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Sustained Improvements in Dyspnea and Pulmonary Function 3 to 5 Years After Lung Volume Reduction Surgery^*

^* From the Departments of Medicine (Ms. Appleton, and Drs. Adams and Ruffin) and Surgery (Mr. Peacock), University of Adelaide, The Queen Elizabeth Hospital Campus, Woodville, SA, Australia; private practice (Dr. Porter), Adelaide, SA, Australia.

Correspondence to: Robert Adams, MBBS, MD, Department of Medicine, The Queen Elizabeth Hospital, 28 Woodville Rd, Woodville, SA, Australia 5011; e-mail: robert.adams{at}nwahs.sa.gov.au

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Objectives: To determine long-term survival rates of patients who underwent lung volume reduction surgery (LVRS) for emphysema and the factors associated with longer survival, and to evaluate levels of perceived dyspnea and health-related quality of life (HRQL) after a follow-up period of 3 to 5.5 years.

Design: Retrospective observational study.

Setting: Academic medical center

Methods: Telephone and postal surveys were used to obtain patient dyspnea scores and HRQL scores. Hospital databases and state registries were searched to determine patient survival and pulmonary function.

Results: Of 54 patients undergoing LVRS, 29 patients (18 men and 11 women) were available for follow-up, which ranged from 36 to 66 months (mean ± SE, 51 ± 1.5 months). There was significant sustained improvement in modified Medical Research Council scores compared to pre-LVRS: 2.19 ± 0.19 vs 2.88 ± 0.14 (p = 0.0000). Eleven of 22 patients demonstrated an increase in all three Mahler baseline dyspnea index grades of at least one level. Baseline body mass index (BMI) and post-LVRS length of stay (LOS) were significantly associated with survival: survivor vs deceased baseline BMI, 24.2 ± 0.6 vs 21.4 ± 0.5 (p = 0.002), and post-LVRS LOS, 15.4 ± 1.7 days vs 28.7 ± 5.3 days (p = 0.015). Compared to pre-LVRS, 20 patients with mean follow-up time of 45 months demonstrated significant sustained improvements in FEV₁ percentage of predicted (31.4 ± 2.1% vs 39.8 ± 3.5%, p = 0.038), total lung capacity percentage of predicted (136 ± 4% vs 122 ± 3%, p = 0.0004), and residual volume percentage of predicted (237 ± 14% vs 172 ± 11%, p = 0.0001). Patient HRQL measured using the Dartmouth Primary Care Co-operative Quality of Life questionnaire was more favorable than that reported in aged-care settings. Caregiver burden scale scores indicate caring for a recipient of LVRS carries similar burden to that for caring for individuals with other chronic illnesses.

Conclusions: In this population, a majority of the LVRS patients survived for ≥ 3 years. Among survivors, dyspnea and lung function benefits were seen. Baseline BMI and postoperative LOS were significantly associated with survival.

Key Words: emphysema • lung diseases, obstructive • lung volume reduction surgery

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Lung volume reduction surgery (LVRS) was reintroduced as a means of improving outcomes for patients with severe COPD; however, little information is available regarding outcomes beyond the 3-year postoperative period. In one study¹ with follow-up of 26 LVRS patients at 4 years, benefits remained in only 20% of patients. Other reports^{2 3} suggest that although absolute benefits persist at 3 years relative to presurgical levels, there is a progressive decline in lung function parameters, exercise tolerance, and increasing oxygen dependence as the time from surgery lengthens. Compared to standard medical care, LVRS has been shown to offer a significant survival benefit after 24 months of follow-up (82% vs 64%).⁴ Available short-term data from randomized controlled trials indicate LVRS improves lung function, walk distance, and health-related quality of life (HRQL) compared to usual medical care,⁵ and pulmonary rehabilitation.⁶

Few studies of LVRS have considered HRQL,^{6 7 8} particularly disease-specific quality of life.^{9 10} These end points are important because care in late-stage COPD can be considered as essentially palliative.

