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Original Research: COPD |

The BODE Index After Lung Volume Reduction Surgery Correlates With Survival* FREE TO VIEW

Stephan Imfeld, PhD, MD; Konrad E. Bloch, MD, FCCP; Walter Weder, MD; Erich W. Russi, MD, FCCP
Author and Funding Information

*From the Pulmonary Division (Drs. Imfeld, Bloch, and Russi) and Division of Thoracic Surgery (Dr. Weder), University Hospital, Zurich, Switzerland.

Correspondence to: Erich W. Russi, MD, FCCP, Pulmonary Division, University Hospital, Raemistr. 100, CH-8091 Zürich, Switzerland; e-mail: erich.russi@usz.ch



Chest. 2006;129(4):873-878. doi:10.1378/chest.129.4.873
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Published online

Study objective: A recently introduced, multidimensional index called BODE (body mass index [BMI], degree of airflow obstruction assessed by spirometry, grade of dyspnea, and exercise capacity), quantified by 6-min walking distance (6MWD), has excellent predictive power with respect to outcome in COPD. We investigated whether the BODE index is able to predict survival after lung volume reduction surgery (LVRS).

Design: Retrospective study.

Setting: Tertiary university hospital.

Patients: One hundred eight-six COPD patients (76 women) with severe emphysema (mean ± SD age, 64 ± 8 years; mean FEV1, 28 ± 8% of predicted).

Intervention: Bilateral thoracoscopic LVRS.

Measurements and results: BMI, pulmonary function, 6MWD, and the modified Medical Research Council dyspnea score were assessed before and 3 months after LVRS, and the BODE index was calculated. The patients were followed up with respect to survival for a median time of 40 months (range, 3 to 116 months) after surgery. The mean BODE index decreased from 7.2 ± 1.6 preoperatively to 4.0 ± 2.0 at 3 months after LVRS (p < 0.001). The postoperative but not the preoperative BODE correlated with survival, although preoperative patient characteristics were comparable between short-term (< 5 years) and long-term (> 5 years) survivors. A decrease to a lower BODE score class was associated with a reduced mortality (hazard ratio, 0.497, 95% confidence interval, 0.375 to 0.659; p < 0.001). The C statistic for the ability of the BODE index to predict the risk of death was larger (0.74) than that for the FEV1 (0.63), the degree of dyspnea (0.64), or the 6MWD (0.62).

Conclusions: The postoperative BODE index is a powerful predictor of survival in COPD patients after LVRS.

Figures in this Article

COPD is one of the most prevalent causes of premature death.1It has a relentless, progressive course and impairs quality of life by shortness of breath related to poorly reversible airflow obstruction, and by recurrent exacerbations. The degree of airflow obstruction, assessed by spirometry, has been extensively studied as a mortality risk factor and shown to correlate with survival.24

Age, hypoxemia,56 pulmonary hypertension,7and features that reflect the systemic manifestation of COPD, namely body weight or body mass index (BMI),8breathlessness,9and impaired exercise capacity,1011 have been shown to correlate with the survival of patients. Recently, Celli et al12 found that a comprehensive multidimensional index, the BODE index (BMI, degree of airflow obstruction assessed by spirometry, grade of dyspnea, and exercise capacity) predicted the risk of death more accurately than any of the individual components alone.

Smoking cessation13 and long-term oxygen therapy in hypoxemic COPD patients56 have been shown to prolong life. In contrast, for treatments such as inhalation of bronchodilators,13corticosteroids,14and intermittent positive pressure breathing,1516 modification of survival has not been demonstrated. Other measures, specifically pulmonary rehabilitation or lung transplantation, have not been studied in randomized prospective trials with respect to their impact on survival.

The effect of lung volume reduction surgery (LVRS) on survival in patients with advanced emphysema remains uncertain. In a retrospective study,17the outcome of 22 candidates for LVRS denied operation by their insurance companies were compared with 65 contemporaneous and comparable volume reduction recipients. During a follow-up of 2 years, patients denied operation had a progressive worsening of their function, whereas patients after LVRS had sustained improvement. Absolute survival was 82% for the surgical group and 64% for the medical group. A post hoc analysis of the National Emphysema Treatment Trial (NETT)18 has suggested that LVRS may improve survival in selected patients with a low exercise capacity with advanced emphysema predominantly affecting the upper lobes.

