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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 69  |  Issue : 1  |  Page : 56-63

Assessment of respiratory muscle functions before and after exercise training in stable chronic obstructive pulmonary disease patients


Department of Chest Diseases, Faculty of Medicine, Alexandria University, Alexandria, Egypt

Date of Submission29-Sep-2018
Date of Acceptance27-Jan-2019
Date of Web Publication31-Jan-2020

Correspondence Address:
MD Heba A Eshmawey
19 Sirhank Street, Louran, Alexandria, 21532
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejcdt.ejcdt_143_18

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  Abstract 


Background Respiratory muscle dysfunction and dynamic hyperinflation are considered important factors leading to exercise intolerance in chronic obstructive pulmonary disease (COPD) patients.
Aim We hypothesized that respiratory muscle functions would improve after an exercise training program in COPD patients.
Patients and methods The study included 24 stable COPD patients, their mean value of forced expiratory volume in the first second (%) was 44.5±15%. The training program was performed three times weekly for 4 weeks. Patients underwent ultrasonographic assessment of diaphragmatic excursion. Maximal inspiratory and expiratory pressures were detected by a handheld manometer. Exercise capacity was assessed using 6-min walking distance. Dyspnea was rated using modified Medical Research Council. Assessment of all parameters was done at baseline and after 4 weeks.
Results Maximal diaphragmatic excursion mean value demonstrated a significant increase (from 3.6±1.6 to 4.5±1.2 cm with P=0.006). PImax mean value illustrated a significant increase (from −40.2±13.8 to −43.8±12.1 cmH2O with P=0.010). PEmax mean value showed a statistically significant increase (from 93.9 to 105 cmH2O). There was a significant increase of exercise capacity presented by an increase of 6-min walking distance mean value (from 185.4±68.5 to 358.5±103 m with P<0.001.) Also, a significant improvement in modified Medical Research Council grade was detected (P<0.001).
Conclusion Exercise can result in significant improvements of respiratory muscle functions in stable COPD patients. This could be an important factor in the improvement of dyspnea and exercise capacity.

Keywords: chronic obstructive pulmonary disease, exercise training, respiratory muscle function


How to cite this article:
Eshmawey HA, Hassan M. Assessment of respiratory muscle functions before and after exercise training in stable chronic obstructive pulmonary disease patients. Egypt J Chest Dis Tuberc 2020;69:56-63

How to cite this URL:
Eshmawey HA, Hassan M. Assessment of respiratory muscle functions before and after exercise training in stable chronic obstructive pulmonary disease patients. Egypt J Chest Dis Tuberc [serial online] 2020 [cited 2022 May 18];69:56-63. Available from: http://www.ejcdt.eg.net/text.asp?2020/69/1/56/277293




  Introduction Top


Chronic obstructive pulmonary disease (COPD) is a progressive disease showing an airflow limitation which is characteristically incomplete and persistent [1].

The disease is manifested by chronic inflammation with submission to acute exacerbations. This is of clinical importance for individuals with COPD because this leads to oxidative stress imbalance and ‘spillover’ of inflammatory mediators into the circulation. Hence, the presence of systemic manifestations is a prominent feature in COPD patients [2].

Indeed, alteration of skeletal muscle structure, metabolism, and function is considered one of the most important systemic manifestations in COPD. This indicates respiratory muscle dysfunction, exercise intolerance, and altered health status in COPD patients [3],[4].

In pulmonary literature, the diaphragm is essential to inspiration acting in coordination with the other respiratory muscles. In COPD patients, it has been reported that hyperinflation-induced diaphragm shortening leads to decreased pressure generating capacity [5]. Furthermore, Rochester and Braun [6] studied the diaphragm length in both COPD patients and healthy controls with patients of the two groups having the same residual volume (RV). They concluded that the diaphragm length in the COPD group was reduced by 28% as compared with the healthy group. Regarding muscle fiber type, Levine et al. [7] have declared that the diaphragm of patients with severe COPD shows decreased proportion of type I fibers; in contrast, the proportion of type II fibers (the more fatigue-resistant fibers) is increased. Also, loss of myosin content in COPD diaphragmatic muscle is considered a prominent manifestation [8]. Therefore, there is accumulating evidence that dyspnea and exercise intolerance are most importantly caused by inspiratory muscle weakness in this population.

Accordingly, many studies have described the efficacy of inspiratory muscle training (IMT) whether alone or as adjuvant to general exercise in improving inspiratory muscle strength and endurance in COPD patients, thus, decreasing their grade of dyspnea [9].

There are only a limited number of studies describing the structure and movement of the diaphragm in patients with COPD. In this context, ultrasonographic assessment of diaphragmatic excursion is a considerable tool in patients with COPD [10].

In addition, the diaphragmatic length and surface area can be measured using other means such as spiral computed tomography, but this entails high risk of radiation hazards [11]. Furthermore, MRI is considered another expensive investigation [12]. Several other methods can be used to assess diaphragm in patients with COPD such as phrenic nerve conduction evaluation and measurement of transdiaphragmatic pressure [13],[14].