We have previously reported¹¹ the short-term effectiveness of LVRS in a cohort of 54 patients, with a median follow-up of 788 days, and demonstrated significant improvements in lung function and 6-min walk distance, and an appreciable mortality rate of 14.8% at 90 days after surgery. These results were consistent with previous reports.^{12 13 14}

The aim of this study was to determine longer-term mortality data after LVRS, and to examine what factors are associated with longer survival. We also sought to determine what qualitative benefits are sustained after a follow-up period in the range of 3 to 5.5 years, in terms of perceived dyspnea and HRQL of patients and their caregivers.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Patient Selection
Fifty-four patients underwent LVRS at The Queen Elizabeth Hospital in Adelaide, South Australia, between 1996 and 1997.¹¹ Of 30 surviving patients, 29 patients were available for follow-up in this study. One patient could not be contacted, and this patient’s survival status was confirmed by a search of the state death registry. The criteria¹¹ for LVRS eligibility satisfied by all LRVS recipients in this study are listed in Table 1 .

Study Design
This study was conducted using a telephone survey. Survival status was ascertained by searching the institutional patient record database and the state death registry. Letters explaining the purpose of the study were mailed to all subjects, inviting their participation. All patients were telephoned over a 3-week period to obtain informed consent, and dyspnea was graded at that time. HRQL questionnaires were mailed out for self-administration by patients and their caregivers, where present.

Dyspnea
Dyspnea was graded using two scales. Firstly, the modified Medical Research Council (MRC) dyspnea scale was used. This is scored on a 5-point scale from 0 to 4, where grade 0 describes the subject as "not troubled by shortness of breath except with strenuous exercise," and grade 4 describes the subject as "too breathless to leave the house or breathless when dressing or undressing."¹⁵ The second scale used was the Mahler baseline dyspnea index (BDI). The Mahler BDI is a multidimensional grading of dyspnea, using the categories of "functional impairment," "magnitude of task," and "magnitude of effort" on a scale of 0 to 4, where 4 represents best and 0 represents worst.¹⁶ The BDI was used to determine current dyspnea (36 to 65 months after LVRS) in preference to the transition dyspnea index because there was a substantial risk of subject recall bias in evaluating change compared to shortly after the procedure. All assessments of patient dyspnea were conducted by the same person to eliminate interobserver error.

Post-LVRS HRQL
HRQL was assessed using the Dartmouth Primary Care Co-operative Quality of Life questionnaire (COOP),¹⁷ modified for use in COPD, as previously reported.¹⁸ The modifications were made so as to avoid floor effects and permit potential deteriorations in condition to be detected. Two changes were made to the original questionnaire: firstly, a supplementary item specifically related to dyspnea was added (When do you become short of breath? Extreme effort [walking up a steep hill/jog at slow pace], moderate effort [walking up stairs/easy digging in garden], little effort [walking on a level surface at regular pace], very little effort [walk at slow pace/washing dishes], and at rest [sitting or lying down]). Secondly, in order to more appropriately relate to the level of activity of patients with severe COPD, the item regarding physical condition (What is the most strenuous level of activity you can do for 2 min?) was altered by deleting the "heavy" category (jog at fast pace) and adding an "extremely light" category (eating, getting out of bed). The remaining eight items refer to the emotional and overall condition and how these impact on the ability to perform daily and social activities, and the perception of pain and change in condition. The COOP questionnaire features a simple graphical layout, has documented reliability and validity in a range of settings including respiratory disease,^{19 20} and was selected in view of the level of morbidity of the subjects to be enrolled. High COOP scores indicate lower perceptions of HRQL.

Caregiver Burden
To determine the caregiver burden associated with caring for a patient who has undergone LVRS, the caregivers completed the Caregiver Burden Scale, which has proven validity and reliability in chronic illness.²¹

Pulmonary Function
Lung function data were obtained on survivors from The Queen Elizabeth Hospital’s Pulmonary Function Laboratory database. Patient data were only included in the analysis if the follow-up time was > 2 years. The data of four subjects were excluded because the follow-up on lung function data was available for < 2 years.