Since LVRS modifies at least three of the four determinants of the BODE index, ie, dyspnea, FEV1, and walking distance shortly after the intervention, we reasoned that changes in the BODE index occurring within 3 months after LVRS could serve as a measure of treatment success and would correlate with the survival in patients with COPD undergoing this intervention. To tests our hypotheses, we calculated the BODE index in a cohort of patients before and at 3 months after LVRS, and followed their survival over several years.

Patients

Between 1994 and 2004, 194 consecutive, severely symptomatic patients with advanced pulmonary emphysema were enrolled in a prospective trial on LVRS outcome. The study was approved by the ethical committee of our hospital. Patients were selected for LVRS according to previously published criteria.19 Briefly, symptomatic COPD patients (modified Medical Research Council [MMRC] dyspnea score ≥ grade 2), with severe airflow obstruction and hyperinflation (FEV1 < 40% of predicted, total lung capacity [TLC] > 120% of predicted), and evidence of severe pulmonary emphysema were considered candidates for LVRS. Emphysema distribution did not have to be upper-lobe predominant, and patients with homogeneous emphysema types were also included. An extremely low functional reserve (FEV1 < 20% predicted) in combination with a diffusing capacity < 20% predicted, CT evidence of very advanced pulmonary parenchymal destruction (“vanished lung”), and comorbidities likely to entail an unacceptable perioperative mortality, such as symptomatic cardiovascular disease, or to affect survival, such as malignant disorders, were exclusion criteria.

Measurements

Bilateral LVRS was performed by video-assisted thoracoscopy. All measurements were performed within 1 month before LVRS, after 3 months, at 6 months, and then at half-annual intervals. Information on survival was obtained from physicians involved in the long-term care of the patients.

Pulmonary Function:

Spirometry and measurements of thoracic gas volumes were measured 10 min after inhalation of two puffs of salbutamol with a mass flowmeter and a body plethysmograph (6200 Autobox; SensorMedics; Yorba Linda, CA). Diffusing capacity of the lung for carbon monoxide was measured with an infrared analyzer (model 66200; SensorMedics) that uses methane as inert tracer gas. Criteria for acceptability and reproducibility and predicted normal values were according to the European Community of Coal and Steel.20Dyspnea was rated with the American Thoracic Society MMRC dyspnea score.21

Six-Minute Walking Distance:

The patients walked in the same hospital hallway without oxygen supplementation encouraged by a technician.2224

BODE indexes were calculated as the sum score proposed by Celli et al,12 based on the following four variables: (1) FEV1 percentage of predicted (≥ 65%, score 0; 50 to 64%, score 1; 36 to 49%, score 2; and ≤ 35%, score 3); (2) 6-min walking distance (6MWD) [≥ 350 m, score 0; 250 to 349 m, score 1; 150 to 249 m, score 2; ≤ 149 m, score 3]; (3) MMRC dyspnea score (0 to 1, score 0; 2, score 1; 3, score 2; and 4, score 3); and (4) BMI (> 21 kg/m2, score 0; ≤ 21 kg/m2, score 1). Scores may range from 0 to 10.

Statistical Analysis

Data are expressed as mean ± SD. Differences between groups were evaluated by the Mann-Whitney U test. Survival was analyzed by Kaplan-Meier curves with log-rank tests and Cox proportional-hazard regression models. In order to determine whether the BODE index is a more powerful predictor of survival than each of its components alone, we calculated C statistics.25

Of the 194 patients, 5 died within 30 days after the operation; hence, perioperative mortality was 2.6%. One patient underwent lung transplantation after 37 days, and two patients died before the 3-month follow-up at 45 days and 93 days after LVRS, respectively. Therefore, data from 186 patients (76 women) with a mean ± SD age of 63.8 ± 8.2 years were used for the subsequent analyses. Table 1 gives an overview on the preoperative characteristics of the study population.

We were able to trace all patients with respect to survival. Median follow-up was 40 months (range, 3 to 116 months). Eight patients died within the first year after LVRS, 77 died subsequently, and 9 patients underwent lung transplantation after a median of 43.0 months (range, 12 to 67.5 months) after LVRS.

