Improvements in the 6-Min Walk Test and Spirometry Following Thoracentesis for Symptomatic Pleural Effusions
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1 CHEST Original Research Improvements in the 6-Min Walk Test and Spirometry Following Thoracentesis for Symptomatic Pleural Effusions Ana Maria Cartaxo, RT ; Francisco S. Vargas, MD ; João Marcos Salge, MD ; Bianca F. Marcondes, RT ; Eduardo H. Genofre, MD ; Leila Antonangelo, MD ; Evaldo Marchi, MD, FCCP ; and Lisete R. Teixeira, MD PULMONARY PROCEDURES Background: Impairment in pulmonary capacity due to pleural effusion compromises daily activity. Removal of fluid improves symptoms, but the impact, especially on exercise capacity, has not been determined. Methods: Twenty-five patients with unilateral pleural effusion documented by chest radiograph were included. The 6-min walk test, Borg modified dyspnea score, FVC, and FEV 1 were analyzed before and 48 h after the removal of large pleural effusions. Results: The mean fluid removed was 1, ml. After the procedure, values of FVC, FEV 1, and 6-min walk distance increased ( P,.001), whereas dyspnea decreased ( P,.001). Statistical correlations ( P,.001) between 6-min walk distance and FVC ( r ) and between 6-min walk distance and FEV 1 ( r ) were observed. Correlations also were observed between the deltas (prethoracentesis 3 postthoracentesis) of the 6-min walk test and the percentage of FVC ( r ) and of FEV 1 ( r ) divided by the volume of fluid removed ( P,.05). Conclusion: In addition to the improvement in lung function after thoracentesis, the benefits of fluid removal are more evident in situations of exertion, allowing better readaptation of patients to routine activities. CHEST 2011; 139(6): Abbreviations: 6MWT 5 6-min walk test; Sp o 2 5 peripheral oxygen saturation Pleural effusion is characterized by the abnormal accumulation of fluid in the pleural space secondary to local or systemic diseases. 1 This clinical condition causes changes in respiratory mechanics, with a reduction in static and dynamic lung function. In extreme cases, the increasing accumulation of fluid can prog ress to respiratory failure and death. The usual symptoms reported by patients are dyspnea, pain, and coughing that generally intensify with effort, precluding, in many cases, the continuation of habitual daily activities. 2 Manuscript received July 1, 2010; revision accepted October 12, Affiliations: From the Pleura Laboratory (Mss Cartaxo and Marcondes and Drs Vargas, Salge, Genofre, Antonangelo, Marchi, and Teixeira), Pulmonary Division Heart Institute (InCor), University of São Paulo Medical School, São Paulo; and Faculdade de Medicina de Jundiaí (Dr Marchi), Jundiaí, Brazil. Funding/Support: This work was supported by the State of São Paulo Research Foundation (FAPESP), and the National Research Council (CNPq), Brazil. Correspondence to: Lisete R. Teixeira, MD, R: Copacabana 415/184, São Paulo, Brazil ; lisetepneumo@ yahoo.com.br Removal of pleural fluid by thoracentesis causes relief of dyspnea and improvement in the mechanical function of the chest, allowing patients to return to routine activities. 3,4 Studies have reported a significant improvement in pulmonary function, particularly in FVC and FEV 1, with removal of pleural fluid. 5-8 It should be noted that this improvement was observed immediately or 24 h after thoracentesis, when the adjustment of the respiratory system to this new condition may not have occurred yet. Additionally, it is important to consider that during the first hours after the procedure, the patient is still susceptible to acute effects resulting from the intervention in the pleural space, particularly coughing and pain, that may underestimate the improvement caused by the fluid drainage. Therefore, the changes resulting. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( site/misc/reprints.xhtml ). DOI: /chest Original Research
2 from the removal of expressive volumes of pleural fluid should be analyzed not only statically but also dynamically during exertion when the improvement in symptoms may be more evident. Few studies have analyzed patient tolerance of daily living activities and pulmonary function in periods. 24 h after thoracentesis. 5-9 Within this context, the 6-min walk test (6MWT) assesses the cardiopulmonary system response at a level of exercise that frequently is submaximal. 10 Thus, it represents most of the activities of daily life and can be useful in analyzing the impact of thoracentesis on patient quality of life. Despite being used to evaluate the effect of therapy and as a predictor of morbidity and mortality in heart failure, COPD, and pulmonary hypertension, there are no reports, to our knowledge, of the application of this test in patients with pleural effusions. 