The aim of this study was to assess the respiratory muscle functions including diaphragmatic excursion and maximal inspiratory and expiratory pressures before and after the exercise training program in stable COPD patients.


  Patients and methods Top


Twenty-four stable COPD patients were enrolled in this study. Informed consent was obtained from all patients. The study was approved by the local ethics committee. Each studied patient had chronic airflow limitation (forced expiratory volume in the first second/forced vital capacity<70% of predicted) based on the spirometric study with a diagnosis of COPD according to the criteria of the Global Initiative for Chronic Obstructive Lung Disease [15]. They had no previous exacerbation in the last 4 weeks. Regular medications including inhaled long-acting B2 agonist and inhaled steroids were also maintained throughout the duration of the program. Exclusion criteria included other medical conditions that could interfere with exercise capacity; they included: other pulmonary diseases, unstable angina, recent myocardial infarction, severe arthritis, and severe osteoporosis.

Exercise training program

The exercise training program of this study was designed according to the American society guidelines [16]. The program extended for 4 weeks with frequency of three sessions of exercise per week. Each exercise session included: (a) Diaphragmatic breathing with pursed lips [17]. (b) Interval exercise using a treadmill [18]. Each patient had 2–3 min of exercise alternating with periods of rest. The exercise was of high intensity guided by the patient heart rate (60–80% of the patient maximal heart rate); exercise intensity was individualized; pulse and oxygen saturation were continuously monitored during exercise. The duration of each session was guided by the patient tolerance with a range of (20–30 min); oxygen saturation was not less than 92% during exercise, two (8.3%) patients were oxygen dependent even at rest, whereas the other patients needed no oxygen therapy during sessions. Exercise was stopped if dyspnea and/or leg fatigue could not be tolerated by the patient or when there was a change in vital signs. (c) Upper and lower limb strengthening exercise using a multigym device; the weight used for exercise was (60–80%) of the maximal weight that could be lifted; each patient had three sets of 10 repetitions with a period of rest in between sets [19],[20].

Methods

All the following parameters were assessed at baseline and after finishing the duration of exercise program:

Exercise capacity

Exercise capacity was assessed in the studied patients using 6-min walking distance (6MWD). The studied patients were instructed to walk through a course of 30 m long. The patients were not allowed to perform any vigorous exercise before the test for 2 h. Oxygen saturation was monitored during the test. Only two patients needed supplemental oxygen during exercise as they were oxygen dependent. The patient was asked to stop the test if one of the following occurred: (i) chest pain, (ii) intolerable dyspnea, (iii) leg cramps, (iv) staggering, (v) sweating, and (vi) pale face appearance [21].

Maximal inspiratory pressure

Patients had PImax measured using a mouthpiece and a dial pressure gauge. The measurement started from the functional RV [22]. The patients were instructed to seal their lips firmly around the mouthpiece to prevent any leakage and to maintain inspiratory pressure for at least 1.5 s [23].

Maximal expiratory pressure

Maximal expiratory pressure is measured starting from total lung capacity [24].

Dyspnea score was rated using modified Medical Research Council (mMRC) [25].

Diaphragmatic excursion

Ultrasonographic measurement of right diaphragmatic excursion was identified in sitting position. Low-frequency probe and M-mode were used during this procedure. Also, subcostal approach was used at both anterior axillary and midclavicular line. Two measurements of excursion were detected. First, tidal excursion which was measured at quiet breathing. Second, maximal excursion from total lung capacity to RV which was measured during deep breathing [26].

Statistical analysis

Data were fed to the computer and analyzed using IBM SPSS software package, version 20.0 (IBM Corp., Armonk, New York, USA). Quantitative data were expressed in median (range) and mean±SD. Normally distributed quantitative data were compared using paired t-test, abnormally quantitative distributed data were compared using Wilcoxon signed-rank test [27].


  Results Top


This study population consisted of 100% men. Regarding smoking status, 20 (83.3%) patients were exsmokers, whereas four (16.7%) patients were current smokers ([Table 1]). The studied patients included five (20.8%) patients of moderate, 15 (62.5%) patients of severe, and four (16.7%) patients of very severe COPD grade. Their mean value of forced expiratory volume in the first second (%) of predicted was 44.5% ([Table 1]). The patients were also classified guided by the combined assessment of Global Initiative for Chronic Obstructive Lung Disease classification plus mMRC dyspnea scale, COPD Assessment Test score and exacerbation history [28]. Accordingly, 20 patients belonged to group D, whereas four patients were of group B .Two (8.3%) patients were oxygen dependent even at rest. Regarding baseline data, decreased inspiratory muscle strength was observed in all the studied patients as mean PImax was −40.2 cmH2O as the reference range of PImax for a male adult is −92 to −121 cmH2O [29].
Table 1 Distribution of the studied cases according to the demographic data (n=24)

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After finishing the period of training, the 6MWD mean value showed an evidence of significant improvement (as it increased from 185.4 to 358.5 m); P was less than 0.001; mMRC significantly improved (P<0.001). Concerning respiratory muscle functions, maximal diaphragmatic excursion mean value illustrated significant increase from 3.6 to 4.5 cm as the P was equal to 0.006 ([Figure 1] and [Table 2]). But, tidal diaphragmatic excursion did not show a statistically significant increase (P=0.076). Also, the PImax mean value significantly increased from −40.2 to −43.8 cmH2O, P=0.010 ([Figure 2] and [Table 2]). In addition, the PEmax mean value showed a statistically significant increase (as increased from 93.9 to 105 cmH2O ([Figure 3] and [Table 2]).
Figure 1 Comparison between maximal diaphragmatic excursion at baseline and after 4 weeks of training (n=24).