Three months after LVRS, we found relevant symptomatic and functional improvements (Table 2 ). Dyspnea decreased considerably: the mean MMRC dyspnea score decreased from 3.5 ± 0.7 to 1.6 ± 0.99 (p < 0.001), the FEV1 increased by 47% from 0.74 ± 0.22 L (27.7 ± 7.8% predicted) to 1.09 ± 0.43 L (40.3 ± 12.9% predicted, p < 0.001), and the 6MWD improved from 258 ± 103 to 345 ± 97 m (p < 0.001). Within 3 months postoperatively, the mean weight of the patients and, hence, their BMI remained unchanged: 22.0 ± 3.8 kg/m2 vs 22.2 ± 3.7 kg/m2.

The preoperative distribution of the BODE index illustrates the severity of COPD of our study population (black bars in Fig 1 ). The functional improvement after LVRS is reflected in a decrease of the mean BODE index from 7.2 ± 1.6 preoperatively to 4.0 ± 2.0 at 3 months after LVRS (p < 0.001), and results in an impressive shift of the scores to the left (white bars).

We arbitrarily defined patients surviving > 5 years after LVRS as long-term survivors, and patients who died within 5 years after LVRS as short-term survivors. These two groups of patients did not differ with respect to preoperative characteristics, except that the degree of pulmonary hyperinflation as assessed by the residual volume to TLC ratio and mean age were somewhat lower in patients who lived longer (Table 1).

Within 3 months after surgery, long-term survivors experienced greater improvements in FEV1 and dyspnea, and had a larger 6MWD than short-term survivors. As a result, the BODE index within 3 months after LVRS decreased to a greater degree in patients surviving for > 5 years than in those who died within 5 years (Table 2).

Preoperative BODE scores did not predict survival after LVRS (hazard ratio, 1.366; 95% confidence interval [CI], 0.934 to 1.998; p > 0.1). In contrast, postoperative BODE scores were significantly correlated with survival: a decrease to a lower BODE score class was associated with a reduced mortality (hazard ratio, 0.497; 95% CI, 0.375 to 0.659; p < 0.001). We classified our patients in three groups of increasing severity with the following BODE score boundaries (approximate lowest and highest quartiles, and quartiles in-between): group 1, 0 to 25th percentile (score 0 to 2, n = 43); group 2, > 25 to 75th percentile (score 3 to 5, n = 106); group 3, > 75th percentile (score 6 to 10, n = 37), and calculated their survival according to Kaplan-Meier (Fig 2 ). A change to a lower BODE score group was associated with a reduced mortality (hazard ratio, 0.419; 95% CI, 0.303 to 0.581; p < 0.001). The estimated survival of group 1 consisting of patients with postoperative BODE indexes within the highest quartile (ie, 0 to 2) was > 90% at 5 years after the operation. The C statistic for the ability of the BODE index to predict the risk of death was larger (0.74) than that for the FEV1 (0.63), the degree of dyspnea (0.64), or the 6MWD (0.62) alone.

Our data demonstrate that the BODE index assessed 3 months after LVRS but not its preoperative value predicts long-term survival in patients with advanced COPD. Therefore, this index might be useful for assessment of the prognosis and response to treatment in COPD. Celli et al12 have shown that a multidimensional grading system incorporating BMI, airflow obstruction, dyspnea, and exercise capacity predicts the risk of death in patients with COPD treated conservatively more reliably than any of its individual components alone.

Our study population consists of typical candidates for LVRS with advanced COPD. This is reflected by a mean BODE index of 7.2, which is higher than the mean score of 4.3 in the population of Celli et al,12 who reported a patient population with a wider COPD severity range. The lack of a correlation between the preoperative BODE index and survival of our operated patients may also be related to differences in the design of our study and that reported by Celli et al.12 Their multicenter study population consisted of 859 outpatients recruited from clinics in the United States, Spain, and Venezuela, receiving standard conservative care for COPD. In contrast, our patients underwent a surgical intervention that not only improved their dyspnea, lung function, and exercise performance but may also have improved survival as suggested recently by the NETT (upper-lobe predominant emphysema with low exercise capacity group)18 and as corroborated by our data.

