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First published online on May 15, 2007
Chest, doi:10.1378/chest.07-0435
doi:10.1378/chest.07-0435
(Chest. 2007; 132:477-482)
© 2007 American College of Chest Physicians
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Replacement of the 6-min Walk Test With Maximal Oxygen Consumption in the BODE Index Applied to Patients With COPD*

An Equivalency Study

Fábio Cardoso, PT, PhD; Andréa Thomazine Tufanin, PT; Marcelo Colucci, PT; Oliver Nascimento, MD and José Roberto Jardim, MD

* From the Pulmonary Rehabilitation Center, Universidade Federal de São Paulo/Lar Escola São Francisco, São Paulo, Brazil.

Correspondence to: José R. Jardim, MD, Rua Botucatu, 740 Third Floor, Respiratory Division (Pneumologia/Unifesp), 04023–062, São Paulo SP, Brazil; e-mail: joserjardim{at}yahoo.com.br

Abstract

Introduction: Patients with COPD have decreased exercise capacity and low oxygen consumption (VO2) during formal cardiopulmonary exercise testing, and lower scores on health-related quality of life questionnaires. When isolated, these three variables show different correlations with COPD mortality. The multidimensional BODE (body mass index[BMI], airflow obstruction, dyspnea, and exercise capacity in COPD) index, which comprises four variables including the 6-min walk test (6MWT), predicts survival in COPD.

Objectives: To evaluate the degree of association between the values of the BODE index using the 6MWT with the BODE index using maximal VO2 (VO2max) obtained in a maximal incremental test.

Materials and methods: Fifty patients with mild-to-severe COPD (average age, 63.5 ± 9.9 years; FEV1, 65.3 ± 23.6% of predicted) [± SD] had BMI, spirometric function (FVC and FEV1), and dyspnea status (Medical Research Council) evaluated. Two BODE index scores were then completed: one with the 6MWT, and one with the VO2max obtained during maximal incremental testing on a treadmill.

Results: Correlation between BODE index and VO2 in milliliters per minute per kilogram (r = – 0.41) was weak; the correlation was moderate (r = – 0.64) when VO2 percentage of predicted was used. The BODE index modified by replacing the 6MWT with VO2 showed excellent correlations with VO2 in milliliters per minute per kilogram (r = 0.92) and VO2 percentage of predicted (r = 0.95).

Conclusion: The excellent correlation between the conventional BODE index and the modified BODE index with VO2 replacing the 6MWT enables us to reach the conclusion that the original BODE index is very effective in the evaluation of COPD patients.

Key Words: COPD • exercise test • exercise tolerance • mortality index • mortality prognosis • oxygen consumption

COPD is one of the most important respiratory conditions, with high morbidity and mortality rates globally, and with higher prevalence and mortality rates being expected in the forthcoming years.123 The clinical signs of the disease are not restricted to the inflammatory and structural changes in the lungs45; patients also present with important abnormalities in nutritional status,34 peripheral muscles,67 ventilatory mechanics,8910 and gas exchange.1112

Celli et al13 developed the BODE (body mass index [BMI], airflow obstruction, dyspnea, and exercise capacity in COPD) multidimensional index based on four relevant variables related to COPD mortality. Celli et al13 showed that this index is a better predictor of mortality for COPD patients than the classical variable FEV1 alone. Besides, the BODE index is easily applicable.

The 6-min walk test (6MWT) is a marker for exercise capacity of COPD patients in the BODE index. However, the 6MWT is a submaximal test dependent on individual motivation and may not express the real physical capacity of the patient. Maximal incremental tests limited by symptoms are highly related with maximal oxygen consumption (VO2max), which is an objective measurement and largely used as a physical training target,141516 a survival rate predictor,17 and is used for evaluation of the severity of the disease and the degree of disability of COPD patients.17181920 However, as far as we know, no one has yet compared the BODE index with a BODE index modified by replacing the distance covered in the 6MWT with VO2max. The objective of our study was to evaluate the correlation between the conventional BODE index and a BODE index modified by replacing the distance covered in the 6MWT with oxygen consumption (VO2) expressed as VO2 in milliliters per minute per kilogram and VO2 percentage of predicted.

Materials and Methods

Subjects
Fifty patients with COPD diagnosed according to Global Initiative for Chronic Obstructive Lung Disease criteria2 were prospectively studied. Requirements for the patient to be included in the study were as follows: clinically stable (no increased wheezing, cough, dyspnea or sputum over the previous 30 days), no systemic corticosteroids or antibiotics over the past month, and a signed consent form. The protocol was approved by the ethics committee of the university.

Protocol
Patients underwent nutritional, spirometry, and dyspnea evaluations, two 6MWTs, and one maximal exercise test on a treadmill.

Measurements
Nutritional Status: BMI was obtained by dividing weight in kilograms by height in square meters; subjects with BMI values < 21 kg/m2 were considered underweight.13

Spirometry: Spirometry was performed before and 15 min after the inhalation of 400 µg of albuterol via a metered-dose inhaler (EasyOne; Zurich, Switzerland); predicted values for FVC and FEV1 were calculated according to the third National Health and Nutrition Examination Survey.21 Our patients were classified into two subgroups, one group with severe-to-very-severe COPD (FEV1 < 50% of predicted), and the other group with mild-to-moderate COPD (FEV1 ≥ 50% of predicted). This cutoff value was established due to the fact that deterioration in quality of life22 and decrease in survival23 increase in patients with FEV1 < 50% of the predicted value.

