Introduction

Chronic obstructive pulmonary disease (COPD) is characterized by airflow limitation, dyspnea, and reduction in exercise capacity, muscle strength, and quality of life [1]. Patients with COPD are frequently characterized by abnormalities in their body composition such as weight loss and fat-free mass depletion, and it is known that reduced body mass index (BMI) and fat-free mass index (FFMI) are independent predictors of mortality in these patients [2–5]. However, recent studies indicate that obesity has become increasingly common in patients with COPD [6–8]. Physical activity in daily life (PADL) is also often reduced in patients with COPD [9, 10] and as described for the alterations in body composition, reduction in PADL is a modifiable risk factor for morbidity and mortality [11, 12]. Public health guidelines regarding physical activity published by the American College of Sports Medicine (ACSM) recommend that a minimum of 30 min of physical activity of moderate intensity (e.g., walking) is necessary for the maintenance or development of physical fitness [13].

In the general population, it is known that physical inactivity is strongly related to obesity [14]. However, this is not necessarily the same in patients with COPD due to the obesity paradox. Despite obesity being characterized by an increased ventilatory demand and work of breathing, respiratory muscle inefficiency, reduced respiratory compliance, and increased dyspnea [15], the literature show that obese patients with COPD have a better prognosis of the disease and less pronounced airway obstruction than patients with normal BMI [2, 4, 8]. Moreover, although previous studies have shown that obese patients with COPD have lower functional exercise capacity [6, 8], other studies found that obese and overweight patients with COPD have higher peak VO2 and similar or reduced perception of dyspnea (due to reduced rest and dynamic hyperinflation) than their lean counterparts [16, 17]. Explanation for these apparently contradictory findings may be linked to the different characteristics of exercise assessment (walking versus cycling and submaximal versus maximal), among other factors. Therefore, taking into account the complex interaction between these conditions (obesity, exercise, and COPD), the relationship between obesity and PADL in these patients is unclear. New knowledge in this matter is relevant since obesity and physical inactivity are global phenomena, both associated with a worse prognosis in COPD.

Therefore, the present study had as its primary aim to determine if there are differences in body composition between active and inactive patients with COPD (according to the ACSM recommendations). It also aimed to verify whether obese patients have a lower level of PADL and worse functional exercise capacity than underweight, normal weight, and overweight patients and to investigate if there are differences in functional exercise capacity and PADL between levels of obesity, according to the percentage of fat mass.

Methods

Sample and Inclusion and Exclusion Criteria

Seventy-four patients with COPD (45 men, 65 ± 9 years old, FEV1 = 40 ± 15%pred, BMI = 27 ± 6 kg m−2) were included in this cross-sectional study. Patients were enrolled at the Pulmonary Outpatient Clinic of a university hospital (State University of Londrina, Brazil). Diagnosis of COPD was based on the Global Initiative for Chronic Obstructive Lung Disease criteria [1]. As inclusion criteria, patients had to be in stable condition (no exacerbations in the last 3 months that required a change in medication or hospital admission), had not participated in any exercise training program in the last year before admission to the study, and did not have other pathological conditions that could impair their performance, such as cerebrovascular, orthopedic, or rheumatic disease. Exclusion criteria were the occurrence of severe acute exacerbation requiring hospitalization during the assessment period and the inability to understand or cooperate with the assessment methods. The ethics committee of Londrina University Hospital approved the research protocol and a signed consent form was obtained from each patient.

Assessments

Pulmonary function (spirometry) was performed using a Pony Graphics® spirometer (Cosmed, Rome, Italy) according to international recommendations [18]. Reference values used were those of Pereira et al. [19].

Functional exercise capacity was evaluated by the 6-minute walking test (6MWT). Standards used were those recommended by the American Thoracic Society [20]. Two tests were performed (with at least a 30-min interval) and the best distance of the two tests was used. Reference values were those described by Troosters et al. [21].

Body composition analysis was performed by bioelectrical impedance (Biodynamics 310™, Biodynamics Corp., Seattle, WA, USA) (BIA), using the technique described by Lukaski et al. [22]. Reference values used were those described by Kyle et al. [23] specifically for patients with chronic lung disease. BMI was calculated by dividing weight by height squared, and FFMI was calculated by dividing the weight of FFM (obtained by BIA) by height squared.

