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Ann Thorac Surg 2006;82:208-213
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Lung-Volume Reduction Surgery as an Alternative or Bridging Procedure to Lung Transplantation

^a Department of Thoracic Surgery, University Hospital, Zurich, Switzerland
^b Division of Pulmonary Medicine, University Hospital, Zurich, Switzerland

Accepted for publication February 2, 2006.

^_* Address correspondence to Dr Weder, Department of Thoracic Surgery, University Hospital, 8091 Zurich, Switzerland (Email: walter.weder{at}usz.ch).

Presented at the Forty-first Annual Meeting of The Society of Thoracic Surgeons, Tampa, FL, Jan 24–26, 2005.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
BACKGROUND: In this study, we prospectively analyzed the functional outcome and the survival after lung-volume reduction surgery (LVRS) in patients with end-stage emphysema who were initially potential candidates for lung transplantation (LTX), and investigated the impact of LVRS on posttransplant course in patients who underwent LTX after LVRS.

METHODS: Of the 216 patients who underwent LVRS between 1994 and 2005, 58 were potential candidates for LTX at the time of LVRS (age 65 years or younger, forced expiratory volume in 1 second 25% of predicted or less; LVRS/LTX group). Lung-volume reduction surgery was performed by means of video-assisted, bilateral stapled resection of target areas. During the same period, 31 patients underwent primary LTX for end-stage emphysema (LTX group). Spirometry, plethysmography, carbon monoxide diffusing capacity, 6-minute walking distance, and dyspnea score were assessed preoperatively and at predetermined times after operation. Survival analysis was performed by use of the Kaplan–Meier method.

RESULTS: All the functional variables significantly improved after LVRS and peaked within the first year. Subjective improvement was observed for up to 5 years after LVRS, and 53% (31 of 58) of the patients were still alive and had not undergone transplantation after a median follow-up of 44 months. Fourteen percent (8 of 58) of the patients underwent secondary LTX because of progressive worsening of the respiratory function after a median bridging time between LVRS and LTX of 33 months. Postoperative recovery after transplantation and median survival time were comparable between the 8 patients of the LVRS/LTX group and the 31 patients of the LTX group (96.5 months versus 118.5 months, p = 0.9).

CONCLUSIONS: Lung-volume reduction surgery can significantly improve symptoms and lung function in selected patients who are initially potential candidates for LTX. Lung-volume reduction surgery can allow the postponement of LTX for up to 4 to 5 years and does not impair the chances for a subsequent successful LTX.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Emphysema is a progressive, debilitating disease associated with a high rate of morbidity and mortality as a result of respiratory failure. Medical therapy and pulmonary rehabilitation are useful palliative measures and can temporarily improve symptoms. However, they do not alter the natural history of the disease. End-stage emphysema markedly limits the quality of life and survival of patients. Two surgical procedures are currently offered at this stage of the disease: lung-volume reduction surgery (LVRS) or lung transplantation (LTX).

In recent years, several prospective single-center studies as well as randomized controlled trials have demonstrated that LVRS can improve lung function, exercise capacity, and quality of life up to 5 years in selected patients with advanced emphysema [1–9]. The maximum of functional improvement was observed at 3 to 6 months postoperatively and declined progressively thereafter [1, 3, 5, 8, 10]. The indication for LVRS in comparison to LTX differs in various aspects. Lung-volume reduction surgery candidates suffer usually from less-advanced disease than lung transplant candidates with particularly no relevant pulmonary hypertension or severe impairment of gas exchange, and no suppurative bronchiectasis, other chronic lung inflammation or pleural scarring. On the other hand, LTX is offered but to biologically younger patients with an age up to approximately 65 years. However, there is a subset of patients who at the time of presentation may be candidates for either procedure. In these patients, it is important to choose the surgical therapy that is most likely to offer the best opportunity for survival and the best quality of life. Furthermore, LVRS has the potential to postpone transplantation but rarely replaces it.

In this study, we prospectively analyzed the degree and duration of improvement in lung function and gain in quality of life in patients with end-stage emphysema who underwent LVRS but were potentially eligible for transplantation as well. Furthermore we investigated the impact of LVRS on the peritransplant and posttransplant course in patients who underwent LTX after LVRS.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Patient Population
Two hundred sixteen patients underwent LVRS between 1994 and 2005 within our prospective study protocol [1]. From these patients, 58 were potential candidates for LTX at the time of LVRS (age younger than 65 years, forced expiratory volume in 1 second less than 25% of predicted value). There were 32 male and 26 female patients, and the mean age was 57 years (range, 38 to 65 years). The other 158 patients (97 male, 61 female, mean age, 67 years [range, 42 to 79 years]) who underwent LVRS fulfilled the selection criteria for this procedure, but were older or had a milder obstructive disease (forced expiratory volume in 1 second greater than 25%) than the 58 patients previously described or had a contraindication for transplantation. During the same period, 31 patients underwent primary LTX for end-stage emphysema, including 21 male and 10 female patients, with a mean age of 52 years (range, 31 to 66 years).