Dyspnea: The dyspnea score was measured according to the Medical Research Council index.

6MWT: The 6MWT was performed on a straight, 22-m corridor with standardized verbal encouragement given every minute. Two 6MWTs were performed on the same day with a minimum interval of 45 min between them and after the physiologic variables had returned to basal values. The longest distance obtained in the two tests was used in the study.24

Incremental Exercise Test With Analysis of Exhaled Gases: Patients were submitted to a maximal symptom-limited exercise test on a treadmill (Cybex Q35CI; Cybex International; Medway, MA) with room temperature between 20° and 24°C, following the Harbor protocol.1415 An accepted test should last 11 to 15 min, including 3 min of warming up at constant speed and no inclination increase, followed by 1% inclination increments every minute. The test was interrupted if heart alterations that could be a risk for the patient were detected.1415 Expired gases were analyzed using portable equipment (K4b2; Cosmed; Rome, Italy). Patients were submitted to the incremental exercise test within 2 to 3 days after the 6MWT.

Calculation of the Conventional BODE Index and the Modified BODE Index by Replacing the 6MWT With VO2 in Milliliters per Minute per Kilogram and VO2 Percentage of Predicted: The BODE index was calculated after obtaining all necessary variables.13 Each variable was distributed in a 0 to 3 scale, except for BMI, which was taken as a dichotomic variable (0 or 1). The sum of the variables corresponds to a BODE index score from 1 to 10. The scale is divided in quartiles, and the first quartile corresponds to a score between 0 and 2 points, the second quartile from 3 to 4 points, the third quartile from 5 to 6 points, and the fourth quartile from 7 to 10 points.13 For calculation of the modified BODE index, the 6MWT was replaced by the VO2max values as obtained in the incremental test using values in VO2max in milliliters per minute per kilogram and VO2max percentage of predicted. Assuming that there is a correlation between the distance walked in the 6MWT and the VO2 achieved during a maximal symptom-limited exercise test on a treadmill, we replaced the stratified values of the 6MWT by stratified values of VO2max in milliliters per minute per kilogram according to the American Medical Association25 evaluation: score 0, > 25 mL/min/kg; score 1, 20 to 25 mL/min/kg; score 2, 15 to 20 mL/min/kg; score 3, < 15 mL/min/kg. The same way we replaced the stratified values of the 6MWT by stratified values of VO2max percentage of predicted according to Neder et al26: score 0, > 70% of predicted; score 1, 60 to 69% of predicted; score 2, 40 to 59% of predicted; score 3, < 40% of predicted. Thus, two other indexes were created: BODE VO2 milliliters per minute per kilogram index, and BODE VO2 percentage of predicted index.

Data Analysis
Data are presented as mean and SD. Patients with severe-to-very-severe COPD were compared with the group of patients with mild-to-moderate COPD in relation to the variables of the study by means of Student t test for nonrelated samples. Significance was set at p < 0.05 or 5%. In order to study the association between numeric variables, a Pearson linear correlation coefficient was used.27 The size of the sample was determined based on the correlation between VO2 and the BODE index described by Sívori et al28 (r = 0.42). For a bidirectional {alpha} error = 0.05 and a ß error = 0.20, 47 patients were required.29

Results

Anthropometric data and pulmonary function values of the 50 patients are shown in Table 1 . Variables studied in the 6MWT and in the incremental test with analysis of exhaled gases are presented in Tables 2 and 3 , respectively.


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  		Table 1.. Demographic, Spirometric, and Dyspnea Variables and BODE Index in 50 COPD Patients (Complete Sample) and in the Sample With Mild-to-Moderate COPD (FEV1 ≥ 50% of Predicted, n = 35) and Severe-to-Very Severe COPD (FEV1 < 50% of Predicted, n = 15)*

 

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  		Table 2.. Variables Obtained in the 6MWT: Initial and Final Cardiorespiratory Variables and Distance Covered by 50 Patients With COPD, and in the Division of the Sample With Mild-to-Moderate COPD (FEV1 ≥ 50% of Predicted, n = 35) and Severe-to-Very Severe COPD (FEV1 < 50% of Predicted, n = 15)*

 

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  		Table 3.. Parameters Obtained in the Treadmill Test: Distance Covered, Incline, Speed, and Time, and Cardiorespiratory and Metabolic Variables of the Patients in the Maximal Incremental Test in 50 Patients With COPD, and in the Division of the Sample With Mild-to-Moderate COPD (FEV1 ≥ 50% of Predicted, n = 35) and Severe-to-Very-Severe COPD (FEV1 < 50% or Predicted, n = 15)*

 
Correlation of BODE Index with BODE VO2 Milliliters per Minute per Kilogram Index and BODE VO2 Percentage of Predicted Index
The conventional BODE index had an excellent correlation with BODE index modified by replacing distance in the 6MWT with VO2 in milliliters per minute per kilogram (r = 0.92) and with VO2 percentage of predicted (r = 0.95), as shown in Figures 1 and 2 .


