respiratory investigation 52 (2014) 41 –48
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Original article
Reduced level of physical activity in Japanese patients with chronic obstructive pulmonary disease Yoshiaki Minakataa,n, Akihito Suginoa, Masae Kandaa, Tomohiro Ichikawaa, Keiichiro Akamatsua, Akira Koaraib, Tsunahiko Hiranoa, Masanori Nakanishia, Hisatoshi Sugiurab, Kazuto Matsunagaa, Masakazu Ichinoseb a
Third Department of Internal Medicine, Wakayama Medical University, Wakayama, Japan Department of Respiratory Medicine, Tohoku University Graduate School of Medicine, Miyagi, Japan
b
art i cle i nfo
ab st rac t
Article history:
Background: There is increasing interest in the quantification of physical activity (PA) with
Received 16 January 2013
an accelerometer for the management of chronic obstructive pulmonary disease (COPD).
Received in revised form
However, a detailed understanding of the PA in Japanese patients with COPD is lacking. We
3 June 2013
evaluated the levels of PA in terms of intensity in Japanese patients with COPD and
Accepted 10 June 2013
evaluated the factors, which could influence the PA.
Available online 18 July 2013
Methods: Forty-three outpatients with COPD and 21 age-matched healthy subjects were
Keywords: COPD Accelerometer Intensity BODE index ADO index
monitored with a triaxial accelerometer, and their PA was compared. Furthermore, the effects of pulmonary function, ADO index (age, dyspnea, and airflow obstruction) and modified BODE index (body mass index, airflow obstruction, dyspnea, and exercise capacity) on the PA were evaluated. Results: The PA in COPD was significantly reduced at all intensities. The reduced levels of PA in COPD were 23.1% at ≥2.0 metabolic equivalents (METs), 33.0% at ≥2.5 METs, 50.9% at ≥3.0 METs, and 66.9% at ≥3.5 METs, compared with that of healthy subjects, and the reduction was significant at GOLD stage III. The values of FVC, FEV1.0, and DLCO/VA were correlated with that of the PA, but the lung volume parameters were not. The ADO and modified BODE indices were also well correlated with the PA. Conclusions: The reduced levels of PA in Japanese patients with COPD were objectively demonstrated in terms of intensity that could provide us a new target for the management of COPD. & 2013 The Japanese Respiratory Society. Published by Elsevier B.V. All rights reserved.
Abbreviations: PA,
physical activity; ADO index,
index including age, dyspnea, and airflow obstruction; BODE index,
including body-mass index, airflow obstruction, dyspnea, and exercise capacity; METs,
metabolic equivalents; MMRC,
index
modified
Medical Research Council n Correspondence to: Third Department of Internal Medicine, Wakayama Medical University, 811-1 Kimiidera Wakayama, Wakayama, 641-0012, Japan. Tel.: 81 73 441 0619; fax: 81 73 446 2877. E-mail addresses: [email protected] (Y. Minakata), [email protected] (A. Sugino), [email protected] (M. Kanda), [email protected] (T. Ichikawa), [email protected] (K. Akamatsu), [email protected] (A. Koarai), [email protected] (T. Hirano), [email protected] (M. Nakanishi), [email protected] (H. Sugiura), [email protected] (K. Matsunaga), [email protected] (M. Ichinose). 2212-5345/$ - see front matter & 2013 The Japanese Respiratory Society. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.resinv.2013.06.002
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1.
respiratory investigation 52 (2014) 41 –48
Introduction
Patients with chronic obstructive pulmonary disease (COPD) are often limited in their daily physical activity (PA), and the level of PA is related to the decline in lung function [1], as well as hospitalizations [2,3] and mortality [4]. Therefore, the PA in patients with COPD has received increasing clinical interest. Recently, motion sensors, especially accelerometers, have been used to quantify the PA in patients with COPD [5–7], instead of questionnaires [8,9], which are less objective and reliable [10]. Among the reported accelerometers, the most reported and well-validated accelerometer for patients with COPD is the DynaPort Activity Monitor (DAM; McRoberts BV; The Hague, the Netherlands) [11–13]. However, it has several impediments to obtaining an accurate measurement of the PA, including the following: its battery only works for several hours, and the sensors are relatively large, so they should be worn on 2 parts of a patient's body (waist and left thigh). A compact and waist-worn type of triaxial accelerometer, the Actimarker (Panasonic; Osaka, Japan), can be operated continuously for more than 1 month and can evaluate the PA in patients with COPD more precisely, as well as in terms of the intensity of PA [14]. The limited parameters of the intensity of the PA in patients with COPD have been measured by arm-worn biaxial accelerometers [7,15]; however, such accelerometers are less accurate than waist-worn triaxial accelerometers [16], and PA with a limited intensity is less important than that of higher intensity for patients with COPD. Therefore, the intensity of PA in COPD is not clearly understood. Furthermore, as socioeconomic and ethnic factors appear to influence patients with stable COPD [17], more specific details pertaining to the PA in Japanese patients with COPD should be objectively evaluated. The aim of this study was to clarify the levels of PA in Japanese patients with COPD in terms of the intensity with a waist-worn triaxial accelerometer. Furthermore, we investigated whether pulmonary function, ADO index (age, dyspnea, and airflow obstruction), and modified BODE index (mBODE index; body mass index (BMI), airway obstruction, dyspnea, and exercise capacity) were associated with the PA in patients with COPD.
2.
Material and methods
2.1.
Subjects
Stable COPD patients (aged ≥60 years) without any other diseases that might interfere with walking were recruited from among the outpatients of Wakayama Medical University Hospital. COPD was diagnosed if the following condition existed: a post-bronchodilator forced expiratory volume in one second (FEV1.0)/forced viral capacity (FVC) of o0.7. The patients did not have any other pulmonary diseases, such as asthma or bronchiectasis [18]. Age-matched healthy subjects were recruited from among members of senior citizens' clubs in Wakayama City, Wakayama Prefecture and Sakai City, Osaka Prefecture, Japan. Subjects with a pre-bronchodilator
FEV1.0/FVC o0.7, an FEV1.0 %predicted o80%, or clinically evident diseases that might interfere with PA were excluded.