As described previously [1], the patients selected for LVRS had nonbullous pulmonary emphysema, were severely symptomatic despite optimal medical therapy, had severe airflow obstruction (forced expiratory volume in 1 second of less than 40% of predicted value), and had pulmonary hyperinflation (residual volume of greater than 200% of predicted value, residual volume to total lung capacity of greater than 0.60). Severely impaired carbon monoxide diffusing capacity (less than 20% of predicted) in the presence of homogeneous distribution of emphysema was a major exclusion criterion for LVRS. Patients with coronary artery disease were not included in this analysis. No systematic rehabilitation was performed at our center before the operation, but the majority of patients had undergone rehabilitation at other institutions before referral.

The study was approved by the hospital ethics committee, and informed consent was obtained from all patients.

Surgical Approach
Lung-volume reduction surgery was performed by means of video-assisted, bilateral stapled resection of approximately 30% of lung volume according to the protocol of the previously described study [1]. Target areas were identified on the basis of the analysis of the computed tomographic scans and perfusion scintigraphies as the lung regions with the most pronounced emphysematous alteration and the greatest reduction in perfusion. For patients with homogeneous disease, the resection was performed in the upper lobes. Patients were operated on in the supine position if resection in the upper lobes was planned. For lower lobe resections, patients were placed in a lateral decubitus position and turned to the other side after completion of the first side. At the end of the operation, chest tubes were placed with suction of 5 to 10 cm H₂O.

Measurements
Spirometry, whole-body plethysmography, and measurement of carbon monoxide diffusing capacity were performed according to standard criteria after inhalation of two puffs of albuterol [11]. Severity of dyspnea was graded according to the American Thoracic Society modified Medical Research Council (MRC) dyspnea score, with a scale ranging from 0 to 4 [12]. For assessment of the 6-minute walking distance, the patients walked along the same hospital hallway without supplemental oxygen. Baseline and follow-up examinations were performed within 1 month before LVRS, at 3 and 6 months after LVRS, and every 6 months thereafter. Lung function tests after LTX were performed every 6 weeks in the first 6 months and then at 3 to 6 months thereafter.

Data Analysis and Statistics
Descriptive statistics were expressed as mean ± standard deviation. Comparisons of continuous factors were made using Fisher's exact test. Comparisons of continuous factors were made using the Wilcoxon test with subsequent Bonferroni's correction. A probability value of p less than 0.05 was considered significant.

Survival analysis was calculated for those patients who underwent LVRS and were potential candidates for LTX at the time of LVRS and those patients who underwent primary LTX during the same period. Survival rates were computed using the Kaplan–Meier method and were compared using the log-rank test.

	Results

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Between 1994 and 2005, 216 LVRS procedures were performed at our institution within our prospective study protocol. One hundred fifty-eight patients fulfilled the inclusion criteria for LVRS only (LVRS group), and 58 patients were also potentially suitable for transplantation at the time of evaluation (age younger than 65 years, forced expiratory volume in 1 second less than 25% of predicted value; LVRS/LTX group). Morphology of emphysema as defined previously [1] was markedly heterogeneous, intermediately heterogeneous, and homogeneous in 72 (46%), 56 (35%), and 30 (19%) patients of the LVRS group and in 27 (47%), 18 (31%), and 13 (22%) patients of the LVRS/LTX group, respectively. During follow-up, LTX was performed in 8 patients of the LVRS/LTX group, including 5 men and 3 women, with a mean age of 55 years (range, 50 to 60 years; LVRS/LTXa group). Of these, 4 patients had severe ₁-antitrypsin deficiency. ₁-Antitrypsin deficiency was documented in 5 of 158 (3%) patients of the LVRS group, in 6 of 50 (12%) patients of the LVRS/LTX group, in 4 of 8 (50%) of the patients undergoing transplantation in the LVRS/LTXa group, and in 10 of 31 (32%) patients of the primary LTX group.

The morphologic type of emphysema in these 8 patients who underwent LTX after LVRS was markedly heterogeneous in 4 patients (2 with ₁-antitrypsin deficiency), intermediately heterogeneous in 2 patients (2 with ₁-antitrypsin deficiency), and homogeneous in 2 patients. During the same interval, 31 LTXs were primarily performed in patients with end-stage emphysema (LTX group).