Figure 1
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  		Figure 1.. Dispersion graph for the conventional BODE index and the index modified by replacing the distance covered in the 6MWT with VO2 in milliliters per minute per kilogram obtained during incremental testing on a treadmill. Numbers above the points represent the same number of patients presenting the same value for the index.

 

Figure 2
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  		Figure 2.. Dispersion graph for the conventional BODE index and the index modified by replacing the distance covered in the 6MWT with VO2 percentage of predicted obtained during incremental testing on a treadmill. Numbers above the points represent the same number of patients presenting the same value for the index.

 
Correlation Between the BODE Index With VO2 in Milliliters per Minute per Kilogram and VO2 Percentage of Predicted
The conventional BODE index showed a weak correlation (r = – 0.41) with VO2 in milliliters per minute per kilogram considering the whole sample (Fig 3 ). The correlation between the BODE index with VO2 percentage of predicted showed a moderate correlation (r = – 0.64; Fig 4 ).


Figure 3
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  		Figure 3.. Dispersion graph for the BODE index and VO2 in milliliters per minute per kilogram.

 

Figure 4
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  		Figure 4.. Dispersion graph for the BODE index and VO2 percentage of predicted.

 
Discussion

COPD is a multisystemic disease,1234 and several parameters have been associated with its prognosis. In addition to the variables that are obtained during resting conditions, it may be appropriate to add variables that may change during increased demands because the behavior of physiologic measurements at rest may not precisely anticipate the physiologic response during effort.

Celli et al13 developed the BODE index, a predictor of mortality that comprises four domains. It is a multidimensional, easy-to-apply index that takes into consideration BMI, bronchial obstruction, degree of dyspnea, and exercise capacity as measured by the distance covered in the 6MWT. The authors13 showed that mortality prognosis as given by the BODE index is much more accurate than that by FEV1 alone. The BODE index has also been associated with positive results in pulmonary rehabilitation30 and with the need for hospitalization.31

The walking test included in the BODE index has been largely used to evaluate the physical condition of patients and also the response to interventions such as pulmonary rehabilitation. However, the 6MWT is a submaximal test and may not express the real physical capacity of the patient. On the contrary, VO2max is considered to be an objective test, and it is taken as the "gold standard" for the evaluation of the physical capacity besides having good relation to COPD survival.173233 However, this test requires expensive and sophisticated equipment to be correctly implemented.

The association between VO2max in milliliters per minute per kilogram achieved in an incremental test and the distance walked in a 6MWT is only moderate, although it always remains as one of the variables of maximal oxygen prediction equations.3435363738 We correlated the conventional BODE index with a second BODE index modified by replacing the distance covered in the 6MWT by the VO2 obtained in a maximal incremental exercise test on the treadmill.

The association between the conventional BODE index and VO2max showed a better correlation with VO2 percentage of predicted (r = – 0.64) than with VO2 in milliliters per minute per kilogram (r = – 0.41). Sívori et al28 evaluated the association between the BODE index with maximal exercise in VO2 in milliliters per minute per kilogram in cycloergometer and found a correlation similar to ours (r = – 0.42). However, they did not evaluate VO2 as a percentage of predicted. Neder et al26 observed that VO2 is better expressed as a percentage of the predicted value in the elderly with chronic respiratory diseases and in obese patients.

We observed an excellent correlation between the conventional BODE index and the modified indexes with the 6MWT being replaced by VO2 expressed in milliliters per minute per kilogram (r = 0.92) and percentage of predicted (r = 0.95). Based on these results, it is clear that the substitution of the 6MWT in the BODE index by a maximal and objective test maintains the same properties of the index as described by Celli et al.13 Our results do not want to show that 6MWT should be replaced with a maximal test but only that the two tests are significantly correlated so strengthening the usefulness of the more practical BODE index assessment. This is the main originality of the present study. These data support the BODE index as an accurate tool despite using a simple test for physical capacity, and little information is gained by substituting VO2 for the easier-to-obtain 6-min walk distance in the construction of the BODE index.

As far as we know, our study is the first one to evaluate the association between the original BODE index with a modified index replacing the 6MWT score by the VO2 in milliliters per minute per kilogram and VO2 percentage of predicted. As our sample population reflected all degrees of disease severity, we believe our results may be applied to other populations of COPD patients.

Footnotes

Abbreviations: BMI = body mass index; BODE = body mass index, airflow obstruction, dyspnea, and exercise capacity in COPD; 6MWT = 6-min walk test; VO2 = oxygen consumption; VO2max = maximal oxygen consumption

Funding was partially provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Conselho Nacional de Desenvolvimento Científico e Tecnológico, and Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil.

The study was approved by the Universidade Federal de São Paulo Ethics Committee (No. IRB-0347/04; http://www.unifesp.br/reitoria/orgaos/comites/etica/).

The authors have no conflicts of interest to disclose.

Received for publication February 16, 2007. Accepted for publication April 4, 2007.

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