Statistical Analysis
Data are provided as mean ± SE. Differences between pre-LVRS and follow-up respiratory parameters and outcomes were analyzed using paired and unpaired t tests. Preoperative and postoperative dichotomous variables and outcomes that were used as predictors of mortality were analyzed for statistical significance using the Pearson ² test. All p values were considered significant if < 0.05. Kaplan-Meier survival analysis was performed to determine survival probability, and Cox proportional hazards models were used to determine preoperative and postoperative factors influencing long-term survival. Institutional ethics committee approval was obtained for this study.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Baseline characteristics of the 54 LVRS recipients are shown in Table 2 . As previously reported,¹¹ no deaths occurred in the first 2 postoperative weeks. Perioperative mortality was 5.5% (3 of 54 patients) at 30 days, 14.8% (8 of 54 patients) at 90 days, and 25.9% (14 of 54 patients) at the median follow-up time of 788 days. A homogeneous pattern on perfusion Q scan significantly correlated with mortality (p = 0.007). The underlying pathology in those who died included ischemic heart disease (n = 5), cardiac failure/arrhythmia (n = 5), respiratory failure associated with sputum retention or failure to re-expand (n = 6), and probable pneumonia (n = 8). Of note, one patient died (electromechanical dissociation/ARDS) and two patients required urgent treatment following tension pneumothorax occurring at least 4 days after removal of drains on that side. Another death was precipitated by major postoperative air leaks in the only patient in whom surgery was complicated by excessive pleural adhesions that proved to be densely adherent, on the basis of asbestos pleuritis.

Twenty-nine of 30 surviving patients who underwent LVRS were available for follow-up with the survey. Median duration of survivor follow-up was 49 months (range, 36 to 66 months).

Table 3 shows the mean modified MRC scale and Mahler BDI scores for all patients prior to LVRS and for the survivors at baseline and follow-up. There was a statistically significant reduction in dyspnea for survivors at follow-up compared to baseline (p ≤ 0.01). Among survivors, 58% (15 of 26 patients) improved at least one level on the modified MRC scale, and 50% (11 of 22 patients) improved by more than one level in all three scales of the Mahler BDI, compared to their baseline values. When dyspnea benefits were considered as a proportion of all subjects undergoing LVRS and not just the survivor fraction, 27.8% and 20.4% of all subjects experienced ongoing reductions in dyspnea according to the MRC scale and Mahler BDI scores, respectively.

Table 5 shows results for patient HRQL as measured by the COOP charts, and for caregiver burden, as measured using the Caregiver Burden Scale. Patient COOP scores and Caregiver Burden Scale scores were not significantly correlated with each other. No significant relationship was demonstrated between the level of patient support and postsurgical mortality (Pearson ² = 1.39, p = 0.71).

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Kaplan-Meier survival curve for LVRS.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
We have reported data on 54 patients followed up for up to 5.5 years after LVRS. Among the survivors, LVRS has resulted in significant ongoing reductions in dyspnea. At least 50% of surviving patients experienced ongoing relief of dyspnea compared to presurgery levels on both dyspnea scales used. Of the 55% of patients surviving, all mean pulmonary function parameters were significantly improved at 2 years after surgery compared to their best pre-LVRS values. This continued beyond 3 years, except for absolute FEV₁ and FVC. Of the preoperative patient physical parameters, only a higher mean BMI was significantly associated with long-term survival. Severely impaired preoperative exercise tolerance, which was demonstrated to be significantly associated with 90-day mortality, did not influence long-term survival. Consistent with the majority of the LVRS literature, none of the preoperative respiratory parameters predicted long-term survival. Only one postoperative variable, mean LOS, was significantly associated with short- and long-term survival. Although, postoperative pneumonia was significantly associated with 90-day mortality, no individual postoperative complications were found to be significantly associated with mortality in the long term.