2.2.
Protocol
Patients with COPD were assessed in terms of their stage, according to their post-bronchodilator FEV1.0 upon entry. Then, they wore Actimarkers for 2 weeks and performed pre-bronchodilator pulmonary function tests and incremental shuttle walking tests (ISWT) on the last day of measurement. Healthy subjects wore Actimarkers for 2 weeks and performed pre-bronchodilator spirometries on the last day of measurement. Written informed consent was obtained from all participants, and the study was approved by the local ethics committee (Committee: IRB committee of Wakayama Medical University; authorization number: 968; date of approval: May 30, 2011).
2.3.
Assessment of PA
The Actimarker is a small (74.5 13.4 34.0 mm) and lightweight (36.0 g) accelerometer that is worn only at the waist and can be continuously monitored for over 1 month. It collects the data of triaxial acceleration at 20 Hz, and the standard deviation of the data for 1 min is defined as the mean value of acceleration. The value of metabolic equivalents (METs) is calculated from the linear regression formula produced by the relationship between the mean value of acceleration and the METs measured using a respiratory gas metabolic system [19]. Actimarker was already validated for evaluating the PA in COPD in terms of intensities [14]. From among the 2-week monitoring data, 3 non-rainy weekdays from the beginning, except the first and last days, were extracted, and the mean values of the PA duration from the extracted 3 days were employed as representative values of the PA for individuals according to a previous investigation [14]. For each intensity of PA, the reduction in PA with COPD was calculated as follows: 100 [(mean duration of PA in COPD)(mean duration of PA in healthy subjects)]/(mean duration of PA in healthy subjects).
2.4.
Assessment of physiological properties
The lung function was evaluated by CHESTAC-8800 DN type (Chest Ltd, Tokyo, Japan) for patients with COPD and HI-801 (Chest Ltd, Tokyo, Japan) for healthy subjects according to the recommendation of American Thoracic Society/European Respiratory Society [20]. ISWT was performed according to Singh's method (Japanese license number; 410) [21]. Dyspnea was evaluated with a modified Medical Research Council (MMRC) dyspnea scale [22], and modified BODE (mBODE) index, in which the original 6-min walking test [23] was substituted for the incremental shuttle walking test (point 0: 4350 m; 1: 250–349 m; 2: 150–249 m; and 3: o149 m).
2.5.
Statistical analysis
Statistical analysis was performed using GraphPad Prism 5 (GraphPad Software, San Diego, CA). The χ2 test and unpaired t test were used for comparing the characteristic variables.
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respiratory investigation 52 (2014) 41 –48
Mann–Whitney U test was used for the single comparison of the PA durations between healthy subjects and COPD patients. Oneway analysis of variance (ANOVA) was used together with post hoc multiple comparisons by Dunnett's test for the comparison between healthy subjects and the patients with each Global Initiative for Chronic Obstructive Lung Disease (GOLD) stage. Pearson correlation coefficients were used for the relationships among the PA duration, age, BMI, and ISWT. Spearman rank correlation coefficients were used for the relationships among the PA duration, MMRC, ADO index, and mBODE index. Significance was considered with a p-value of o0.05.
3.
Results
Forty-three patients with COPD and 21 age-matched healthy subjects were recruited. The numbers of patients with GOLD stages I, II, III, and IV were 8, 19, 9, and 7, respectively (Table 1). Thirty-four patients with COPD could perform the ISWT. The durations of PA in the COPD group were significantly reduced, as compared to those of the healthy subjects at all intensities (Fig. 1). The mean durations of PA in the COPD group were reduced by 23.1% at ≥2.0 METs, 33.0% at ≥2.5 METs, 50.9% at ≥3.0 METs, and 66.9% at ≥3.5 METs, as compared to those of the healthy subjects (Fig. 2). The durations of PA were significantly reduced as the GOLD stage progressed (≥2.0 METs, po0.001; ≥2.5 METs, p¼ 0.001; ≥3.0 METs, p ¼0.003; and ≥3.5 METs, p ¼0.030 by ANOVA), and the reduction was significant for the GOLD stage III patients at all intensities and GOLD stage IV patients at intensities that
were ≥2.0, ≥2.5, and ≥3.0 METs, as compared to those of the healthy subjects (Fig. 3). Among the pulmonary function tests, the FEV1.0 values were significantly correlated with the PA at all intensities, and the FVC values were correlated with the PA at ≥2.5, ≥3.0, and ≥3.5 METs. Although the values for the carbon monoxide diffusing capacity (DLCO) were not correlated with the PA, the values for the DLCO/alveolar volume (VA) were significantly correlated at intensities that were ≥2.5, ≥3.0, and ≥3.5 METs. The values of the lung volume subdivisions including functional residual capacity (FRC), residual volume (RV), total lung capacity (TLC), and inspiratory capacity (IC)/TLC were not correlated with the PA (Table 2). Age was weakly correlated with the PA at an intensity ≥3.5, and the MMRC and ISWT distance were correlated with the PA at all intensities. The complex indices, ADO index, and mBODE index were well correlated with the PA at all intensities (Table 3, Figs. 4 and 5).
4.
Discussion
In the current study, we examined the intensity of PA measured with a waist-worn triaxial accelerometer and demonstrated its reduction in Japanese patients with COPD compared to that of healthy subjects. The reduction in PA was prominent as the intensity of PA increased. The PA was significantly reduced at GOLD stage III at all intensities. The values of FVC, FEV1.0 and DLCO/VA, except lung volume, were correlated with the degree of PA. The ADO index and the mBODE index were well correlated with the PA at all intensities.
Table 1 – Characteristics of healthy subjects and COPD.