Shortly after the introduction of LVRS by Cooper et al,26 many centers worldwide started to offer this type of palliative surgery and reported mortality rates ranging from 2.5 to 16%.18,2728 In the NETT, a subset of 69 patients with an FEV1 ≤ 20% of predicted, and either a homogeneous emphysema or a carbon monoxide diffusing capacity ≤ 20% of predicted, had a 30-day postoperative mortality of 16%, as compared with a rate of 0% among 70 medically treated patients.,28 From the start of our LVRS program in 1994, we did not consider patients with such low lung function in combination with homogeneous emphysema as candidates for LVRS. This and the fact that patients with cardiovascular diseases associated with an increased perioperative complication rate were not considered suitable for LVRS may explain our perioperative mortality of 2.6%, which is among the lowest reported in the literature.

LVRS improved lung function, dyspnea, and exercise performance to a degree comparable with the results of other large series.18,27,2930 In our entire study population, the BODE index decreased from a mean of 7.2 ± 1.6 preoperatively to 4.0 ± 2.0 at 3 months after LVRS (p < 0.001), which is the result of a change in three of the four parameters. The mean weight of the patients did not increase over 3 months after surgery, and therefore the BMI remained unchanged. However, LVRS had a major impact on dyspnea, walking distance, and FEV1.

We are unable to compare our postsurgical changes of BODE with the findings of other groups, since to our knowledge only cross-sectional data with this novel index have been published,12 and we are the first reporting on changes of BODE due to a therapeutic intervention. A major finding in our study is the correlation between the postoperative BODE and long-term survival, ie, that the decrease to a lower BODE score class after LVRS was associated with a reduced mortality compared to patients without or only marginal changes in BODE indexes.

Patients with a lower postoperative BODE index had a longer survival. In the NETT, LVRS increased the chance of improved exercise capacity but did not confer an overall survival advantage over medical therapy.18 However, a subgroup of patients with predominantly upper-lobe emphysema and low exercise capacity, ie, a maximal workload of 25 W in women and 40 W in men, had a mortality that was lower in the surgery group than in the medical therapy group (risk ratio for death, 0.47; p = 0.005).

Our follow-up with respect to patient survival was complete, and the survival analysis was performed using all-cause mortality as the outcome. Considering the inconclusive impact of lung transplantation on the survival of COPD patients,31 the nine patients who underwent transplantation were regarded as survivors. Since deaths occurred in the patients home and postmortem examination was rarely performed in those who died in a hospital, we were unable to discriminate between respiratory and nonrespiratory deaths as done in the study by Celli et al.12

Components of the BODE index can be assessed with broadly available tools, and the BODE index is simple to calculate. Although the BODE has been used as a predictor of the risk of death, our data suggest that it might serve as a useful indicator of disease progression and the clinical response to therapy.

Abbreviations: BMI = body mass index; BODE = body mass index, degree of airflow obstruction assessed by spirometry, grade of dyspnea, and exercise capacity; CI = confidence interval; LVRS = lung volume reduction surgery; MMRC = modified Medical Research Council; NETT = National Emphysema Treatment Trial; TLC = total lung capacity; 6MWD = 6-min walk distance

Supported by grants from the Swiss National Foundation (grant No. 3200–063709.00) and the Zurich Lung League.

Table Graphic Jump Location
Table 1. Preoperative Patient Characteristics*
* 

Data are presented as mean ± SD unless otherwise indicated.

 

Fisher exact test for gender difference between short and long-term survivors.

Table Graphic Jump Location
Table 2. Results at 3 Months After LVRS*
* 

Data are presented as mean ± SD unless otherwise indicated.

 

Δ Denotes difference of 3-month postoperative − preoperative values.

Figure Jump LinkFigure 1. The distribution of BODE indexes after LVRS (white) is centered around lower values than before LVRS (black).Grahic Jump Location
Figure Jump LinkFigure 2. Kaplan-Meier survival curves for the BODE score groups with group limits of BODE 0 to 2 (n = 43), 3 to 5 (n = 106), 6 to 10 (n = 37).Grahic Jump Location
Murray, CJ, Lopez, AD (1997) Mortality by cause for eight regions of the world: Global Burden of Disease Study.Lancet349,1269-1276. [CrossRef] [PubMed]
 
Fletcher, CM, Peto, R, Tinker, C, et al. The natural history of chronic bronchitis and emphysema. 1976; Oxford Press. New York, NY:.
 