Table 1 summarizes the baseline preoperative functional variables in the different groups of patients according to the type of surgical treatment (LVRS or LTX). The 8 patients of the LVRS/LTX group who underwent LTX secondarily had comparable functional variables to those of the other LVRS/LTX patients. Additionally, no difference was observed between these 8 patients as they were listed for transplantation and the patients who primarily underwent transplantation (LTX group) with respect to the severity of obstruction, the degree of hyperinflation, and the impairment of diffusion capacity for carbon monoxide.

Lung-volume reduction surgery/lung transplantation group
Eight patients of this group (14%) underwent LTX 3, 12, 18, 36, 48, 54, 54, and 56 months after LVRS owing to progressive worsening of the respiratory function (LVRS/LTXa). The median time between LVRS and transplantation time was 35.1 months (range, 3 to 56 months), and the median time on the waiting list was 2.2 months (range, 7 days to 4.1 months), so that the effective median bridging time between LVRS and LTX was 32.9 months. Median survival time after LTX was 96.5 months after a median follow-up of 66.6 months (interquartile range, 49.2 to 93.0 months). During this follow-up, 4 (50%) patients died as a result of multiorgan failure secondary to septic infection. From the other 50 patients who were potential transplantation candidates at the time of LVRS, 19 (38%) died during a median follow-up of 40 months (interquartile range, 10.4, 65.4 months). Cause of death consisted of respiratory insufficiency in 8 patients, pneumonia in 3 patients, cardiac failure in 2 patients, and mechanical bowel obstruction, liver cirrhosis, and malignant tumor in 1 patient each. In 3 patients, the cause of death could not be determined.

The median survival time in this group of 58 patients was 68.1 months, and more than half of these patients (31 of 58) or 53.4% were still alive and had not undergone transplantation after a median follow-up of 43.7 months (interquartile range, 13.6 to 68.1 months).

Lung transplantation group
In this group of patients, median survival was 118.5 months (95% confidence interval, 57.8 to 131.2 months) after a median follow-up of 39.6 months (interquartile range, 5.7 to 71.6 months). This survival time was not different from the survival time of the 8 patients of the LVRS/LTX group who underwent LTX secondarily (p = 0.9, log-rank test; Fig 1). The median time on the waiting list before LTX was 163 days. Death occurred in 11 of these patients (35%), as a result of pneumonia in 3 patients, septicemia and cytomegalovirus infection in 2 patients, perforated diverticulitis complicated by multiorgan failure in 2 patients, and primary graft failure, lymphoma, and aspergillosis in 1 patient each. In 1 patient, cause of death remained unclear.

View larger version (12K): [in this window] [in a new window]   Fig 1. Kaplan–Meier curves showing survival of 8 potentially transplant-eligible patients after primary lung-volume reduction surgery and secondary lung transplantation (LVRS/LTX; group 1, solid line), of 31 patients who underwent primary lung transplantation (LTX; group 2, dotted line with open squares), and of 50 potential transplant patients who underwent lung-volume reduction surgery only (LVRS; group 3, solid line with filled squares).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
This study demonstrates that in selected patients with end-stage emphysema who are potential candidates for LTX, LVRS can alleviate symptoms and improve lung function and quality of life to a degree that allowed the postponement of transplantation for up to 4 to 5 years. Additionally, primary LVRS had no adverse impact on outcome after LTX and did not influence the patients' candidacy for transplantation.

Chronic obstructive pulmonary disease, particularly lung emphysema, represents the most common indication for LTX and accounts for about 48% of the reported lung transplantations in the International Society for Heart and Lung Transplantation in 2004 [13]. Compared with the international registry, the proportion of patients with emphysema who underwent LTX at our institution during the last few years was only 26%. This may be related to the fact that LVRS was investigated in our institution in a prospective study by the same multidisciplinary and dedicated team for the last 10 years. Lung-volume reduction surgery has been demonstrated to improve lung function and quality of life and therefore could be a possible alternative to LTX for selected patients with severe emphysema [1, 14]. Based on our favorable experience, we offered LVRS to suitable candidates as an alternative option to LTX whenever possible. The observation that only a minority (13%) of the patients initially eligible for both LVRS and LTX needed transplantation and that more than 50% of the patients of this group were still alive after a median follow-up of 43.7 months demonstrates the value of LVRS as alternative therapy to LTX in selected patients. Functional improvement and long-term effect after LVRS of these patients was comparable with that of patients of the LVRS group, who generally had a milder disease at the onset of treatment.

