days [15th percentile, 13 days; 85th percentile, 61 days] versus 14 days [15th percentile, 10 days; 85th percentile, 24 days], p = 0.002).

A total of 94 repeated events occurred in 15 of the 48 patients, of which 26 were necrosis, 67 were obstruction, and one was torsion. Of the 94 occurrences, 32 (34%) were asymptomatic, while 52 (55%) were accompanied by dyspnea, 8 (8.5%) by sepsis, and 2 (2.2%) by pneumothorax. The cumulative number of complications per patient was 0.18, 0.24, 0.31, and 0.34, respectively, at 3, 6, 12, and 36 months after transplant (Fig 1).

View larger version (9K): [in this window] [in a new window]   Fig 1. Anastomotic airway complications after lung transplantation. Cumulative number of events per patient is depicted from repeating-events analysis. Each symbol is an event, vertical bars are asymmetric 68% confidence limits (CL) equivalent to ± one standard error, and numbers in parentheses are patients remaining at risk. Solid line is parametric estimate enclosed within dashed 68% CLs.

View larger version (12K): [in this window] [in a new window]   Appendix Fig 4. Necrotic (circles) and obstructive (squares) anastomotic airway complications after lung transplantation. Cumulative number of events per patient is depicted from repeating-events analysis. Each symbol is an event, vertical bars are asymmetric 68% confidence limits (CL) equivalent to ± one standard error, and numbers in parentheses are patients remaining at risk. Solid lines are parametric estimates enclosed within dashed 68% CLs.

View larger version (9K): [in this window] [in a new window]   Fig 2. Instantaneous risk (hazard function) of necrosis-related (top line) and obstruction-related (bottom line) anastomotic airway complications after lung transplant. Solid lines are parametric estimates enclosed within dashed 68% confidence limits.

View larger version (13K): [in this window] [in a new window]   Fig 3. Probability of occurrence of one anastomotic airway complication after lung transplantation and recurrence of a second and third event. Each symbol represents an occurrence, vertical bars are 68% confidence limits (equivalent to ± one standard error), and numbers in parentheses are patients remaining at risk. Solid lines are parametric estimates enclosed within dashed 68% confidence limits.

View larger version (12K): [in this window] [in a new window]   Fig 4. Anastomotic airway complications after lung transplantation, formatted as in Fig 1, stratified by telescoping versus end-to-end technique.

View larger version (8K): [in this window] [in a new window]   Appendix Fig 5. Anastomotic airway complications within 24 months of lung transplantation according to date of operation. Solid line is parametric temporal trend enclosed within dashed 68% confidence limits (equivalent to ± one standard error).

View larger version (9K): [in this window] [in a new window]   Appendix Fig 6. Relation of height mismatch to occurrence of obstructive complications within 24 months of lung transplantation. Format is as for Appendix Fig 5.

View larger version (6K): [in this window] [in a new window]   Appendix Fig 7. Proportion of complications treated according to date of their occurrence. Filled circles are grouped prevalence, and solid curve is the temporal trend estimate.

View larger version (17K): [in this window] [in a new window]   Fig 5. Impact of anastomotic airway complications and their treatment on survival after lung transplantation. Format is as for Fig 3. Open circles represent survival before occurrence of complications (competing-risk modulated renewal analysis), closed circles are survival after a treated anastomotic airway complication, and squares are survival after an untreated complication.

	Comment

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

• Airway anastomoses are constructed in a contaminated field, with microbiologic pathogens often being multidrug resistant.

• A tension-free anastomosis cannot be created, because the bronchial suture line is subject to wall stress imparted by positive pressure ventilation until extubation occurs.

• Perhaps most important, anastomoses are likely ischemic from the outset and may not derive meaningful collateral blood flow for several weeks.

It is, consequently, not surprising that prevalence of anastomotic airway complications has remained unchanged during the last 15 years [2–7] despite the improved survival of lung transplant recipients [1].

Prevalence
At least one anastomotic airway complication developed in 18% of our transplant population, consistent with many other investigators’ findings. Simply reporting this as the prevalence would be misleading for three reasons, however. First, we used inclusive criteria for reporting anastomotic complications rather than focusing solely on patients receiving intervention at the time of diagnosis, as most others have. This allowed us to gain insight into the natural history of airway complications as they evolved. Second, the phenomenon is a time-related lifelong risk, confounded by the competing possibility of death. Third, complications can recur or manifest with different characteristics over time; for example, initially necrosis, followed by obstruction. Thus, prevalence of airway complications can be expressed accurately only by time-related, repeating-events estimates.