Anthonisen, N, Wright, EC, Hodgkin, JE Prognosis in chronic obstructive pulmonary disease.Am Rev Respir Dis1986;133,14-20. [PubMed]
 
Burrows, B Predictors of loss of lung function and mortality in obstructive lung diseases.Eur Respir Rev1991;1,340-345
 
Report of the Medical Research Council Working Party.. Long-term domiciliary oxygen therapy in chronic hypoxic cor pulmonale complicating chronic bronchitis and emphysema.Lancet1981;1,681-685. [PubMed]
 
Nocturnal Oxygen Therapy Trial Group.. Continuous or nocturnal oxygen therapy in hypoxemic chronic obstructive lung disease.Ann Intern Med1980;93,391-398. [PubMed]
 
Weitzenblum, E, Hirth, C, Ducolone, A, et al Prognostic value of pulmonary artery pressure in chronic obstructive pulmonary disease.Thorax1981;36,752-758. [CrossRef] [PubMed]
 
Schols, AM, Slangen, J, Volovics, L, et al Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease.Am J Respir Crit Care Med1998;157,1791-1797. [PubMed]
 
Nishimura, K, Izumi, T, Tsukino, M, et al Dyspnea is a better predictor of 5-year survival than airway obstruction in patients with COPD.Chest2002;121,1434-1440. [CrossRef] [PubMed]
 
Pinto-Plata, VM, Cote, C, Cabral, H, et al The 6-min walk distance: change over time and value as a predictor of survival in severe COPD.Eur Respir J2004;23,28-33. [CrossRef] [PubMed]
 
Oga, T, Nishimura, K, Tsukino, M, et al Analysis of the factors related to mortality in chronic obstructive pulmonary disease: role of exercise capacity and health status.Am J Respir Crit Care Med2003;167,544-549. [CrossRef] [PubMed]
 
Celli, BR, Cote, CG, Marin, JM, et al The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease.N Engl J Med2004;350,1005-1012. [CrossRef] [PubMed]
 
Anthonisen, NR, Skeans, MA, Wise, RA, et al The effects of a smoking cessation intervention on 14.5-year mortality: a randomized clinical trial.Ann Intern Med2005;142,233-239. [PubMed]
 
Fan, VS, Bryson, CL, Curtis, JR, et al Inhaled corticosteroids in chronic obstructive pulmonary disease and risk of death and hospitalization: time-dependent analysis.Am J Respir Crit Care Med2003;168,1488-1494. [CrossRef] [PubMed]
 
Wilson, DO, Rogers, RM, Wright, EC, et al Body weight in chronic obstructive pulmonary disease: the National Institutes of Health Intermittent Positive-Pressure Breathing Trial.Am Rev Respir Dis1989;139,1435-1438. [PubMed]
 
The Intermittent Positive Pressure Breathing Trial Group.. Intermittent positive pressure breathing therapy of chronic obstructive pulmonary disease: a clinical trial.Ann Intern Med1983;99,612-620. [PubMed]
 
Meyers, BF, Yusen, RD, Lefrak, SS, et al Outcome of Medicare patients with emphysema selected for, but denied, a lung volume reduction operation.Ann Thorac Surg1998;66,331-336. [CrossRef] [PubMed]
 
NETT, Trialists A randomized trial comparing lung-volume-reduction surgery with medical therapy for severe emphysema.N Engl J Med2003;348,2059-2073. [CrossRef] [PubMed]
 
Russi, EW, Stammberger, U, Weder, W Lung volume reduction surgery for emphysema.Eur Respir J1997;10,208-218. [CrossRef] [PubMed]
 
ECCS working party.. Standardization of lung function tests.Bull Eur Physiopath Respir1983;19,7-92
 
American Thoracic Society.. Surveillance for respiratory hazards in the occupational setting.Am Rev Respir Dis1982;126,952-956. [PubMed]
 
Bernstein, M, Despars, JA, Singh, NP, et al Reanalysis of the 12-minute walk in patients with chronic obstructive pulmonary disease.Chest1994;105,163-167. [CrossRef] [PubMed]
 
McGavin, CR, Gupta, SP, McHardy, GJR Twelve-minute walking test for assessing disability in chronic bronchitis.BMJ1976;1,822-823. [CrossRef] [PubMed]
 
Butland, RJA, Pang, J, Gross, ER, et al Two-, six-, and 12-minute walking tests in respiratory disease.BMJ1982;284,1607-1608. [CrossRef] [PubMed]
 