Assessment of PADL was performed simultaneously by two activity monitors: the accelerometer-based DynaPort Activity Monitor (DAM) (McRoberts BV, The Hague, the Netherlands) and the multisensor SenseWear Armband (SAB) (BodyMedia Inc., Pittsburgh, PA, USA). The DAM consists of a small, lightweight box enclosed in a belt worn around the waist and a leg sensor (total weight = 375 g). The DAM was shown to be as accurate as video recordings (criterion method) in order to assess time spent in different activities by patients with COPD, such as the time spent walking/day (TW) [24]. Technical specifications about the DAM can be found elsewhere [24]. The SAB is a lightweight (80 g) activity monitor worn on the triceps brachial bulk of the right arm. The device estimates energy expenditure based on a biaxial accelerometer and physiologic sensors that detect galvanic skin response, heat flux, and skin temperature in a manufacturer’s algorithm. It also provides the duration of activities performed above a determined level of intensity (e.g., time spent per day in activities of at least moderate intensity, or TPA > moderate). The SAB was already validated for the estimate of energy expenditure in patients with COPD [25–28].

The main outcomes of the PADL assessment were TW (from the DynaPort) and TPA > moderate (from the SenseWear). Assessments with both activity monitors were performed over two consecutive weekdays, for 12 h per day (from wake-up time to 12 h after waking). The mean of the two assessment days was used for statistical analysis, and the minimal number of days needed to obtain a reliable assessment of daily physical activity was determined in a previous study [9].

For analysis, patients were first divided into two groups according to the minimum recommended daily physical activity determined by the ACSM [13]: active (performed more than 30 min/day of TPA > moderate) and inactive (did not achieve this recommendation). The threshold of metabolic equivalents (METs) to characterize an activity as at least of moderate intensity was also suggested by the ACSM as between 4.0 and 5.9 METs for subjects 40–64 years old and between 3.2 and 4.7 METs for subjects ≥65 years old [13]. Data obtained from the SAB were reanalyzed for every patient using these customized ACSM thresholds instead of the three METs threshold usually given by the SAB software. Secondarily, the same group was divided according to the BMI classification suggested for patients with COPD by the ATS-ERS Statement of Pulmonary Rehabilitation [29] into underweight [UW] (BMI < 21 kg m−2), normal weight [NW] (21 ≤ BMI < 25 kg m−2), overweight [OW] (25 ≤ BMI < 30 kg m−2), and obese [OB] (BMI > 30 kg m−2). Finally, the group was divided according to the percentage of fat mass (%FM) into nonobese (women [W]: < 25%FM; men [M]: < 15%FM); mild obesity (W: 25 ≤ %FM < 30; M: 15 ≤ %FM < 20); moderate obesity [MO] (W: 30 ≤ %FM < 35; M: 20 ≤ %FM < 25), high obesity [HO] (W: 35 ≤ %FM < 40; M: 25 ≤ %FM < 30) and morbid obesity [MbO] (W: %FM ≥ 40; M: %FM ≥ 30) [30].

Statistical Analysis

Statistical analysis was performed using the SPSS statistical package software ver. 17.0 (SPSS Inc., Chicago, IL, USA) and GraphPad Prism 3.0 (GraphPad Software, San Diego, CA, USA) programs. The Kolmogorov–Smirnov test was used to check for normal distribution. Comparisons between groups were performed using Student’s t-test or the Mann–Whitney test, and one-way ANOVA or Kruskal–Wallis, followed by a post-hoc test (Bonferroni or Dunns, respectively). Correlations were studied using the Pearson or Spearman coefficient, according to the normality in data distribution. To verify the similarity in gender between the groups, the χ2 test was used. A significance level of p ≤ 0.05 was adopted.

Results

Body Composition and Patients’ Characteristics (Active vs. Inactive)

According to the ACSM guidelines, 70% of the 74 patients included in the study were classified as physically inactive (52 vs. 22 physically active). Results of the whole group and differences in body composition between physically active and inactive subgroups are given in Table 1. Physically active and inactive patients with COPD had important differences in their body composition. Inactive patients had higher body weight (p = 0.002), BMI (p = 0.001), and FM (p = 0.004). Because of the higher body weight, the inactive group had higher absolute values of FFM (p = 0.05). However, when analyzing FFM as % of body weight, the inactive group had significantly lower values (p = 0.03).

Table 1 Results from the general group of patients with chronic obstructive pulmonary disease (COPD) and the physically active and inactive subgroups according to American College of Sports Medicine (ACSM) minimum recommendations of daily physical activity
Full size table

In the whole group, TPA > moderate correlated weakly and significantly with weight (r = −0.29; p = 0.02), BMI (r = −0.28; p = 0.02), and FM (r = −0.30; p = 0.001), but not with FFM (r = −0.18; p = 0.13). Correlation between BMI and %FM was r = 0.47; p < 0.0001. The 6MWT was significantly lower in inactive patients, whereas the active and inactive subgroups did not differ in their airway obstruction (Table 1).