Lung transplantation provides greater and longer functional improvement than LVRS, but this improvement offered by transplantation must be balanced against the lifelong need for immunosuppression and the continued risk of infection and chronic rejection. In the majority of patients with severe emphysema in whom no further improvement of lung function can be reached by means of conservative medical therapy, the choice between LVRS and LTX is obvious, based on different selection criteria. However, the decision-making in patients who are initially both LVRS and LTX candidates might be more difficult.

An additional issue that we attempted to address in this study was whether LVRS has a negative impact on the postoperative course of lung transplantation patients either because of the overall physical situation by delaying the time of transplantation or because of previous surgery.

Patients who underwent primary LTX did not differ from those who underwent delayed LTX after a median time of 32.9 months after LVRS in disease severity (pulmonary function) at the time of listing. This shows that after the functional benefit of LVRS has faded, patients remained suitable lung transplantation candidates. Additionally, we did not observe a higher perioperative risk in terms of excess bleeding caused by severe adhesions, phrenic nerve palsy, intubation time, and mean stay in the intensive care unit in patients with a history of LVRS, which confirms previous observations [15, 16]. Further supportive evidence of a comparable prognosis is the similarity in long-term outcome after transplantation, with a median survival of 96.5 months in the LVRS/LTXa patients and of 118.5 months in the LTX patients. A comparable survival between these two groups of patients was already observed, but the average posttransplant survival and the follow-up time were 31.8 months and 34 months, respectively, shorter than in our study [15]. Caution is needed in the interpretation of these results because of the relatively small sample size of the LVRS/LTXa group. Indeed, the strategy considering the primary use of LVRS in patients potentially eligible for LTX may provide definitive therapy for a few patients, but act as a temporary treatment or a bridge to transplantation for others, thereby permitting better rationalization of the scarce donor organ pool to sicker patients for whom transplants may offer the only chance for survival, thereby decreasing the attendant waiting period. The median bridging time from LVRS to LTX in our study was 32.9 months, which is longer than in the series of 15 patients published by Wisser and colleagues [16] (19.6 months) and comparable with the results observed by Burns and associates [15] and Zenati and coworkers [17] (27.4 months). Not surprisingly it was shown that bilateral LVRS had even a greater impact on extending the time to transplantation in comparison with the unilateral procedure, which supports our policy of performing bilateral LVRS in almost all of the patients with equal distribution of emphysema.

Finally, our mid-term and long-term functional results after LVRS confirmed the observations of other authors that LVRS in selected patients with chronic obstructive pulmonary disease might bring patients to improved physical condition at the time of transplantation [15, 16, 18, 19]. This might reduce the mortality on the waiting list in patients with delayed deterioration of the lung function. In our series, of the 3 patients who underwent transplantation within 2 years after LVRS, 2 of them suffered from ₁-antitrypsin deficiency. However, 2 other patients with this disease benefited from prolonged improvement in their quality of life and underwent transplantation 36 and 54 months after initial LVRS.

Our results emphasized the previous observation regarding the impact of the emphysema morphology on outcome [1, 20]. In the 58 patients who were potential candidates for LTX at the time of LVRS, long-term improvement of lung function, exercise capacity, and quality of life occurred up to 4 years, not only in patients with markedly heterogeneous emphysema but also in patients with intermediately heterogeneous and homogeneous emphysema. Indeed, of the 13 patients with homogeneous distribution of emphysema, only 2 underwent LTX secondarily, 36 and 54 months after LVRS.

In conclusion, our results confirm the effectiveness of the LVRS as a procedure that can delay the need for LTX. The primary use of LVRS in patients potentially suitable for transplantation does not impair the chances for a subsequent successful transplantation and its outcome.

	Discussion

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
DR DANIEL MILLER (Atlanta, GA): Were there any conditions that you could predict that would signify those 8 that deteriorate, such as ₁-antitrypsin deficiency? Also, too, I know that in your group, Walter has always done a high percentage of homogeneous disease, and out of those 8 patients, 3 of them were homogeneous and 4 were intermediate, and I just wondered if you went back and looked to see if there was any correlation in regards to a radiologic evaluation and also with regards to ₁-antitrypsin deficiency.

DR TUTIC: Yes, you are right. The patients who underwent lung transplantation, they had not a very favorable emphysema distribution, and this is one of the reasons why they underwent lung transplantation. They had also less good improvement in their lung function and in their dyspnea score, and half of them had an ₁-antitrypsin deficiency.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
This study was supported by the Swiss National Science Foundation (grant 3200–04 3358; 95.1) and the Sonnenwiese Stiftung.

	References

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 

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15. Burns KEA, Keenan RJ, Grgurich WF, Manzetti JD, Zenati MA. Outcomes of lung volume reduction surgery followed by lung transplantationa matched cohort study. Ann Thorac Surg 2002;73:1587-1593.[Abstract/Free Full Text]
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