Harrell, FE, Jr, Lee, KL, Mark, DB Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors.Stat Med1996;15,361-387. [CrossRef] [PubMed]
 
Cooper, JD, Trulock, EP, Triantafillou, AN, et al Bilateral pneumectomy (volume reduction) for chronic obstructive pulmonary disease.J Thorac Cardiovasc Surg1995;109,106-109. [CrossRef] [PubMed]
 
Ciccone, AM, Meyers, BF, Guthrie, TJ, et al Long-term outcome of bilateral lung volume reduction in 250 consecutive patients with emphysema.J Thorac Cardiovasc Surg2003;125,513-525. [CrossRef] [PubMed]
 
NETT, Trialists Patients at high risk of death after lung-volume-reduction surgery.N Engl J Med2001;345,1075-1083. [CrossRef] [PubMed]
 
Munro, PE, Bailey, MJ, Smith, JA, et al Lung volume reduction surgery in Australia and New Zealand: six years on; registry report.Chest2003;124,1443-1450. [CrossRef] [PubMed]
 
Gelb, AF, McKenna, RJ, Jr, Brenner, M, et al Lung function 5 yr after lung volume reduction surgery for emphysema.Am J Respir Crit Care Med2001;163,1562-1566. [PubMed]
 
Hosenpud, JD, Bennett, L, Keck, BM, et al Effect of diagnosis on survival benefit of lung transplantation for end- stage lung disease.Lancet1998;351,24-27. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1. The distribution of BODE indexes after LVRS (white) is centered around lower values than before LVRS (black).Grahic Jump Location
Figure Jump LinkFigure 2. Kaplan-Meier survival curves for the BODE score groups with group limits of BODE 0 to 2 (n = 43), 3 to 5 (n = 106), 6 to 10 (n = 37).Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Preoperative Patient Characteristics*
* 

Data are presented as mean ± SD unless otherwise indicated.

 

Fisher exact test for gender difference between short and long-term survivors.

Table Graphic Jump Location
Table 2. Results at 3 Months After LVRS*
* 

Data are presented as mean ± SD unless otherwise indicated.

 

Δ Denotes difference of 3-month postoperative − preoperative values.

References

Murray, CJ, Lopez, AD (1997) Mortality by cause for eight regions of the world: Global Burden of Disease Study.Lancet349,1269-1276. [CrossRef] [PubMed]
 
Fletcher, CM, Peto, R, Tinker, C, et al. The natural history of chronic bronchitis and emphysema. 1976; Oxford Press. New York, NY:.
 
Anthonisen, N, Wright, EC, Hodgkin, JE Prognosis in chronic obstructive pulmonary disease.Am Rev Respir Dis1986;133,14-20. [PubMed]
 
Burrows, B Predictors of loss of lung function and mortality in obstructive lung diseases.Eur Respir Rev1991;1,340-345
 
Report of the Medical Research Council Working Party.. Long-term domiciliary oxygen therapy in chronic hypoxic cor pulmonale complicating chronic bronchitis and emphysema.Lancet1981;1,681-685. [PubMed]
 
Nocturnal Oxygen Therapy Trial Group.. Continuous or nocturnal oxygen therapy in hypoxemic chronic obstructive lung disease.Ann Intern Med1980;93,391-398. [PubMed]
 
Weitzenblum, E, Hirth, C, Ducolone, A, et al Prognostic value of pulmonary artery pressure in chronic obstructive pulmonary disease.Thorax1981;36,752-758. [CrossRef] [PubMed]
 
Schols, AM, Slangen, J, Volovics, L, et al Weight loss is a reversible factor in the prognosis of chronic obstructive pulmonary disease.Am J Respir Crit Care Med1998;157,1791-1797. [PubMed]
 
Nishimura, K, Izumi, T, Tsukino, M, et al Dyspnea is a better predictor of 5-year survival than airway obstruction in patients with COPD.Chest2002;121,1434-1440. [CrossRef] [PubMed]
 
Pinto-Plata, VM, Cote, C, Cabral, H, et al The 6-min walk distance: change over time and value as a predictor of survival in severe COPD.Eur Respir J2004;23,28-33. [CrossRef] [PubMed]
 