Given the limitations inherent in a retrospective analysis of a case series and absence of adequate presurgical HRQL measures for follow-up analysis, we have demonstrated reductions in dyspnea comparable to previous reports. Gelb et al²² reported a reduction in dyspnea grade ≥ 1 at 3-year, 4-year, and 5-year follow-up in 46%, 27%, and 15% of subjects, respectively. Approximately 30% of our patients who had dyspnea relief did not have an increase of > 200 mL of FEV₁ after surgery. Post-LVRS improvements in dyspnea have been related to increased lung elastic recoil,^{23 24} reduced hyperinflation,²⁴ improved respiratory muscle function,²⁴ and reduced mechanical restraints on tidal volume,²⁵ all of which may be independent of FEV₁.²⁶

Our results show that a lower BMI has an adverse impact on longer-term survival after LVRS. This was not due to any effect of patients with very poor nutritional status, as patients with a BMI < 18 were not eligible for surgery. In particular, a post hoc analysis indicated that a BMI of between 25 and 30 was significantly associated with improved survival. We also observed a trend for a low BMI (18 to <20) to be associated with a prolonged after surgery LOS. Nutritional status, specifically depletion, has been linked to morbidity²⁷ and mortality²⁸ in patients with COPD, and with adverse LVRS outcomes in the early postsurgical period.^{29 30} A study³⁰ with 6-month follow-up of 23 patients has demonstrated significantly higher mean BMI and fat-free mass index in patients without major complications. The significantly increased mortality among those with both low and normal BMI, compared with those with BMI ≥ 25 to 30, may be related to masking of fat-free muscle depletion in the apparently normal weight patients^{31 32} as a contributing factor. This may need to be considered when planning and selecting candidates for LVRS.

We were unable to confirm the high-risk baseline factors for mortality of FEV₁ ≤ 20% predicted and DLCO ≤ 20% predicted or a homogeneous pattern of emphysema recently reported on preliminary data by the National Emphysema Treatment Trial (NETT) Research Group.³³ We did detect a trend toward a higher DLCO predicting survival. However, only 5 of 54 patients in our uncontrolled case series had an FEV₁ ≤ 20% at baseline, and only one subject had a DLCO at baseline of ≤ 20%. The NETT investigators also reported a much higher 30-day mortality rate than our study (16% vs 5.5%). It is of note that with less severely affected patients than in the NETT, we were able to demonstrate substantial ongoing functional benefits from LVRS.

There is clear variation in function and quality of life in our patient group. Mean COOP scores 3 to 5.5 years after LVRS were better than those reported in a trial of hospital at home care vs standard hospital care for patients with COPD³⁴ and in a group of elderly patients in residential care,³⁵ even though an extra item pertaining to breathing was included in our "modified" COOP questionnaire. A significant limitation of this study is that we have inadequate pre-LVRS COOP data and follow-up lung function data to make statistically valid pre-LVRS and post-LVRS comparisons for these variables. Few studies have reported HRQL outcomes after LVRS. A study by Leyenson et al³⁶ showed short-term improvements in HRQL were not correlated with routine measures of pulmonary function, gas exchange, and exercise tolerance. Another study³⁷ showed that improvements in Medical Outcomes Study Short Form-36 scores at 6 months were significantly associated with improvements in FEV₁. An increased level of performance of daily activities may maintain exercise tolerance and prevent physical deconditioning in the presence of gradually declining objective lung function benefits.

There was no significant correlation between overall patient HRQL and caregiver burden, nor was there a significant independent relationship between care burden scores and the COOP social support item. Caregiver burden was lower for our patients’ caregivers than that reported by those caring for people with rheumatoid arthritis³⁸ and for people 3 years after stroke.²¹ Although interpretation of this data is limited by the lack of preoperative comparison data, it suggests that LVRS is unlikely to impose a significant extra burden on most caregivers.

The number of subjects with sustained increases in lung function at follow-up compared to pre-LVRS is consistent with that previously reported. Gelb et al^{1 39} demonstrated that increases in FEV₁ > 200 mL and/or FVC > 400 mL occurred in 46% of patients at 2 years and in 35% of subjects at 3 years, and Flaherty et al² reported FEV₁ improvements > 200 mL in 29% of patients at 3 years.