Gender [male/female] Age BMI (kg/m2) Smoking [non/ex/curr] [pack-years] COPD Stage (I/II/III/IV) Pulmonary function tests FVC (L) FVC % pred (%) FEV1.0 (L) FEV1.0/FVC (%) FEV1.0 % pred (%) FRC (L) FRC % pred (%) RV (L) RV % pred (%) TLC (L) TLC % pred (%) IC/TLC DLCO (mL/min/mmHg) DLCO % pred (%) DLCO/VA (mL/min/mmHg/L) DLCO/VA % pred (%)
HS
COPD
p-value
18/3 71.977.1 23.173.4 5/14/2 44.2726.3 –
42/1 72.676.8 20.973.6 0/36/7 64.7736.5 8/19/9/7
0.064 0.678 0.024 0.004 0.024 NA
104.6715.0 2.5670.51 77.076.1 100.6714.8 104.6715.0 NA NA NA NA NA NA NA NA NA NA NA
97.8714.9 1.5670.60 46.0713.5 57.5721.6 97.8714.9 4.1571.19 107.7728.8 2.7070.95 155.6753.1 6.2571.59 118.0728.7 33.279.6 13.076.3 89.6744.1 2.8871.41 66.9733.1
0.094 o0.0001 o0.0001 o0.0001 0.094 NA NA NA NA NA NA NA NA NA NA NA
HS ¼healthy subjects; BMI ¼ body mass index; non ¼non smoker; ex ¼ exsmoker; curr ¼ current smoker; FVC ¼ force vital capacity; FEV1.0¼ forced expiratory volume in one second; % pred ¼ % of predicted; FRC ¼functional residual capacity; RV ¼residual capacity; TLC ¼ total lung capacity; DLCO ¼ pulmonary carbon monoxide diffusing capacity; VA ¼alveolar volume; NA ¼ not available, COPD stages were diagnosed by postbronchodilator FEV1.0 at the entry, and pulmonary function tests were demonstarated as prebronchodilator values.
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respiratory investigation 52 (2014) 41 –48
Fig. 1 – Comparison of the durations of physical activity. Data are shown as box plots (each box represents the 25% percentile at the lower extreme of the box; the median at the central line of the box; and the 75% percentile at the upper extreme of the box). The minimum and maximum values are also depicted and correspond to the lines outside each box. Data were analyzed with Mann–Whitney U test. *: po0.05, †: po0.01, ‡: po0.005, as compared with healthy subjects. METs¼metabolic equivalents; HS¼ healthy subjects.
Fig. 2 – Mean reduction rate of physical activity in patients with COPD compared to healthy subjects. Mean reduction rate of physical activity (PA) in COPD was calculated as 100 [(mean duration of PA in COPD)(mean duration of PA in healthy subjects)]/(mean duration of PA in healthy subjects) at each intensity of PA. The durations of PA in patients with COPD were reduced at all intensities, and the PA at the intensities ≥2.0, ≥2.5, ≥3.0, and ≥3.5 METs in COPD were reduced by 23.1%, 33.0%, 50.9%, and 66.9%, respectively. The PA at 2.0, 2.5, 3.0, 3.3, and 3.8 METs were equivalent to walking on level ground at a speed
of o3.2 km/h, 3.2 km/h, 4.0 km/h, 4.8 km/h, and 5.6 km/h, respectively [24]. The ordinary walking speed of healthy adults is 4.0 km/h (3.0 METs). The current results indicated that the intensity of PA was greatly reduced in patients with COPD, as compared to that of the healthy subjects' ordinary walking speed, or faster. Reduced walking durations at an ordinary speed might cause the leg muscles to become weak. A reduction in the mid-thigh muscles or quadriceps was reported to be a better predictor of mortality in patients with COPD [25,26]. Troosters et al. evaluated the PA of Italian, Belgian, and American patients with COPD. They reported that the time spent in PA for patients with COPD at 2.5–3.6 METs with an age ≥65 years was reduced by 50% and at ≥3.6 METs with an age ≥65 years was reduced by 64%, compared to that of agematched control subjects [15]. These results were similar to ours. This suggests that the reduced rate of PA in COPD is fairly constant when compared to healthy subjects, regardless of the country, though PA with COPD is influenced by socioeconomic and ethnic factors [17]. The duration of PA was reduced as the GOLD stage progressed at all intensities, which is compatible with previous reports [6,15,27,28]. The PA was significantly reduced
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respiratory investigation 52 (2014) 41 –48
Fig. 3 – Relationship between GOLD stages and the duration of physical activity. Data are shown as box plots (each box represents the 25% percentile at the lower extreme of the box; the median at the central line of the box; and the 75% percentile at the upper extreme of the box). The minimum and maximum values are also depicted and correspond to the lines outside each box. *: po0.05; one-way analysis of variance with Dunnett's post hoc comparisons. METs¼ metabolic equivalents; HS¼healthy subjects. Table 2 – Correlation coefficients between duration of physical activity and pulmonary functions in COPD. ≥2.0 METs FVC % pred FEV1.0 % pred DLCO % pred DLCO/VA % pred FRC % pred RV % pred TLC % pred IC/TLC
0.372n 0.551‡ 0.144 0.116 0.082 0.169 0.161 0.048
≥2.5 METs †
0.398 0.545‡ 0.188 0.178 0.085 0.181 0.121 0.105
≥3.0 METs
≥3.5 METs
0.318n 0.500‡ 0.274 0.400n 0.043 0.235 0.164 0.121
0.163 0.337n 0.124 0.387n 0.150 0.246 0.200 0.101
METs ¼ metabolic equivalents; FVC ¼forced vital capacity; FEV1.0 ¼forced expiratory volume in one second; DLCO ¼ carbon monoxide diffusing capacity; VA ¼ alveolar volume; FRC ¼functional residual capacity; RV ¼residual volume; TLC ¼total lung capacity; IC ¼ inspiratory capacity; % pred ¼% of predicted value. Data recorded are Spearman's rank correlation coefficients. n po0.05. † po0.01. ‡ o0.005.
with GOLD stage III at all intensities. Watz et al. reported that the PA in patients with GOLD stages III and IV differed markedly from that of patients with earlier stages [28], which supports our results. Troosters et al. reported that the PA was significantly decreased with GOLD stage II [15]. In that report, however, the PA was evaluated with an arm-worn biaxial accelerometer, and the duration of PA, which was limited to moderate intensity, was employed for the index. An armworn biaxial accelerometer might overestimate the energy expenditure [29–31], and its reliability is lower than that of a waist-worn triaxial accelerometer [16]. Furthermore, the durations of PA were limited to moderate intensities and
did not include vigorous intensity, so they would not be suitable as representative indices of the PA of individuals. These factors might cause different results at different GOLD stages. Though a reduction in PA was not found with GOLD Stage IV at ≥3.5 METs, the duration of PA in this condition might be too short to detect statistically significant differences. The values of FEV1.0 were correlated with the durations of PA at all intensities, and the values of FVC and DLCO/VA were correlated with the durations of PA at some intensities, but the lung volume parameters were not. In most of the previous reports, in which the PA was measured with an
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respiratory investigation 52 (2014) 41 –48
Table 3 – Correlation coefficients between duration of physical activity and ADO and BODE indices in COPD.