Oga, T, Nishimura, K, Tsukino, M, et al Analysis of the factors related to mortality in chronic obstructive pulmonary disease: role of exercise capacity and health status.Am J Respir Crit Care Med2003;167,544-549. [CrossRef] [PubMed]
 
Celli, BR, Cote, CG, Marin, JM, et al The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease.N Engl J Med2004;350,1005-1012. [CrossRef] [PubMed]
 
Anthonisen, NR, Skeans, MA, Wise, RA, et al The effects of a smoking cessation intervention on 14.5-year mortality: a randomized clinical trial.Ann Intern Med2005;142,233-239. [PubMed]
 
Fan, VS, Bryson, CL, Curtis, JR, et al Inhaled corticosteroids in chronic obstructive pulmonary disease and risk of death and hospitalization: time-dependent analysis.Am J Respir Crit Care Med2003;168,1488-1494. [CrossRef] [PubMed]
 
Wilson, DO, Rogers, RM, Wright, EC, et al Body weight in chronic obstructive pulmonary disease: the National Institutes of Health Intermittent Positive-Pressure Breathing Trial.Am Rev Respir Dis1989;139,1435-1438. [PubMed]
 
The Intermittent Positive Pressure Breathing Trial Group.. Intermittent positive pressure breathing therapy of chronic obstructive pulmonary disease: a clinical trial.Ann Intern Med1983;99,612-620. [PubMed]
 
Meyers, BF, Yusen, RD, Lefrak, SS, et al Outcome of Medicare patients with emphysema selected for, but denied, a lung volume reduction operation.Ann Thorac Surg1998;66,331-336. [CrossRef] [PubMed]
 
NETT, Trialists A randomized trial comparing lung-volume-reduction surgery with medical therapy for severe emphysema.N Engl J Med2003;348,2059-2073. [CrossRef] [PubMed]
 
Russi, EW, Stammberger, U, Weder, W Lung volume reduction surgery for emphysema.Eur Respir J1997;10,208-218. [CrossRef] [PubMed]
 
ECCS working party.. Standardization of lung function tests.Bull Eur Physiopath Respir1983;19,7-92
 
American Thoracic Society.. Surveillance for respiratory hazards in the occupational setting.Am Rev Respir Dis1982;126,952-956. [PubMed]
 
Bernstein, M, Despars, JA, Singh, NP, et al Reanalysis of the 12-minute walk in patients with chronic obstructive pulmonary disease.Chest1994;105,163-167. [CrossRef] [PubMed]
 
McGavin, CR, Gupta, SP, McHardy, GJR Twelve-minute walking test for assessing disability in chronic bronchitis.BMJ1976;1,822-823. [CrossRef] [PubMed]
 
Butland, RJA, Pang, J, Gross, ER, et al Two-, six-, and 12-minute walking tests in respiratory disease.BMJ1982;284,1607-1608. [CrossRef] [PubMed]
 
Harrell, FE, Jr, Lee, KL, Mark, DB Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors.Stat Med1996;15,361-387. [CrossRef] [PubMed]
 
Cooper, JD, Trulock, EP, Triantafillou, AN, et al Bilateral pneumectomy (volume reduction) for chronic obstructive pulmonary disease.J Thorac Cardiovasc Surg1995;109,106-109. [CrossRef] [PubMed]
 
Ciccone, AM, Meyers, BF, Guthrie, TJ, et al Long-term outcome of bilateral lung volume reduction in 250 consecutive patients with emphysema.J Thorac Cardiovasc Surg2003;125,513-525. [CrossRef] [PubMed]
 
NETT, Trialists Patients at high risk of death after lung-volume-reduction surgery.N Engl J Med2001;345,1075-1083. [CrossRef] [PubMed]
 
Munro, PE, Bailey, MJ, Smith, JA, et al Lung volume reduction surgery in Australia and New Zealand: six years on; registry report.Chest2003;124,1443-1450. [CrossRef] [PubMed]
 
Gelb, AF, McKenna, RJ, Jr, Brenner, M, et al Lung function 5 yr after lung volume reduction surgery for emphysema.Am J Respir Crit Care Med2001;163,1562-1566. [PubMed]
 
Hosenpud, JD, Bennett, L, Keck, BM, et al Effect of diagnosis on survival benefit of lung transplantation for end- stage lung disease.Lancet1998;351,24-27. [CrossRef] [PubMed]
 
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