Peripheral muscle dysfunction is a prevalent condition in patients with chronic obstructive pulmonary disease (COPD). Common features include reduced muscle strength and endurance, muscle atrophy and poor oxidative capacity.1 This muscle dysfunction is directly related to exercise intolerance, impaired health-related quality of life2 and involves increased use of health care resources.3

In addition to peripheral muscle dysfunction subjects with COPD may present impairment in mucociliary clearance, an essential mechanism of pulmonary defense. Mucociliary clearance removes inhaled particles and microorganisms from the respiratory tract.4,5 Dysfunction of this mechanism causes hypersecretion leading to lung infections and exacerbations.4,5

The efficiency of mucociliary clearance can be analyzed by the velocity of nasal mucociliary transport (MCT) and is well correlated with tracheobronchial transport6,7 which requires more invasive procedures to assess. MCT is measured using substances with a characteristic flavor, for example, the saccharin transit time (STT).6–9 STT test has been widely reported in previous studies as being simple, valid and reliable with similar results to those obtained with the use of radioisotope particles for MCT analysis.6,10

Pulmonary rehabilitation (PR) in subjects with COPD is supported by the highest-level of evidence.11 Resistance training (RT) is an important component in improving muscle strength, activities of daily living and functional exercise capacity and reducing fatigue and dyspnea symptoms.1,12,13

RT protocols routinely include weight machines and free weights in standard proposals, however elastic tubing (ET) was recently investigated as an alternative to the conventional RT for subjects with COPD. Studies with elastic devices have demonstrated similar benefits to conventional training14–17 with the added advantage of being portable, and inexpensive.14,17 The linear increase of resistance occurring in ET is less harmful to the joints, and provides a greater recruitment of motor units when compared to the conventional resistance training.18 This is particularly interesting for patients with muscle dysfunction like COPD.

There is evidence that aerobic exercise improves the mucociliary system by altering the viscosity of nasal mucus, thus can be recommended as an adjunctive treatment to respiratory physiotherapy techniques.4,19,20 This type of exercise increases the levels of adrenergic mediators that contribute to changes in mucociliary clearance during or after exercise.21 Although the effects of RT on mucociliary system have not yet been reported, it is reasonable to hypothesize that it has a positive influence on mucociliary clearance as RT modulates changes in the autonomic control in subjects with COPD.22

Knowing the effects of RT on MCT in subjects with COPD is essential for health professionals involved in pulmonary rehabilitation for COPD. MCT is the first line of defense of the respiratory system against aggressor agents and irritants. The maintenance of its integrity, therefore, is necessary to reduce the risk of respiratory infections and hospitalizations in COPD.4,19 Furthermore, such knowledge could lead to strategies to improve mucociliary clearance in subjects with COPD. Therefore, the aim of this study was to evaluate the effects of two RT programs on mucociliary clearance in subjects with COPD.

A statistical package (SPSS v.22, SPSS Inc., USA) was used for data analysis. Normal distribution of the data was evaluated using the Shapiro–Wilk test. The results are presented as mean values±standard deviations or as median [interquartile range 25–75%] according to the data distribution. ANOVA for repeated measures model in two-factor scheme was performed for each group to compare training effects. Data used for the repeated measurements was checked for violation of sphericity using the Mauchly test. The Greenhouse–Geisser correction was used when the sphericity was violated. Between groups comparisons for both baseline and training changes (Δ=baseline−12 weeks) were performed using the Student t test for independent samples (or Mann–Whitney test for nonparametric data). Categorical variables (training frequency) were analyzed using the chi-square test. The significance level was set at p<0.05.

A complete overview of the study can be seen in Fig. 1. Twenty-eight subjects with COPD were included and allocated to one of the two groups. Nine subjects quit the study after randomization (three withdrew consent and six dropped out during the training). Eventually 19 subjects completed the study and were included in the analysis (convenience sample). All subjects completed more than 75% of training frequency, with no differences between groups (p>0.05).

Figure 1.

Consort flow diagram. GET: training with elastic tubing and GCT: training with weight training equipment.

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Table 1 presents the sample characterization. No significant differences were found between the groups in any of the investigated outcomes at baseline. Lung function remained unchanged after interventions in both groups (Table 2) and the analysis of hemodynamic parameters showed a similar magnitude of changes between the two training groups (Table 3).