Age BMI MMRC ISWT ADO index mBODE index
≥2.0 METs
≥2.5 METs
≥3.0 METs
≥3.5 METs
0.069 0.045 0.307n 0.529‡ 0.477‡ 0.594‡
0.142 0.070 0.379n 0.616‡ 0.508‡ 0.576‡
0.182 0.205 0.313n 0.540‡ 0.433‡ 0.503‡
0.357n 0.255 0.383n 0.389n 0.460‡ 0.426n
METs ¼metabolic equivalents; BMI ¼ body mass index; MMRC ¼modified Medical Research Council; ISWT ¼incremental shuttle walk test; ADO index ¼age, dyspnea, airflow obstruction; mBODE index¼ body mass index, air flow obstruction, dyspnea, exercise capacity (ISWT). Data of age, BMI and ISWT are Pearson's correlation coefficients, and data of MMRC, ADO index and mBODE index are Spearman's rank correlation coefficients. n po0.05. ‡ o0.005.
Fig. 4 – Correlation between ADO index and the duration of physical activity in COPD. Spearman rank correlation coefficient was used for analysis. ADO¼age, dyspnea, and airway obstruction.
accelerometer, FEV1.0 was weakly to moderately correlated with the PA [5,6,12,13]. The diffusing capacity was strongly correlated with PA, but the lung volume was not or only weakly correlated with the PA [12,27]. These results are compatible with our results. As FEV1.0 reflects the airway resistance and diffusing capacity reflects hypoxemia, especially during exercise [32], airway resistance and subclinical hypoxemia during movement might affect the PA in patients with COPD. This hypothesis was also supported by the finding that of 2 groups of patients with ISWT distances ≥250 m, which had an mBODE index of 0 or 1, those with the lowest oxygen saturation by pulse oximetry (SpO2) during ISWT of o90% showed durations of PA at intensities of ≥3.0 METs that were significantly shorter than in those with SpO2≥90% (SpO2o90%: 16.3717.3 min, n¼ 16; SpO2≥90%, 37.3723.4 min, n¼ 16; p¼ 0.013).
Though lung function was associated with the PA in this study, the relationship was weak. However, the complex indices, ADO index and mBODE index, were well correlated with the PA at all intensities. The BODE index was reported to reflect the PA [6,27,28], which was compatible with our data. We demonstrated that the ADO index reflects the PA for the first time. Both complex indices could be better predictors of PA, as well as of the prognosis of COPD [23,33]. Because the ADO index does not require exercise capacity, which requires stress testing, it could become a clinically useful predictor of PA in patients with COPD, compared with that of the mBODE index. In previous reports, the PA in patients with COPD was mainly evaluated according to the GOLD stages [6,15,27,28]. However, it would be better if it were evaluated according to the intensity of PA, because the walking speed of COPD patients is low [15], and
respiratory investigation 52 (2014) 41 –48
47
Fig. 5 – Correlation between modified BODE index and the duration of physical activity in COPD. Spearman rank correlation coefficient was used for analysis. BODE¼ body mass index, airway obstruction, dyspnea, and exercise capacity. the correlation between PA and FEV1.0 was weak [5,6,12,13]. In the current study, we could clearly and objectively demonstrate the inactivity of COPD in terms of the intensity of PA. The accelerometer itself might restrict the PA or reduce the wearing compliance because of its complexity and weight, especially in elderly patients. As the Actimarker is more user friendly and much lighter (36.0 g) than the previously reported ones [DAM 440 g, SenseWear (Bodymedia, Pittsburgh, PA) 80 g, and RT3 (StayHealthy, Monrovia, CA) 65.2 g] and was well validated in precisely detecting the PA in patients with COPD [14], it could become a useful tool for monitoring the PA in patients with COPD in general practice. This study had several limitations. First, the number of recruited patients was small. A larger study is necessary to further detail the features of PA in patients with COPD. Second, most of the subjects recruited for the present study were male, though the distribution of gender did not differ statistically between healthy subjects and COPD patients. As gender differences in skeletal muscle characteristics were not found in patients with COPD [34], we think the current results could also be applied to females. Third, potential comorbidities, including right heart overload, depression, osteoporosis, or muscular weakness, were not completely excluded, although the study subjects had not been diagnosed with comorbidities. It has been reported that up to 25% of the population older than 65 years has 2 comorbidities and up to 17% of that population has three [35]. The influence of comorbidities and muscular weakness on the PA in patients with COPD should be elucidated in future studies.
4.1.
Conclusions
In conclusion, the level of PA in Japanese patients with COPD was objectively demonstrated in terms of the intensity, and
the reduction was more prominent at the higher intensities. Airflow limitation and diffusing capacity were associated with PA. The ADO index and BODE index could be better predictors of the PA in patients with COPD. This intensitybased study of PA could provide us a new target for the management of COPD.
Conflict of interest The authors have no conflicts of interest.
Contributions Y. Minakata performed all the processes; A. Sugino and M. Kanda set and analyzed the accelerometer; and T. Ichikawa, K. Akamatsu, A. Koarai, T. Hirano, M. Nakanishi, H. Sugiura, K. Matsunaga, and M. Ichinose recruited subjects and modified the manuscript.
Acknowledgments The authors thank Mr. Manabu Nishigai for technical support and assistance with the statistical analysis; Mr. Yuichi Honda for support to attach an accelerometer; and Mr. Brent Bell for reading the manuscript. This study was supported by Grant H23-(3)-3 from the Environmental Restoration and Conservation Agency of Japan.