Post-LVRS survival rates vary across studies. Our follow-up has shown a survival rate of 67% at 3 years after LVRS, 63% at 4 years, and 56% at 5 years. This compares favorably with reported 3-year, 4-year, and 5-year survival rates of 69%, 54%, and 42%, respectively, by Gelb et al.²⁶ In contrast, our survival rates compare unfavorably with other reports of 5-year survival of 74%³ and the 3-year survival of 82%.² These differences may be explained by the younger age,^{2 3} less dyspnea,² and better exercise tolerance³ at baseline in these study subjects, compared to our study subjects.

It is arguable, however, that analysis of outcomes in the survivor fraction exaggerates the true benefits of LVRS. When lung function and dyspnea benefits were considered as a proportion of all of those subjects who underwent the procedure, the benefits were reduced and, at best, would seem marginal. Significant increases in FEV₁ and FVC after 3 years were demonstrable in 11% and 13% of all subjects, respectively. Similarly, 28% and 20% of all subjects experienced ongoing dyspnea relief as measured with the MRC scale and Mahler BDI. However, in a discussion of survival benefits associated with LVRS, it is necessary to consider the prognosis for people with COPD who receive optimal medical management only. Varying survival rates are reported in the literature. In the study by Almagro et al⁴⁰ in 135 elderly patients (mean age, 72.2 ± 9.3 years) who were hospitalized for acute exacerbations of COPD, the survival rate was 64% at 2 years. Given that people undergoing LVRS are a highly selected group of patients who usually undergo presurgical and postsurgical respiratory rehabilitation programs that in themselves are known to be beneficial,⁴¹ a direct comparison of our 3-year to 5-year survival rates and associated benefits in outcome measures with those reported in the literature for medical management alone possibly is not valid. Meyers et al⁴ compared 3-year survival rates for patients who were eligible for but were denied LVRS and proceeded to receive medical care, and those that underwent LVRS. They reported 3-year survival rates of 64% in the medical group, and 82% for the LVRS group, suggesting that the survival benefit conferred by LVRS is indeed meaningful. Indirect measures, such as rates of hospital admissions for exacerbations of COPD, in addition to the direct benefits of LVRS should be considered in future studies because these also have significant impacts on patients and health-care systems.

In summary, we have demonstrated sustained improvements in perceived dyspnea and lung function from LVRS that are preserved beyond 3 years. These improvements appear to be ongoing among those with up to 5.5-year survival. The HRQL of survivors is comparable to that experienced by the "healthy" elderly in the community. LVRS does not appear to impose an onerous burden on patient caregivers. Importantly, we have identified BMI as a predictor of longer postsurgical survival. This may have implications for selection of LVRS candidates and for preoperative management.

	Acknowledgements

 
The authors thank Lucy Saccoia from the Pulmonary Function Laboratory, and Kathy Fennel, Respiratory Nurse, from the Respiratory Medicine Unit for their assistance in the preparation of this article.

	Footnotes

 
Abbreviations: BDI = baseline dyspnea index; BMI = body mass index; COOP = Dartmouth Primary Care Co-operative Quality of Life questionnaire; DLCO = diffusion capacity of the lung for carbon monoxide; HRQL = health-related quality of life; NETT = National Emphysema Treatment Trial; LOS = length of stay; LVRS = lung volume reduction surgery; MRC = Medical Research Council; RV = residual volume; TLC = total lung capacity; VA = alveolar volume

This study was conducted entirely at The Queen Elizabeth Hospital.

Received for publication March 19, 2002. Accepted for publication September 27, 2002.