Classification According to BMI

When the whole group was divided according to BMI, 19% of the patients were UW, 23% were NW, 30% were OW, and 28% were OB. Table 2 shows that when comparing the four groups with respect to level of PADL, the OB group had significantly lower TW than the UW group and the NW group, and significantly lower TPA > moderate than the UW group (p < 0.05 for all). No differences were found between the OW group and the other three groups (UW, NW, and OB). Despite the differences in PADL between the OB group vs. the UW and NW groups, the groups did not differ significantly in the 6MWT, although there was an average difference of 54 m between the OB group and the UW group and 41 m between the OB group and the NW group.

Table 2 Comparison of patients with chronic obstructive pulmonary disease (COPD) classified according to the body composition based on the body mass index (BMI)
Full size table

Classification According to %FM

As for the classification according to the %FM, no subject in the present sample could be classified as nonobese. Three patients had mild obesity and were therefore excluded from subsequent analysis. Table 3 offers a detailed overview of the differences between MO, HO, and MbO in patients with COPD. Concerning PADL, significant differences were found in TW (MbO vs. MO and vs. HO) and TPA > moderate (MO vs. MbO and vs. HO). A poorer 6MWT occurred with morbidly obese patients (Table 3).

Table 3 Comparison of patients with chronic obstructive pulmonary disease (COPD) classified according to the body composition based on the percentage of fat mass (FM%)
Full size table

Discussion

This study showed that despite physically active and inactive patients with COPD having similar age, level of airway obstruction, and gender proportion, inactive patients have less FFM and more FM (in % of body weight) than their active counterparts. In addition, time spent in activities of at least moderate intensity (as classified by the ACSM) has weak correlation with BMI and absolute values of FM but no correlation with FFM. Almost 30% of the patients were obese according to the classification based on the BMI. On the other hand, when using percentage of fat mass to classify obesity, 100% of patients were classified as obese, either mildly, moderately, highly, or morbidly. Obese patients had a worse level of daily physical activity than underweight and normal-weight patients. Moreover, higher degrees of obesity (according to %FM) are related to more impaired PADL and worse functional exercise capacity.

It is widely known that patients with COPD have important alterations in body composition and this is an independent predictor of mortality [4]. We now observed that inactive patients with COPD have higher body weight and BMI, and this was mainly caused by higher weight of fat mass. The inactive subgroup had higher absolute values of FFM, but this was due to the fact that these subjects had higher body weight, since FFM as % of body weight was significantly lower in this group. Moreover, although weakly, FM was significantly correlated with the level of PADL, which was not the case regarding FFM. These results suggest that in COPD, obesity is somewhat better linked to physical inactivity than loss of FFM, although none of the two factors appear to be a strong correlate of the level of PADL in this population. This corroborates previous findings by Watz et al. [31], who studied the determinants of objectively measured physical activity in patients with COPD. These authors also concluded that BMI was not a determining factor for PADL level. Other studies also did not find BMI to be a strong correlate of the level of physical activity in daily life in patients with COPD [9, 32, 33].

Obesity is known as an important issue in COPD and BMI is the most used variable to identify obesity in these patients. The literature reports obesity prevalence (according to BMI) in COPD as ranging between 18% [34] and 54% [35]. In the present study, 28% of the patients were obese according to their BMI. Our results showed that obese patients (BMI ≥ 30 kg m−2) are less active than underweight and normal-weight patients with COPD but not in comparison to overweight patients. Similar results were found in a study of older healthy adults in whom obesity but not being overweight was associated with lower levels of physical activity [36].

Although differences in the 6MWT between the groups classified according to BMI did not reach statistical significance, our data showed that obese patients walked an average of 54 m less than underweight patients and 41 m less than normal-weight patients, values that are well above the two values for minimal clinically important difference recently suggested for the 6MWT in the literature (25 and 35 m) [37, 38]. Therefore, despite not reaching statistical significance, a worse functional exercise capacity in obese patients appears to be clinically relevant. The previous literature has shown that higher BMI is associated with lower functional exercise capacity [8, 15, 39] and this is likely the result of the increase in energy expenditure associated with weight-bearing exercise [40]. Furthermore, previous studies showed that the combined mechanical effects of obesity and COPD increase peak oxygen uptake and reduce the dyspnea perception during exercise (cycle ergometry) [16, 17]. These favorable effects caused by obesity are explained by the less pronounced dynamic hyperinflation that is commonly found in obese patients with COPD.