We were able to distinguish two distinct patterns of risk for airway necrosis and airway obstruction. Risk of necrosis peaked early and receded quickly. This seems logical, because airway anastomoses cannot remain profoundly ischemic for extended periods without either healing or dehiscing. We suspect that some necrotic complications transition into obstruction, which is supported by the delayed early and protracted late risk of obstruction. Surprisingly, before they were first diagnosed, most obstructive complications were not preceded by a necrotic event. The timing of surveillance bronchoscopy, however, was not designed to demonstrate this but rather to identify rejection. As a consequence, any direct temporal progression of necrosis to obstruction is difficult to document. Clearly, some obstructive events, such as cicatricial fibrosis, may occur de novo over a protracted period without obvious antecedent necrosis.

Risk Factors
We have, similar to others, attempted to identify quantifiable risk factors for anastomotic airway complications. Telescoping anastomotic technique was a dominant one for both necrotic and obstructive complications. The literature on this lacks consensus: some have argued in favor of the standard telescoping technique [7, 16]; others, a modified telescoping technique [6]; and still others, end-to-end anastomoses [4, 17]. There is no doubt that exaggerated intussusception of the donor bronchus should be avoided. The donor bronchial edge is at risk for ischemia, which may cause sloughing and mechanical obstruction; moreover, the intussuscepted bronchus likely entraps airway pathogens [18]. Nevertheless, a minimally telescoped anastomosis may be the only solution to size mismatch, which we have also identified as a risk factor.

We have modified our practice to perform end-to-end or minimally telescoped anastomoses according to the intraoperative assessment of size discrepancy. We suspect that in the past, surgeon preference was instead the more common explanation for use of the telescoping technique. Regardless of which technique is used, we believe that the donor and recipient peribronchial tissues should not be disturbed, and the donor airway should be cut back as close to the secondary carina as possible.

Of concern, risk of airway complications was greater in the latter years of the study. This may represent our heightened sensitivity, a direct result of therapy, or unrecognized technical factors. We are continuing to investigate possible mechanisms that may explain this phenomenon.

We have essentially abandoned routinely wrapping anastomoses with recipient tissues because it is unlikely that buttressing alters the natural history of full-thickness necrosis or prevents late stenosis [17]. Donor peribronchial tissues, as well as the donor lung itself, become surprisingly adherent to the anastomosis, as we have found at reoperation; we suspect that these donor tissues are responsible for preventing a dehiscence from fistulizing to the pleural space.

Management of Complications
Less than half our patients with anastomotic airway complications underwent intervention. The nature of these interventions shifted because of endobronchial therapies, evidenced in our own practice by the paucity of open surgical procedures.

Self-expanding metallic stents (SEMS) were used liberally early in the experience because of ease of deployment and lack of migration. It became apparent that their use led to formidable problems from excessive granulation tissue, fracture, bacterial and fungal colonization, and perforation. Late extraction of SEMS for these indications is treacherous [19]. As a consequence, we now avoid airway stenting whenever possible. We have, nonetheless, successfully salvaged some patients with bronchial dehiscence by short-term deployment of uncovered SEMS [20], which appear to serve as scaffolds for granulation tissue and mucosal in-growth. These patients must be surveyed frequently, however, and stents removed or exchanged before becoming fully incorporated. This strategy has been more successful in our practice than use of silicone stents [21, 22].

Impact on Survival
Of interest was that we observed three distinct patterns of survival that depended on the presence or absence of anastomotic airway complications and whether or not they were treated. Remembering that we could not identify an association of treating airway complications with symptoms, the pattern of survival of untreated airway complications is unexpected.

These patients appeared to segregate into two major categories based on instantaneous risk. The first group had exceptionally high early mortality. Interventions were not performed on these patients because the airway complications were considered incidental, less consequential than other more critical aspects of the posttransplant course, or not amenable to therapy. The second group demonstrated late mortality equivalent to that of patients without airway complications. Their complications presumably self-healed; one might imagine that intervention in these patients would demonstrate no positive survival impact and could be deleterious.

The pattern of survival of patients treated for airway complications suggests that we can palliate these problems successfully for several months but may be unable to cure them. We suspect that in some patients, treatment itself could perpetuate airway difficulties, possibly accounting for additional late mortality. Recognizing this possibility, our recent practice has tended toward less frequent use of airway stents and fewer interventions for minimally symptomatic patients. Because each center has a different threshold for treating anastomotic airway complications, conflicting reports of their impact on survival could be reconciled by institutional bias [3, 5, 23].

Limitations
This is a single-institution study representing the results of a changing team of surgeons across time, with variation in techniques and accrual of experience. It was impossible to account for every technical variation in performing airway anastomoses; subtle differences among surgeons are undocumented and so cannot be assessed.

Recognition and timing of anastomotic airway complications, particularly if asymptomatic, depend on frequency of observation. It is possible that reduced hazard for these events, and consequent leveling off of their cumulative occurrence, could be underestimated early by the coarseness of surveillance and late by decreasing frequency of surveillance.

Only 1 bronchoscopist was present at each surveillance bronchoscopy, so interobserver variation could not be quantified. Further, until recently, we have not graded airway complications or electronically captured images of them for collective review [20, 24, 25].