11 Therefore, the objective of this study was to evaluate pulmonary function, emphasizing exercise tolerance 48 h after thoracentesis. Patients Materials and Methods The study was performed from February 2008 to September 2009 at the Pleural Diseases outpatient clinic of the Pulmonary Division, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo, Brazil. All patients signed a free informed consent after the study was approved by the institutional ethics committee (CAPPesq # 998/05). Patients were enrolled according to the following inclusion criteria: presence of unilateral pleural effusion occupying more than one-half of the hemithorax with an indication for therapeutic thoracentesis, good clinical condition (Karnofsky index 70), and physically able to perform the 6MWT. Initially, we evaluated 42 patients; however, 17 were excluded as follows: 10 refused to perform the 6MWT after thoracentesis, and seven had loculated effusions, with a small amount of drained pleural fluid (, 300 ml). No patient had previously undergone pleurodesis or had clinical signs of heart failure. Radiography All 25 patients included in the study were evaluated before and 48 h after thoracentesis. The chest radiographs (prethoracentesis and postthoracentesis) were analyzed by a radiologist who classified the effusion by scores from 1 to 5, with 1 representing the absence of fluid and 5 a volume occupying. 75% of the hemithorax. 12 Thoracentesis Procedure Thoracentesis was performed by a trained pulmonologist using the standard technique, including pleural manometry. 2 The procedure was suspended if spontaneous cessation of liquid drainage occurred or if the patient experienced discomfort with exacerbation of symptoms (coughing, dyspnea, or chest pain) or vagal manifestations (dizziness or nausea). Pulmonary Function The patients were evaluated by spirometry and the 6MWT. To measure FVC and FEV 1, a Koko spirometer (nspire Health, Inc; Longmont, California) was used, and the maneuvers were performed according to the guidelines of the American Thoracic Society and European Respiratory Society. 13 The values obtained were compared with normal predicted values reported by Knudson et al. 14 Six-Minute Walk Test The 6MWT was carried out according to American Thoracic Society standards. 10 The patients performed the walk test at a free pace over a 30-m flat corridor for 6 min. All tests were conducted by the same examiner without the use of words of encouragement. The test was interrupted if the patient experienced chest pain, intolerable dyspnea, muscle cramps, dizziness, malaise, or sweating associated with skin pallor. 10 The walked distance was recorded at the end of each test and compared with predictive normal values according to equations described by Enright and Sherrill. 15 During the 6MWT, peripheral oxygen saturation (Sp o 2 ) and heart rate were monitored with a pulse oximeter (model 3100; Nonin Medical, Inc; Plymouth, Minnesota). Dyspnea was evaluated at the beginning and end of each test by using the Borg modified dyspnea score, which consists of a scale of 0 to 10 with corresponding verbal expressions of a progressively increasing sensation intensity. 16 Statistical Analysis Data are expressed as mean SD. The comparisons were done using paired t tests or Wilcoxon test according to the distribution of the data. The Friedman repeated measurements test was used followed by the Tukey test for heart rate and Sp o 2. For the correlation among variables, the Pearson test was applied. The level of significance was defined as P.05. For statistical analysis, SigmaStat version 3.5 (Systat Software, Inc; San Jose, California) software was used. Results Of the 25 patients evaluated, 15 (60%) were men. The average age was years. In 20 patients, the pleural effusion was an exudate (14 secondary to cancer and six to TB) and a transudate in five (liver failure). In the excluded patients, none had a transudative pleural effusion (etiology of cancer in 14 and TB in 3). The 10 patients who refused to perform the 6MWT presented moderate to large pleural effusion. The mean of fluid removed was 1, ml. The procedure was interrupted when no fluid came out spontaneously. The maximum negative pressure observed by pleural manometry at the end of fluid removal was cm H 2 O. No patients presented with adverse side effects during thoracentesis. According to the radiographic evaluation, the initial score ( ) represented the involvement of 50% to 75% of the hemithorax, significantly greater ( P,.001) than that observed after thoracentesis ( ), reflecting an involvement of, 25% of the pleural cavity. After the procedure, no patient had clinical or radiologic evidence of pneumothorax or signs of reexpansion pulmonary edema. CHEST / 139 / 6 / JUNE,