	References

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1. Gelb, A, KcKenna, R, Brenner, M, et al (1999) Lung function 4 years after lung volume reduction surgery for emphysema. Chest 116,1608-1615[Abstract/Free Full Text]
2. Flaherty, K, Kazerooni, E, Curtis, J, et al Short-term and long-term outcomes after bilateral lung volume reduction surgery: prediction by quantitative CT. Chest 2001;119,1337-1346[Abstract/Free Full Text]
3. Pohl MS, Lefrak S, Yusen RD, et al. Functional results of 200 consecutive bilateral lung volume reduction surgery patients [abstract]. Presented at: American Lung Association/American Thoracic Society International Conference, San Diego, CA, 1999
4. Meyers, B, Yusen, R, Lefrak, S, et al Outcome of Medicare patients with emphysema selected for, but denied, a lung volume operation. Ann Thorac Surg 2001;66,331-336
5. Geddes, D, Davies, M, Koyama, H, et al Effect of lung volume reduction surgery in patients with severe emphysema. N Engl J Med 2000;343,239-245[Abstract/Free Full Text]
6. Criner, G, Cordova, F, Furukawa, S, et al Prospective randomised trial comparing bilateral lung volume reduction surgery to pulmonary rehabilitation in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999;160,2018-2027[Abstract/Free Full Text]
7. Cooper, J, Patterson, G, Sundaresan, R, et al Results of 150 consecutive bilateral lung volume reduction procedures in patients with emphysema. J Thorac Cardiovasc Surg 1996;112,1319-1329[Abstract/Free Full Text]
8. Ferguson, G, Fernandez, E, Zamora, M, et al Improved exercise performance following lung volume reduction surgery for emphysema. Am J Respir Crit Care Med 1998;157,1195-1203[Abstract/Free Full Text]
9. Bagley, P, Davis, S, O’Shea, M, et al Lung volume reduction surgery at a community hospital: program development and outcomes. Chest 1997;111,1552-1559[Abstract/Free Full Text]
10. Norman, M, Hillerdal, G, Orre, L, et al Improved lung function and quality of life following increased elastic recoil after lung volume reduction surgery in emphysema. Respir Med 1998;92,653-658[CrossRef][ISI][Medline]
11. Porter, S, Ruffin, R, Pfitzner, J, et al Videoscopic lung volume reduction surgery in an Australian public teaching hospital. Aust N Z J Med 2000;30,202-208[Medline]
12. Brenner, M, McKenna, R, Gelb, A, et al Rate of FEV₁ change following lung volume reduction surgery. Chest 1998;113,652-659[Abstract/Free Full Text]
13. Cassina, P, Teschler, H, Konietzko, N, et al Two-year results after lung volume reduction surgery in ₁-antitrypsin deficiency versus smoker’s emphysema. Eur Respir J 1998;12,1028-1032[Abstract]
14. Yusen, R, Trulock, E, Pohl, M, et al Results of lung volume reduction surgery in patients with emphysema. The Washington University Emphysema Surgery Group. Semin Thorac Cardiovasc Surg 1996;8,99-109[Medline]
15. Mahler, D, Wells, C Evaluation of clinical methods for rating dyspnea. Chest 1988;93,580-585[Abstract/Free Full Text]
16. Mahler, D, Weinberg, D, Wells, C, et al The measurement of dyspnea. Chest 1984;85,751-757[Abstract/Free Full Text]
17. Nelson, E, Wasson, J, Kirk, J, et al Assessment of function in routine clinical practice: description of the COOP chart method and preliminary findings. J Chronic Dis 1987;40,55s-63s
18. Smith, B, Appleton, S, Bennett, P, et al The effect of a respiratory home nurse intervention in patients with chronic obstructive pulmonary disease (COPD). Aust N Z J Med 1999;29,718-725[Medline]
19. Landgraf, J, Nelson, E Summary of the WONCA/COOP International Health Assessment Field Trial. Aust Fam Physician 1992;21,255-269[Medline]
20. Nelson, E, Landgraf, J, Hays, R, et al The functional status of patients: how can it be measured in physician’s offices? Med Care 1990;28,1111-1125[CrossRef][ISI][Medline]