BMI is the most used outcome to classify obesity, although it does not provide clear information about the distribution of FM and FFM. Patients with COPD commonly develop cachexia which is caused by different factors such as increased metabolic rate, hypoxemia, sympathetic upregulation, inactivity, oxidative stress, inflammation, and anabolic hormone insufficiency [41]. This reduction in percentage of FFM leads to a higher proportion of fat mass, even though the patient’s weight is not necessarily high. This explains the fact that 100% of the present sample was classified as obese based on the %FM, with 42% classified as morbidly obese. A study by Park et al. [42], which verified the relationship of body composition with PADL in adult women, suggested that the relationship between obesity and daily physical activity should be discussed using not only BMI but also fat mass index or %FM since these two variables were related to the physical activity level, which was corroborated by the present results. Obesity is defined as excessive accumulation of fat mass, and patients with COPD present high %FM despite not having high body weight. In addition, our data showed that more pronounced levels of obesity (i.e., morbid obesity) denote lower levels of PADL and lower exercise capacity in comparison to moderate obesity. Corroborating these results, the study by Park et al. [42] in older women showed that those with more pronounced obesity (according to %FM) had taken fewer steps per day and performed less moderate and vigorous physical activity. We believe that this is not necessarily caused only by changes due to excessive weight but also by a reduction in the percentage of muscle mass.

It was interesting to observe that as with BMI, the correlation between %FM and PADL in our sample of patients with COPD was weak. Studies of other populations already reported that PADL appears to be negatively associated with FM [43, 44]. On the other hand, classification of obesity according to %FM showed that all subjects with COPD in our sample were obese, which might be misinterpreted as an indication that patients with COPD do not present cachexia. In fact, the FFMI value was indicative of depletion in 23 patients (32%) from the present sample (FFMI < 16 kg m−2 for men and FFMI < 15 kg m−2 for women) [45]. A study by Furutate el al. [46] showed that the prevalence of abdominal obesity in patients with COPD according to visceral fat area was 52.5% in contrast to 38.7% in a matched control group. In addition, they showed that patients with COPD retained visceral fat despite the absence of obesity (i.e., their visceral fat area was significantly greater regardless if they had the same BMI as the control group), and this finding was more evident in more advanced stages of COPD. Therefore, although BMI does not correctly classify obesity, specific cutoff points of %FM for the COPD population are needed since they present specific changes in body composition. Thus, both options (BMI and %FM) present clear limitations when used to reflect body composition in this population as well as their level of physical activity.

Limitations

One may argue that assessment of body composition should ideally be performed with DEXA and not with bioimpedance; use of bioimpedance can be considered a limitation of the present study. However, electrical bioimpedance has been widely and successfully used in this population and has provided useful and reliable information concerning body composition of patients with COPD, especially when a specific formula for these patients is used [23, 47, 48]. Furthermore, although the study had power enough to yield significant differences between the obese and underweight groups concerning the main outcomes, a prospective sample size calculation was not performed and a larger sample could have provided higher power to detect other potentially significant differences in PADL, such as between the obese and normal-weight groups (see Table 2). Moreover, the relatively small sample size of the present study for an investigation of such nature could lead to lack of power in certain secondary variables such as the 6MWT (see Table 2). A larger sample could have yielded more solid results, although this would not interfere directly in the main conclusions of the study.

Clinical Implications and Conclusions

The findings of this study highlight the need for specific interventions for patients with COPD who are classified as obese. Our data showed that according to the ACSM recommendations, patients with higher BMI or %FM present more marked inactivity in daily life, whereas patients with low BMI and %FM are more likely to achieve the recommendations and therefore are better able to maintain or improve their physical fitness. Hence, these results show that although the literature suggests that obesity might be a protecting factor in patients with COPD, special attention must be given to making obese patients a preferential target for interventions aimed at increasing their physical activity in daily life, since obesity in COPD is clearly linked to physical inactivity.

In conclusion, despite the high prevalence of physical inactivity in patients with COPD, those who are active in daily life have proportionally more fat-free mass and less fat mass than inactive patients. Classification of obesity according to body mass index or percentage of fat mass leads to completely different obesity prevalence rates in this population. More pronounced physical inactivity occurs in obese patients, although in general the correlations between body composition and PADL are weak. This suggests that body composition does not qualify as a determining factor of the objectively assessed level of PADL in patients with COPD.