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Respiratory Investigation journal homepage: www.elsevier.com/locate/resinv
Original article
Reduced level of physical activity in Japanese patients with chronic obstructive pulmonary disease Yoshiaki Minakataa,n, Akihito Suginoa, Masae Kandaa, Tomohiro Ichikawaa, Keiichiro Akamatsua, Akira Koaraib, Tsunahiko Hiranoa, Masanori Nakanishia, Hisatoshi Sugiurab, Kazuto Matsunagaa, Masakazu Ichinoseb a
Third Department of Internal Medicine, Wakayama Medical University, Wakayama, Japan Department of Respiratory Medicine, Tohoku University Graduate School of Medicine, Miyagi, Japan
b
art i cle i nfo
ab st rac t
Article history:
Background: There is increasing interest in the quantification of physical activity (PA) with
Received 16 January 2013
an accelerometer for the management of chronic obstructive pulmonary disease (COPD).
Received in revised form
However, a detailed understanding of the PA in Japanese patients with COPD is lacking. We
3 June 2013
evaluated the levels of PA in terms of intensity in Japanese patients with COPD and
Accepted 10 June 2013
evaluated the factors, which could influence the PA.
Available online 18 July 2013
Methods: Forty-three outpatients with COPD and 21 age-matched healthy subjects were
Keywords: COPD Accelerometer Intensity BODE index ADO index
monitored with a triaxial accelerometer, and their PA was compared. Furthermore, the effects of pulmonary function, ADO index (age, dyspnea, and airflow obstruction) and modified BODE index (body mass index, airflow obstruction, dyspnea, and exercise capacity) on the PA were evaluated. Results: The PA in COPD was significantly reduced at all intensities. The reduced levels of PA in COPD were 23.1% at ≥2.0 metabolic equivalents (METs), 33.0% at ≥2.5 METs, 50.9% at ≥3.0 METs, and 66.9% at ≥3.5 METs, compared with that of healthy subjects, and the reduction was significant at GOLD stage III. The values of FVC, FEV1.0, and DLCO/VA were correlated with that of the PA, but the lung volume parameters were not. The ADO and modified BODE indices were also well correlated with the PA. Conclusions: The reduced levels of PA in Japanese patients with COPD were objectively demonstrated in terms of intensity that could provide us a new target for the management of COPD. & 2013 The Japanese Respiratory Society. Published by Elsevier B.V. All rights reserved.
Abbreviations: PA,
physical activity; ADO index,
index including age, dyspnea, and airflow obstruction; BODE index,
including body-mass index, airflow obstruction, dyspnea, and exercise capacity; METs,
metabolic equivalents; MMRC,
index
modified
Medical Research Council n Correspondence to: Third Department of Internal Medicine, Wakayama Medical University, 811-1 Kimiidera Wakayama, Wakayama, 641-0012, Japan. Tel.: 81 73 441 0619; fax: 81 73 446 2877. E-mail addresses: [email protected] (Y. Minakata), [email protected] (A. Sugino), [email protected] (M. Kanda), [email protected] (T. Ichikawa), [email protected] (K. Akamatsu), [email protected] (A. Koarai), [email protected] (T. Hirano), [email protected] (M. Nakanishi), [email protected] (H. Sugiura), [email protected] (K. Matsunaga), [email protected] (M. Ichinose). 2212-5345/$ - see front matter & 2013 The Japanese Respiratory Society. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.resinv.2013.06.002
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1.
respiratory investigation 52 (2014) 41 –48
Introduction
Patients with chronic obstructive pulmonary disease (COPD) are often limited in their daily physical activity (PA), and the level of PA is related to the decline in lung function [1], as well as hospitalizations [2,3] and mortality [4]. Therefore, the PA in patients with COPD has received increasing clinical interest. Recently, motion sensors, especially accelerometers, have been used to quantify the PA in patients with COPD [5–7], instead of questionnaires [8,9], which are less objective and reliable [10]. Among the reported accelerometers, the most reported and well-validated accelerometer for patients with COPD is the DynaPort Activity Monitor (DAM; McRoberts BV; The Hague, the Netherlands) [11–13]. However, it has several impediments to obtaining an accurate measurement of the PA, including the following: its battery only works for several hours, and the sensors are relatively large, so they should be worn on 2 parts of a patient's body (waist and left thigh). A compact and waist-worn type of triaxial accelerometer, the Actimarker (Panasonic; Osaka, Japan), can be operated continuously for more than 1 month and can evaluate the PA in patients with COPD more precisely, as well as in terms of the intensity of PA [14]. The limited parameters of the intensity of the PA in patients with COPD have been measured by arm-worn biaxial accelerometers [7,15]; however, such accelerometers are less accurate than waist-worn triaxial accelerometers [16], and PA with a limited intensity is less important than that of higher intensity for patients with COPD. Therefore, the intensity of PA in COPD is not clearly understood. Furthermore, as socioeconomic and ethnic factors appear to influence patients with stable COPD [17], more specific details pertaining to the PA in Japanese patients with COPD should be objectively evaluated. The aim of this study was to clarify the levels of PA in Japanese patients with COPD in terms of the intensity with a waist-worn triaxial accelerometer. Furthermore, we investigated whether pulmonary function, ADO index (age, dyspnea, and airflow obstruction), and modified BODE index (mBODE index; body mass index (BMI), airway obstruction, dyspnea, and exercise capacity) were associated with the PA in patients with COPD.
2.
Material and methods
2.1.
Subjects
Stable COPD patients (aged ≥60 years) without any other diseases that might interfere with walking were recruited from among the outpatients of Wakayama Medical University Hospital. COPD was diagnosed if the following condition existed: a post-bronchodilator forced expiratory volume in one second (FEV1.0)/forced viral capacity (FVC) of o0.7. The patients did not have any other pulmonary diseases, such as asthma or bronchiectasis [18]. Age-matched healthy subjects were recruited from among members of senior citizens' clubs in Wakayama City, Wakayama Prefecture and Sakai City, Osaka Prefecture, Japan. Subjects with a pre-bronchodilator
FEV1.0/FVC o0.7, an FEV1.0 %predicted o80%, or clinically evident diseases that might interfere with PA were excluded.