Recommendations and Conclusions
Anastomotic airway complications remain a formidable and persistent problem after lung transplantation. Although uncommonly encountered, they present a therapeutic dilemma, often in the context of other, unrelated critical management issues. They ultimately contribute to a late survival disadvantage.

We, and others, have identified a few modifiable risk factors. Minimally intussuscepting disparate bronchi and end-to-end anastomoses should be performed to reduce these complications. Perhaps more attention should be paid to donor–recipient size mismatch, which is often unavoidable given the donor shortage, critical illness of patients on waiting lists, and altered chest dimensions of recipients.

Additional research is needed to identify the most appropriate candidates for intervention as well as to improve existing therapies and develop new ones that might improve long-term survival. For now, interventions for anastomotic airway complications should be applied judiciously.

Use of SEMS is controversial. Their ease of deployment and low immediate morbidity initially made them attractive options for managing necrotic and obstructive airway complications. Only in hindsight have we come to understand the important limitations of this technology. Specifically, although we found that SEMS offered excellent early palliation for obstruction, their late complications were often more formidable than the initial obstructive problem; as a consequence, use of SEMS in this context has more recently been curtailed. Our only current indication for SEMS placement in transplant recipients is for airway dehiscence [20]. Even in these circumstances, patients with SEMS must be vigilantly followed up and stents changed every 10 to 14 days until airway healing is complete. This has been found to be an excellent strategy to manage this particularly difficult, although rare, airway complication. Our current patient management algorithm for anastomotic airway complications, based on this experience, is presented in Figure 6.

View larger version (15K): [in this window] [in a new window]   Fig 6. Patient management algorithm for anastomotic airway complications, based on this reported experience. (*Resolved necrosis event may proceed to obstruction; **for example, ablation, dilatation, silicon stent placement; ***mildly symptomatic obstructions may be closely observed, particularly if the complication is malacia. BPF = bronchopleural fistula; SEMS = self-expanding metallic stents.)

	Appendix 1

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Immunosuppression
Perioperative and postoperative immunosuppression consisted of triple drug therapy (calcineurin inhibition [cyclosporine or tacrolimus], azathioprine, and steroids).

Induction therapy with antithymocyte gammaglobulin (ATGAM) was used when dictated by a positive actual or virtual cross-match. Acute rejection was treated with a methylprednisolone pulse (1000 mg/d for 3 days), and acute refractory rejection was an indication for ATGAM administration, with or without concomitant plasmapheresis.

	Appendix 2

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Variables Used for Multivariable Analyses
Recipient demographics: Race, sex, age, height, weight, body surface area, body mass index

Indication for transplant: -1-Antitrypsin deficiency, chronic obstructive pulmonary disease/emphysema, cystic fibrosis, idiopathic pulmonary fibrosis

Comorbidity: Coronary artery disease, diabetes, cytomegalovirus status, steroid therapy

Donor variables: Race, sex, age, height, weight, body surface area, body mass index

Recipient–donor mismatch: Difference in height, weight, body surface area, body mass index

Transplant: Single lung, left or right, double lung; ischemic time

Transplant technique:

Airway anastomotic suture technique: permanent only, absorbable; continuous suture only, interrupted sutures only, mixed sutures

Anastomotic technique: telescoping versus end-to-end, suture line buttressing—not covered, wrapped, wrapped with fat pad, pleural flap, or omentum

Support technique: Off cardiopulmonary bypass versus on cardiopulmonary bypass

Experience: Interval from January 1997 to transplant

Postoperative: Reintubation (used only for analysis of complications)

For modulated renewal analyses: Number of previous anastomotic airway complications, interval between occurrences, type of each occurrence, treated necrotic or obstructive event

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
Supported in part by the Kenneth Gee and Paula Shaw, PhD, Chair in Heart Research; the Peter and Elizabeth C. Tower and Family Endowed Chair in Cardiothoracic Research; James and Sharon Kennedy; the Slosburg Family Charitable Trust; and Stephen and Saundra Spencer.

We thank Joan Alster, MS, for preliminary statistical analysis; Jeevanantham Rajeswaran, MS, for assistance in data analysis; Lucy Thuita, MS, for statistical programming; Angela York for database programming; and Tess Parry, BS, for editorial assistance.

	Footnotes

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 
^_* The Appendices are available only online. To access the Appendices, please visit: http://ats.ctsnetjournals.org and search for the article by Murthy, Vol 84, pages 401–409.e1–4.

	References

Top Abstract Introduction Patients and Methods Results Comment Appendix 1 Appendix 2 Footnotes Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Sudish C. Murthy Eugene H. Blackstone Gonzalo V. Gonzalez-Stawinski David P. Mason Gösta B. Pettersson Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Murthy, S. C. Search for Related Content PubMed PubMed Citation Articles by Murthy, S. C. Related Collections Lung - transplantation