21. Elmstahl, S, Malmberg, B, Annerstedt, L Caregiver’s burden of patients 3 years after stroke assessed by a novel caregiver burden scale. Arch Phys Med Rehabil 1996;77,177-182[CrossRef][ISI][Medline]
22. Gelb, A, McKenna, R, Brenner, M, et al Lung function 5 yr after lung volume reduction surgery for emphysema. Am J Respir Crit Care Med 2001;163,1562-1566[Abstract/Free Full Text]
23. Gelb, A, Zamel, N, McKenna, R, et al Mechanism of short-term improvement in lung function after emphysema resection. Am J Respir Crit Care Med 1996;154,945-951[Abstract]
24. Martinez, F, de Oca, M, Whyte, R, et al Lung-volume reduction improves dyspnea, dynamic hyperinflation, and respiratory muscle function. Am J Respir Crit Care Med 1997;155,1984-1990[Abstract]
25. O’Donnell, D, Webb, K, Bertley, J, et al Mechanisms of relief of exertional breathlessness following unilateral lung volume reduction surgery in emphysema. Chest 1996;110,18-27[Abstract/Free Full Text]
26. Gelb, A, McKenna, R, Brenner, M Expanding knowledge of lung volume reduction. Chest 2001;119,1300-1302[Free Full Text]
27. Pouw, E, Ten Velde, G, Croonen, B, et al Early non-elective readmission for chronic obstructive pulmonary disease is associated with weight loss. Clin Nutr 2000;19,95-99[CrossRef][ISI][Medline]
28. Schols, A, 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 Med 1998;157,1791-1797
29. Mazolewski, P, Turner, J, Baker, M, et al The impact of nutritional status on the outcome of lung volume reduction surgery: a prospective study. Chest 1999;116,693-696[Abstract/Free Full Text]
30. Nezu, K, Yoshikawa, M, Yoneda, T, et al The effect of nutritional status on morbidity in COPD patients undergoing bilateral lung reduction surgery. Thorac Cardiovasc Surg 2001;49,216-220[Medline]
31. De Benedetto, F, Del Ponte, A, Marinari, S, et al In COPD patients, body weight excess can mask lean tissue depletion: a simple method of estimation. Monaldi Arch Chest 2000;55,273-278
32. Schols, A, Wouters, E Nutritional abnormalities and supplementation in chronic obstructive pulmonary disease. Clin Chest Med 2000;21,753-762[CrossRef][ISI][Medline]
33. National Emphysema Treatment Trial Research Group.. Patients at high risk of death after lung-volume-reduction surgery. N Engl J Med 2001;345,1075-1083[Abstract/Free Full Text]
34. Shepperd, S, Harwood, D, Jenkinson, C, et al Randomised control trial comparing hospital at home care with inpatient hospital care: I. Three month follow-up of health outcomes. BMJ 1998;316,1786-1791[Abstract/Free Full Text]
35. Siu, A, Hays, R, Ouslander, J, et al Measuring functioning and health in the very elderly. Med Sci 1993;48,M10-M14
36. Leyenson, V, Furukawa, S, Kuzma, A, et al Correlation of changes in quality of life after lung volume reduction surgery with changes in lung function, exercise, and gas exchange. Chest 2000;118,728-735[Abstract/Free Full Text]
37. Moy, M, Ingenito, E, Mentzer, S, et al Health-related quality of life improves following pulmonary rehabilitation and lung volume reduction surgery. Chest 1999;115,383-389[Abstract/Free Full Text]
38. Das Chagas Medeiros, M, Bosi Ferraz, M, Rodrigues Quaresma, M The effect of rheumatoid arthritis on the quality of life of primary caregivers. J Rheum 2000;27,76-83[ISI][Medline]
39. Gelb, A, Brenner, M, McKenna, R, et al Serial lung function and elastic recoil 2 years after lung volume reduction surgery for emphysema. Chest 1998;113,1497-1506[Abstract/Free Full Text]
40. Almagro, P, Calbo, E, de Echaguen, A, et al Mortality after hospitalization for COPD. Chest 2002;121,1441-1448[Abstract/Free Full Text]
41. British Thoracic Society Standards of Care Subcommittee on Pulmonary Rehabilitation.. Pulmonary rehabilitation. Thorax 2001;56,827-834[Free Full Text]

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