2.2.
Protocol
Patients with COPD were assessed in terms of their stage, according to their post-bronchodilator FEV1.0 upon entry. Then, they wore Actimarkers for 2 weeks and performed pre-bronchodilator pulmonary function tests and incremental shuttle walking tests (ISWT) on the last day of measurement. Healthy subjects wore Actimarkers for 2 weeks and performed pre-bronchodilator spirometries on the last day of measurement. Written informed consent was obtained from all participants, and the study was approved by the local ethics committee (Committee: IRB committee of Wakayama Medical University; authorization number: 968; date of approval: May 30, 2011).
2.3.
Assessment of PA
The Actimarker is a small (74.5 13.4 34.0 mm) and lightweight (36.0 g) accelerometer that is worn only at the waist and can be continuously monitored for over 1 month. It collects the data of triaxial acceleration at 20 Hz, and the standard deviation of the data for 1 min is defined as the mean value of acceleration. The value of metabolic equivalents (METs) is calculated from the linear regression formula produced by the relationship between the mean value of acceleration and the METs measured using a respiratory gas metabolic system [19]. Actimarker was already validated for evaluating the PA in COPD in terms of intensities [14]. From among the 2-week monitoring data, 3 non-rainy weekdays from the beginning, except the first and last days, were extracted, and the mean values of the PA duration from the extracted 3 days were employed as representative values of the PA for individuals according to a previous investigation [14]. For each intensity of PA, the reduction in PA with COPD was calculated as follows: 100 [(mean duration of PA in COPD)(mean duration of PA in healthy subjects)]/(mean duration of PA in healthy subjects).
2.4.
Assessment of physiological properties
The lung function was evaluated by CHESTAC-8800 DN type (Chest Ltd, Tokyo, Japan) for patients with COPD and HI-801 (Chest Ltd, Tokyo, Japan) for healthy subjects according to the recommendation of American Thoracic Society/European Respiratory Society [20]. ISWT was performed according to Singh's method (Japanese license number; 410) [21]. Dyspnea was evaluated with a modified Medical Research Council (MMRC) dyspnea scale [22], and modified BODE (mBODE) index, in which the original 6-min walking test [23] was substituted for the incremental shuttle walking test (point 0: 4350 m; 1: 250–349 m; 2: 150–249 m; and 3: o149 m).
2.5.
Statistical analysis
Statistical analysis was performed using GraphPad Prism 5 (GraphPad Software, San Diego, CA). The χ2 test and unpaired t test were used for comparing the characteristic variables.
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respiratory investigation 52 (2014) 41 –48
Mann–Whitney U test was used for the single comparison of the PA durations between healthy subjects and COPD patients. Oneway analysis of variance (ANOVA) was used together with post hoc multiple comparisons by Dunnett's test for the comparison between healthy subjects and the patients with each Global Initiative for Chronic Obstructive Lung Disease (GOLD) stage. Pearson correlation coefficients were used for the relationships among the PA duration, age, BMI, and ISWT. Spearman rank correlation coefficients were used for the relationships among the PA duration, MMRC, ADO index, and mBODE index. Significance was considered with a p-value of o0.05.
3.
Results
Forty-three patients with COPD and 21 age-matched healthy subjects were recruited. The numbers of patients with GOLD stages I, II, III, and IV were 8, 19, 9, and 7, respectively (Table 1). Thirty-four patients with COPD could perform the ISWT. The durations of PA in the COPD group were significantly reduced, as compared to those of the healthy subjects at all intensities (Fig. 1). The mean durations of PA in the COPD group were reduced by 23.1% at ≥2.0 METs, 33.0% at ≥2.5 METs, 50.9% at ≥3.0 METs, and 66.9% at ≥3.5 METs, as compared to those of the healthy subjects (Fig. 2). The durations of PA were significantly reduced as the GOLD stage progressed (≥2.0 METs, po0.001; ≥2.5 METs, p¼ 0.001; ≥3.0 METs, p ¼0.003; and ≥3.5 METs, p ¼0.030 by ANOVA), and the reduction was significant for the GOLD stage III patients at all intensities and GOLD stage IV patients at intensities that
were ≥2.0, ≥2.5, and ≥3.0 METs, as compared to those of the healthy subjects (Fig. 3). Among the pulmonary function tests, the FEV1.0 values were significantly correlated with the PA at all intensities, and the FVC values were correlated with the PA at ≥2.5, ≥3.0, and ≥3.5 METs. Although the values for the carbon monoxide diffusing capacity (DLCO) were not correlated with the PA, the values for the DLCO/alveolar volume (VA) were significantly correlated at intensities that were ≥2.5, ≥3.0, and ≥3.5 METs. The values of the lung volume subdivisions including functional residual capacity (FRC), residual volume (RV), total lung capacity (TLC), and inspiratory capacity (IC)/TLC were not correlated with the PA (Table 2). Age was weakly correlated with the PA at an intensity ≥3.5, and the MMRC and ISWT distance were correlated with the PA at all intensities. The complex indices, ADO index, and mBODE index were well correlated with the PA at all intensities (Table 3, Figs. 4 and 5).
4.
Discussion
In the current study, we examined the intensity of PA measured with a waist-worn triaxial accelerometer and demonstrated its reduction in Japanese patients with COPD compared to that of healthy subjects. The reduction in PA was prominent as the intensity of PA increased. The PA was significantly reduced at GOLD stage III at all intensities. The values of FVC, FEV1.0 and DLCO/VA, except lung volume, were correlated with the degree of PA. The ADO index and the mBODE index were well correlated with the PA at all intensities.
Table 1 – Characteristics of healthy subjects and COPD.