In relation to the MCT analysis, no differences were observed between the baseline evaluations of the training groups (p>0.05). There was a significant reduction in the SST values after 12 weeks in GET and GCT (p=0.03) (Fig. 2), but no interaction between type of training and SST decrease (p=0.97) and no differences between groups were observed on the magnitude of SST changes after interventions (p=0.97).

Figure 2.

Comparison of the mucociliary transportability values before and after resistance training of 12 weeks. Data expressed as mean and standard deviation. STT: saccharin transit time; GET: training with elastic tubings; GCT: training with weight training equipment; *: significant difference between initial and final evaluation (p=0.03).

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The results of this study indicate significant improvements in MCT after RT in subjects with COPD in both conventional method (weight training), and the elastic tubing method. This is the first study up until now to analyze the effects of RT on the mucociliary system of subjects with COPD.

It has been shown that physical exercise is essential for improving airway clearance of subjects with COPD. It is particularly important as the dysfunction of this mechanism causes hypersecretion leading to lung infections and exacerbations and hospitalization.4,5,8

Few studies in the literature investigated the chronic effects of exercise on MCT. Leite et al. were the only ones to investigate the chronic effect of exercise on MCT in patients with COPD.27 They observed that MCT did not change after 12 weeks of aerobic training. Similarly, Salh et al. performed 8 weeks of aerobic training in patients with cystic fibrosis and concluded that aerobic training had no effect on mucociliary clearance, using an indirect measurement of MCT (i.e. amount of mucus expectoration).19

Essentially exercise induces an increase in the autonomic nervous system activity, release of adrenergic mediators, increases ventilation and respiratory rate, which causes an increase in the velocity of MCT. These phenomena occur consistently in different populations (i.e. athletes aged between 18 and 37 years,28 smokers and nonsmokers with an average age of 40 years29). Furthermore, two cross-sectional studies,30,31 have pointed out that for individuals with normal lung function, MCT is more efficient in physically active individuals than in those insufficiently active. The chronic effects of regular exercise, however, remain unclear.

It is believed that the improvement in MCT observed in the present study may be related to the behavior of the autonomic nervous system after a period of RT. There is evidence that the autonomic function is impaired in COPD and that exercise has positive effects on it.32,33 RT induces an overall improvement in the parasympathetic and sympathetic components of the autonomic nervous system.34,35 Underlying mechanisms of autonomic improvement in these subjects after RT are yet to be clarified. Factors such as the reduction in circulating norepinephrine may be attributed to this improvement.

Additionally, it is important to mention that there were similar improvements in the peripheral muscle strength between the groups (data not shown). Due to the important relation between muscle strength and autonomic function in subjects with COPD,36 it could be hypothesized that improvements in muscle function are partly responsible for the improvements in the autonomic nervous system. Since the mucociliary system is regulated by the autonomic nervous system,37 it is believed that the possible improvement in autonomic modulation could influence improved MCT values.

Another hypothesis for the improvements in MCT is related to low-grade chronic inflammation. Most of the subjects included in the study were ex-smokers. It is known that the toxic substances released by the cigarette promote local inflammation in the respiratory tract,38,39 causing damage that can affect mucociliary function.40 When smokers give up there can be reversibility of mucociliary function after 15 days of abstinence from smoking.41 However, when COPD is present, the chronic low-grade inflammation could impair this reparative process. As RT is able to decrease the proinflammatory profile of subjects with COPD,16 we speculate that the anti-inflammatory “millie” generated by chronic exercise training may help in some way to repair the mucociliary function of these subjects. Future studies are warranted in this area to clarify the possible associations between the outcomes of chronic exercise and MCT in COPD.

The reduced sample size and absence of a control group may be considered limitations of the study. With the limited sample, it was not possible to verify differences in subgroups of subjects according to COPD severity. Further studies investigating this specific issue are warranted. Another limitation would be that we did not include the effects of RT on outcomes such as cough and sputum, since both are related to MTC.4,5 However, it is important to note that the data presented in this study are secondary analyzes of a larger project which presents other variables demonstrating the effects of training with elastic tubing.

In conclusion, the present study demonstrated that both RT with elastic tubing and conventional training promoted similar gains in the mucociliary transportability of subjects with COPD. Future research needs to approach the chronic effects of exercise on mucociliary clearance in subjects with COPD, in order to clarify the physiological mechanisms that influence this process.

This study was supported by the National Council of Scientific Researches (CNPq) [Grant number: 470742/2014-3]. BSAS is funded by CAPES/Brazil.

The authors declare that they have no conflict of interest.