3 Table 1 Pulmonary Function Results Before and After Thoracentesis Parameters Before Thoracentesis After Theracentesis D a P Value FVC L % FEV 1 L % FEV 1 /FVC Data are presented as mean SD, unless otherwise indicated. aafter 2 before. In the presence of pleural effusion, spirometry showed reduction of FVC and FEV 1. After thoracentesis, there was an increase ( P,.001) of 350 ml (18.5%) in FVC and of 280 ml (18.4%) in FEV 1 ( Table 1 ). However, no correlation was observed between the spirometric results and the volume of fluid drained. The distance walked ( Fig 1A ) after pleural fluid removal increased significantly ( P,.001), with a mean gain of 63 m (14.6%), varying from m (73.3% predicted) in the presence of pleural effusion to m (83.9% predicted) after thoracentesis. Dyspnea score ( Fig 1B ) was significantly greater in the presence of pleural effusion (resting, ; 6MWT, ) than after fluid removal (resting, ; 6MWT, ). The Sp o 2 ( Fig 1C ) declined from the second minute of the 6MWT ( P,.001), returning to initial levels 2 min after the end. There was no difference ( P..05) due to the fluid removal. The heart rate ( Fig 1D ) showed progressive elevation from the second minute, returning independently of fluid removal to baseline levels 2 min after the end of the test. Significant correlations were observed ( P,.001) between the distance walked and the values of FVC ( r ) and of FEV 1 (r ) after thoracentesis ( Figs 2A, 2B ). Similarly, the variation of the distance walked during the 6MWT, as a result of emptying the pleural cavity, correlated significantly ( P,.05) with the percentage of variation of FVC ( r ) or FEV 1 ( r ), corrected by the volume of fluid removed ( Figs 2C, 2D ). Discussion The removal of a significant volume of fluid from the pleural space, based on the analysis performed 48 h after the procedure, resulted in an increase in the distance walked in 6 min, FVC, and FEV 1, with an evident reduction in dyspnea. These results show that the improvement resulting from emptying the pleural cavity increases exercise tolerance, contributing positively toward patients being able to return to their daily activities. Prior studies demonstrated that 24 h after removal of pleural fluid, the spirometric variables improved. 6,7,9 Figure 1. The thoracentesis effect of the 6-min walk test. A, Walked distance. B, Modified dyspnea Borg score. C, Sp o 2. D, Heart rate ( P,.001). After thoracentesis vs before thoracetesis. # D0 vs D 6 min. Sp o 2 5 peripheral oxygen saturation Original Research
4 Figure 2. The relationship among pulmonary function, 6-min walk test, and removed fluid by thoracentesis. A, Relationship between the walked distance and FVC after thoracentesis. B, Relationship between the walked distance and FEV 1 after thoracentesis. C, Relationship between the ratio of the improvement in FVC to the amount of fluid removed and the improvement in the walked distance. D, Relationship between the ratio of the improvement in FEV 1 to the amount of fluid removed and the improvement in the walked distance. It is noteworthy that these changes are similar to those found after 48 h, which suggests that the symptoms of pain or cough caused by thoracentesis are irrelevant and transient and that early adequate pulmonary accommodation occurs. In this way, despite not having a correlation between the spirometric enhancement and the volume of fluid drained, the impact of thoracentesis is significant, with an improvement of. 10% both in FVC and FEV 1. 5 One should take into account, however, that the functional improvement obtained at rest cannot be extrapolated for situations of exertion, even for the development of moderate exercise, such as daily activities. Because patients with pleural effusions predominantly report the lack of capacity to perform their habitual daily tasks, in this study, we sought to assess exercise tolerance by means of the 6MWT. The analysis of the functional capacity for exercise in patients with lung diseases has been the object of study since the 1970s. 17 It is known that patients with different degrees of functional limitations may be symptomatic only during exertion, and thus, evaluation during exercise is important for characterizing not only the intensity of the impairment but also the prognosis, including the impact of therapeutic measures. Of the various forms of evaluation, we point out the cardiac stress test, which analyzes cardiac adaptations, and cardiopulmonary exercise testing, which allows the study of ventilatory variables providing maximal oxygen uptake. 18,19 Even though they are capable of offering specific, detailed, functional information, these tests are relatively high cost, require special equipment and trained professionals, and depend on the familiarity of the patient with the equipment. 18 However, studies using exercise testing in patients with pleural effusions are scarce. In 1987, Shinto et al 20 wrote a brief report (abstract) on cardiopulmonary exercise testing in 13 patients with large pleural effusions after the removal of volumes. 1.5 L. Even though the authors referred to no difference in ventilation and exercise levels, the preliminary finding that patients who had more amounts of drained pleural fluid were able to attain a higher maximum workload roused new interest. Commonly used in the evaluation of exercise tolerance, the 6MWT is a submaximal test that reproduces daily activities. It is well accepted by patients and allows an integrated assessment of the cardiopulmonary system, including analysis of distance walked, degree of dyspnea, and behavior of Sp o 2 and heart rate. Despite its importance, it has been ignored in patients with pleural diseases. CHEST / 139 / 6 / JUNE,