Gender [male/female] Age BMI (kg/m2) Smoking [non/ex/curr] [pack-years] COPD Stage (I/II/III/IV) Pulmonary function tests FVC (L) FVC % pred (%) FEV1.0 (L) FEV1.0/FVC (%) FEV1.0 % pred (%) FRC (L) FRC % pred (%) RV (L) RV % pred (%) TLC (L) TLC % pred (%) IC/TLC DLCO (mL/min/mmHg) DLCO % pred (%) DLCO/VA (mL/min/mmHg/L) DLCO/VA % pred (%)
HS
COPD
p-value
18/3 71.977.1 23.173.4 5/14/2 44.2726.3 –
42/1 72.676.8 20.973.6 0/36/7 64.7736.5 8/19/9/7
0.064 0.678 0.024 0.004 0.024 NA
104.6715.0 2.5670.51 77.076.1 100.6714.8 104.6715.0 NA NA NA NA NA NA NA NA NA NA NA
97.8714.9 1.5670.60 46.0713.5 57.5721.6 97.8714.9 4.1571.19 107.7728.8 2.7070.95 155.6753.1 6.2571.59 118.0728.7 33.279.6 13.076.3 89.6744.1 2.8871.41 66.9733.1
0.094 o0.0001 o0.0001 o0.0001 0.094 NA NA NA NA NA NA NA NA NA NA NA
HS ¼healthy subjects; BMI ¼ body mass index; non ¼non smoker; ex ¼ exsmoker; curr ¼ current smoker; FVC ¼ force vital capacity; FEV1.0¼ forced expiratory volume in one second; % pred ¼ % of predicted; FRC ¼functional residual capacity; RV ¼residual capacity; TLC ¼ total lung capacity; DLCO ¼ pulmonary carbon monoxide diffusing capacity; VA ¼alveolar volume; NA ¼ not available, COPD stages were diagnosed by postbronchodilator FEV1.0 at the entry, and pulmonary function tests were demonstarated as prebronchodilator values.
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respiratory investigation 52 (2014) 41 –48
Fig. 1 – Comparison of the durations of physical activity. Data are shown as box plots (each box represents the 25% percentile at the lower extreme of the box; the median at the central line of the box; and the 75% percentile at the upper extreme of the box). The minimum and maximum values are also depicted and correspond to the lines outside each box. Data were analyzed with Mann–Whitney U test. *: po0.05, †: po0.01, ‡: po0.005, as compared with healthy subjects. METs¼metabolic equivalents; HS¼ healthy subjects.
Fig. 2 – Mean reduction rate of physical activity in patients with COPD compared to healthy subjects. Mean reduction rate of physical activity (PA) in COPD was calculated as 100 [(mean duration of PA in COPD)(mean duration of PA in healthy subjects)]/(mean duration of PA in healthy subjects) at each intensity of PA. The durations of PA in patients with COPD were reduced at all intensities, and the PA at the intensities ≥2.0, ≥2.5, ≥3.0, and ≥3.5 METs in COPD were reduced by 23.1%, 33.0%, 50.9%, and 66.9%, respectively. The PA at 2.0, 2.5, 3.0, 3.3, and 3.8 METs were equivalent to walking on level ground at a speed
of o3.2 km/h, 3.2 km/h, 4.0 km/h, 4.8 km/h, and 5.6 km/h, respectively [24]. The ordinary walking speed of healthy adults is 4.0 km/h (3.0 METs). The current results indicated that the intensity of PA was greatly reduced in patients with COPD, as compared to that of the healthy subjects' ordinary walking speed, or faster. Reduced walking durations at an ordinary speed might cause the leg muscles to become weak. A reduction in the mid-thigh muscles or quadriceps was reported to be a better predictor of mortality in patients with COPD [25,26]. Troosters et al. evaluated the PA of Italian, Belgian, and American patients with COPD. They reported that the time spent in PA for patients with COPD at 2.5–3.6 METs with an age ≥65 years was reduced by 50% and at ≥3.6 METs with an age ≥65 years was reduced by 64%, compared to that of agematched control subjects [15]. These results were similar to ours. This suggests that the reduced rate of PA in COPD is fairly constant when compared to healthy subjects, regardless of the country, though PA with COPD is influenced by socioeconomic and ethnic factors [17]. The duration of PA was reduced as the GOLD stage progressed at all intensities, which is compatible with previous reports [6,15,27,28]. The PA was significantly reduced
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respiratory investigation 52 (2014) 41 –48
Fig. 3 – Relationship between GOLD stages and the duration of physical activity. Data are shown as box plots (each box represents the 25% percentile at the lower extreme of the box; the median at the central line of the box; and the 75% percentile at the upper extreme of the box). The minimum and maximum values are also depicted and correspond to the lines outside each box. *: po0.05; one-way analysis of variance with Dunnett's post hoc comparisons. METs¼ metabolic equivalents; HS¼healthy subjects. Table 2 – Correlation coefficients between duration of physical activity and pulmonary functions in COPD. ≥2.0 METs FVC % pred FEV1.0 % pred DLCO % pred DLCO/VA % pred FRC % pred RV % pred TLC % pred IC/TLC
0.372n 0.551‡ 0.144 0.116 0.082 0.169 0.161 0.048
≥2.5 METs †
0.398 0.545‡ 0.188 0.178 0.085 0.181 0.121 0.105
≥3.0 METs
≥3.5 METs
0.318n 0.500‡ 0.274 0.400n 0.043 0.235 0.164 0.121
0.163 0.337n 0.124 0.387n 0.150 0.246 0.200 0.101
METs ¼ metabolic equivalents; FVC ¼forced vital capacity; FEV1.0 ¼forced expiratory volume in one second; DLCO ¼ carbon monoxide diffusing capacity; VA ¼ alveolar volume; FRC ¼functional residual capacity; RV ¼residual volume; TLC ¼total lung capacity; IC ¼ inspiratory capacity; % pred ¼% of predicted value. Data recorded are Spearman's rank correlation coefficients. n po0.05. † po0.01. ‡ o0.005.
with GOLD stage III at all intensities. Watz et al. reported that the PA in patients with GOLD stages III and IV differed markedly from that of patients with earlier stages [28], which supports our results. Troosters et al. reported that the PA was significantly decreased with GOLD stage II [15]. In that report, however, the PA was evaluated with an arm-worn biaxial accelerometer, and the duration of PA, which was limited to moderate intensity, was employed for the index. An armworn biaxial accelerometer might overestimate the energy expenditure [29–31], and its reliability is lower than that of a waist-worn triaxial accelerometer [16]. Furthermore, the durations of PA were limited to moderate intensities and
did not include vigorous intensity, so they would not be suitable as representative indices of the PA of individuals. These factors might cause different results at different GOLD stages. Though a reduction in PA was not found with GOLD Stage IV at ≥3.5 METs, the duration of PA in this condition might be too short to detect statistically significant differences. The values of FEV1.0 were correlated with the durations of PA at all intensities, and the values of FVC and DLCO/VA were correlated with the durations of PA at some intensities, but the lung volume parameters were not. In most of the previous reports, in which the PA was measured with an
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respiratory investigation 52 (2014) 41 –48
Table 3 – Correlation coefficients between duration of physical activity and ADO and BODE indices in COPD.