5 In addition to the presence of pleural effusion, multiple factors should be considered to explain the exercise limitations these patients experienced, including physical debilitation due to the underlying disease and the predominant cause being cancer in the present study, which like TB and hepatopathy, causes systemic alterations that can reduce exercise capacity. The distance walked before thoracentesis was 27% lower than that predicted for a healthy population with the same characteristics. However, the removal of a mean 1.5 L of pleural fluid resulted in a gain of 11%. Therefore, after the procedure, patients had improved exercise capacity but did not reach the predicted value, maintaining a mild reduction of 16%. One should consider that therapeutic thoracentesis, indicated for relief of symptoms in patients, sometimes does not totally empty the cavity, although Feller-Kopman et al 21 suggested to drain the pleural space completely. In the present study, the reduction of the fluid content in the drained hemithorax was significant, decreasing from 75% to, 25% after thoracentesis. It is essential to consider the sensation of dyspnea resulting from the presence of the effusion and the improvement obtained with the emptying of the pleural cavity. At rest, dyspnea is mild and well tolerated; however, a small amount of effort intensifies the symptoms, generating a sensation of discomfort that hinders even the most common daily activities. In this regard, the results obtained are clarifying. Although the removal of pleural fluid reduces the sensation of dyspnea at rest (positioning the patient at a level at which the symptom is no longer perceptible), after walking for 6 min, this sensation diminishes significantly more (reaching a level lower than that reported by patients at rest but in the presence of pleural effusion). This finding demonstrates that the limitations of these patients is greater in situations of effort and that thoracentesis with drainage of fluid promotes great benefits, allowing the patient to return to an active life. The 6MWT poses a physiologic stress that uncovers oxygen desaturation and tachycardia in the presence of pleural effusion. The notable improvement in these indices suggests a significant reduction in this stress and these abnormal responses with pleural fluid drainage. In conclusion, we demonstrated that although there is an improvement in pulmonary function, the benefits of thoracentesis are more evident in situations of exertion, allowing for a better readaptation of these patients to their routine activities. Acknowledgments Author contributions: Ms Cartaxo had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Ms Cartaxo: contributed to the study design, data collection, and writing of the manuscript. Dr Vargas: contributed to the study design and revision of the manuscript. Dr Salge: contribute to the data interpretation and revision of the manuscript. Ms Marcondes: contributed to the data collection and approval of the manuscript. Dr Genofre: contributed to the data interpretation and writing of the manuscript. Dr Antonangelo: contributed to the statistical analysis and revision of the manuscript. Dr Marchi: contributed to the statistical analysis and revision of the manuscript. Dr Teixeira: contributed to the study design, data collection, and writing and revision of the manuscript. Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article. Role of sponsors: The sponsors had no role in the design of the study, the collection and analysis of the data, or in the preparation of the manuscript. References 1. Light RW, Jenkinson SG, Minh VD, George RB. Observations on pleural fluid pressures as fluid is withdrawn during thoracentesis. Am Rev Respir Dis ;121(5): Antunes G, Neville E, Duffy J, Ali N ; Pleural Diseases Group, Standards of Care Committee, British Thoracic Society. BTS guidelines for the management of malignant pleural effusions. Thorax ;58(suppl 2 ):ii29-ii Agustí AGN, Cardús J, Roca J, Grau JM, Xaubet A, Rodriguez-Roisin R. Ventilation-perfusion mismatch in patients with pleural effusion: effects of thoracentesis. Am J Respir Crit Care Med ;156(4 pt 1 ): Feller-Kopman D, Walkey A, Berkowitz D, Ernst A. The relationship of pleural pressure to symptom development during therapeutic thoracentesis. Chest ; 129 ( 6 ): Brown NE, Zamel N, Aberman A. Changes in pulmonary mechanics and gas exchange following thoracocentesis. Chest ;74(5): Light RW, Stansbury DW, Brown SE. The relationship between pleural pressures and changes in pulmonary function after therapeutic thoracentesis. Am Rev Respir Dis ;133(4): Wang JS, Tseng CH. Changes in pulmonary mechanics and gas exchange after thoracentesis on patients with inversion of a hemidiaphragm secondary to large pleural effusion. Chest ;107(6): Estenne M, Yernault JC, De Troyer A. Mechanism of relief of dyspnea after thoracocentesis in patients with large pleural effusions. Am J Med ;74(5): Wang LM, Cherng JM, Wang JS. Improved lung function after thoracocentesis in patients with paradoxical movement of a hemidiaphragm secondary to a large pleural effusion. Respirology ;12(5): ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med ;166(1): Enright PL. The six-minute walk test. 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