Age BMI MMRC ISWT ADO index mBODE index
≥2.0 METs
≥2.5 METs
≥3.0 METs
≥3.5 METs
0.069 0.045 0.307n 0.529‡ 0.477‡ 0.594‡
0.142 0.070 0.379n 0.616‡ 0.508‡ 0.576‡
0.182 0.205 0.313n 0.540‡ 0.433‡ 0.503‡
0.357n 0.255 0.383n 0.389n 0.460‡ 0.426n
METs ¼metabolic equivalents; BMI ¼ body mass index; MMRC ¼modified Medical Research Council; ISWT ¼incremental shuttle walk test; ADO index ¼age, dyspnea, airflow obstruction; mBODE index¼ body mass index, air flow obstruction, dyspnea, exercise capacity (ISWT). Data of age, BMI and ISWT are Pearson's correlation coefficients, and data of MMRC, ADO index and mBODE index are Spearman's rank correlation coefficients. n po0.05. ‡ o0.005.
Fig. 4 – Correlation between ADO index and the duration of physical activity in COPD. Spearman rank correlation coefficient was used for analysis. ADO¼age, dyspnea, and airway obstruction.
accelerometer, FEV1.0 was weakly to moderately correlated with the PA [5,6,12,13]. The diffusing capacity was strongly correlated with PA, but the lung volume was not or only weakly correlated with the PA [12,27]. These results are compatible with our results. As FEV1.0 reflects the airway resistance and diffusing capacity reflects hypoxemia, especially during exercise [32], airway resistance and subclinical hypoxemia during movement might affect the PA in patients with COPD. This hypothesis was also supported by the finding that of 2 groups of patients with ISWT distances ≥250 m, which had an mBODE index of 0 or 1, those with the lowest oxygen saturation by pulse oximetry (SpO2) during ISWT of o90% showed durations of PA at intensities of ≥3.0 METs that were significantly shorter than in those with SpO2≥90% (SpO2o90%: 16.3717.3 min, n¼ 16; SpO2≥90%, 37.3723.4 min, n¼ 16; p¼ 0.013).
Though lung function was associated with the PA in this study, the relationship was weak. However, the complex indices, ADO index and mBODE index, were well correlated with the PA at all intensities. The BODE index was reported to reflect the PA [6,27,28], which was compatible with our data. We demonstrated that the ADO index reflects the PA for the first time. Both complex indices could be better predictors of PA, as well as of the prognosis of COPD [23,33]. Because the ADO index does not require exercise capacity, which requires stress testing, it could become a clinically useful predictor of PA in patients with COPD, compared with that of the mBODE index. In previous reports, the PA in patients with COPD was mainly evaluated according to the GOLD stages [6,15,27,28]. However, it would be better if it were evaluated according to the intensity of PA, because the walking speed of COPD patients is low [15], and
respiratory investigation 52 (2014) 41 –48
47
Fig. 5 – Correlation between modified BODE index and the duration of physical activity in COPD. Spearman rank correlation coefficient was used for analysis. BODE¼ body mass index, airway obstruction, dyspnea, and exercise capacity. the correlation between PA and FEV1.0 was weak [5,6,12,13]. In the current study, we could clearly and objectively demonstrate the inactivity of COPD in terms of the intensity of PA. The accelerometer itself might restrict the PA or reduce the wearing compliance because of its complexity and weight, especially in elderly patients. As the Actimarker is more user friendly and much lighter (36.0 g) than the previously reported ones [DAM 440 g, SenseWear (Bodymedia, Pittsburgh, PA) 80 g, and RT3 (StayHealthy, Monrovia, CA) 65.2 g] and was well validated in precisely detecting the PA in patients with COPD [14], it could become a useful tool for monitoring the PA in patients with COPD in general practice. This study had several limitations. First, the number of recruited patients was small. A larger study is necessary to further detail the features of PA in patients with COPD. Second, most of the subjects recruited for the present study were male, though the distribution of gender did not differ statistically between healthy subjects and COPD patients. As gender differences in skeletal muscle characteristics were not found in patients with COPD [34], we think the current results could also be applied to females. Third, potential comorbidities, including right heart overload, depression, osteoporosis, or muscular weakness, were not completely excluded, although the study subjects had not been diagnosed with comorbidities. It has been reported that up to 25% of the population older than 65 years has 2 comorbidities and up to 17% of that population has three [35]. The influence of comorbidities and muscular weakness on the PA in patients with COPD should be elucidated in future studies.
4.1.
Conclusions
In conclusion, the level of PA in Japanese patients with COPD was objectively demonstrated in terms of the intensity, and
the reduction was more prominent at the higher intensities. Airflow limitation and diffusing capacity were associated with PA. The ADO index and BODE index could be better predictors of the PA in patients with COPD. This intensitybased study of PA could provide us a new target for the management of COPD.
Conflict of interest The authors have no conflicts of interest.
Contributions Y. Minakata performed all the processes; A. Sugino and M. Kanda set and analyzed the accelerometer; and T. Ichikawa, K. Akamatsu, A. Koarai, T. Hirano, M. Nakanishi, H. Sugiura, K. Matsunaga, and M. Ichinose recruited subjects and modified the manuscript.
Acknowledgments The authors thank Mr. Manabu Nishigai for technical support and assistance with the statistical analysis; Mr. Yuichi Honda for support to attach an accelerometer; and Mr. Brent Bell for reading the manuscript. This study was supported by Grant H23-(3)-3 from the Environmental Restoration and Conservation Agency of Japan.
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