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Table 2 Comparison of respiratory muscle parameters before and after exercise training program (n=24)

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Figure 2 Comparison between PImax at baseline and after 4 weeks of training (n=24). PImax, maximal inspiratory pressure.

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Figure 3 Comparison between PEmax at baseline and after 4 weeks of training (n=24). PEmax, maximal expiratory pressure.

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  Discussion Top


Thanks to the adopted exercise program in this study, improvement in maximal diaphragmatic excursion, PImax and PEmax could be obtained in patients with stable COPD. This study also illustrated an increase of exercise capacity and dyspnea grade in these patients. Meanwhile, exercise training is considered the cornerstone of any pulmonary rehabilitation program as it is charged with the task of improving muscle function. It has been proved that even severe and very severe COPD patients can benefit from exercise training [30].

There are several issues to consider when interpreting the results of this study. Most importantly, the cause of respiratory muscle weakness in COPD patients thus is the expected effect of exercise training on these muscles and its impact on relieving dyspnea.

There is accumulating evidence that pulmonary hyperinflation that occurs in COPD directly affects the length and subsequently the function of inspiratory muscles. Diaphragm and external intercostal muscles are submitted to displacement from optimal configuration for contraction. Evident change in chest wall geometry is present in these patients as the diaphragm muscle fibers become shorter, whereas the external intercostal muscles become lengthened. Thus, greater airway resistance and reduced supply of nutrients and oxygen occur [31].

Also, there are several issues to consider on explaining respiratory muscle dysfunction in COPD patients. These factors refer to oxidative stress, local activation of proteases in the respiratory muscles, malnutrition, aging, deconditioning, and systemic factors [32].

Some studies have investigated the structure and function of diaphragm in COPD patients; these studies revealed compensatory overuse hypertrophy [10].

In this line, dyspnea is the main symptom causing exercise limitation in COPD patients. Usually, this patient has to stop exercise before reaching his lactic threshold. This can be explained by the disability to expand tidal volume during exercise beyond minimal inspiratory reserve volume because of dynamic hyperinflation [33].

In this context, Casaburi and Porszasz [34] found that trained muscles elicit a reduction of lactic acid production with decreased ventilatory stimulation. Moreover, slowing of respiratory rate gives more time for exhalation decreasing the undesired dynamic hyperinflation. This indicates a potential for exercise training as a cornerstone modality to improve dyspnea and exercise capacity in COPD patients.

It has been reported that general exercise training can cause improvement of inspiratory muscle function and endurance. This can be explained by the increased number of oxidative fibers and oxidative enzyme activity in inspiratory muscles [35],[36]. General exercise training is considered a respiratory load serving a proper respiratory muscle training even without using any specific training for respiratory muscles when ventilation is increased by more than 12-fold [37].

It has been proved that improvement of lung hyperinflation provides a decrease of the elastic load on inspiratory muscles thus improving their performance. In addition, improvement of respiratory muscle functions after exercise training may be related to a significant increase of type II muscle fiber size and enhancement of velocity of inspiratory muscle shortening [38].

In this context, a recent study investigated the effect of daily program of respiratory muscle strength and endurance exercise. They declared a significant improvement of PImax and a significant decrease of the ratio of breathing frequency to minute ventilation (bf/VE). The latter indicates breathing pattern improvement. Also, the previous results were associated with a significant decrease of dyspnea grade [39].

In fact, general exercise should reach a certain intensity to provide loading of respiratory muscles. Usually, attaining this level of intensity is not easy for most COPD patients especially those of severe grade .Thus, interval exercise is considered a proper means to let patients have less limiting symptoms during exercise particularly dyspnea and leg fatigue; therefore, the patients can attain longer periods of exercise as interval exercise elicits decreased level of metabolic and ventilatory response in comparison to continuous training [40]. In this line, interval exercise was adopted in this study.

In line with our results, Chun et al. [12] studied the effect of a 3-month pulmonary rehabilitation program on diaphragmatic movement in 37 COPD patients. They concluded that there was a significant improvement of diaphragmatic movement in these patients using fluoroscopy.

Furthermore, Mills et al. [38] proved that IMT for 8 weeks increased maximal inspiratory pressure (+34±43%, P=0.008), diaphragm thickness at RV using M-mode of ultrasound (38±39%, P=0.03), and peak inspiratory flow (35±42%, P=0.049). Thirty-four healthy adults (68±3 years) with normal spirometry were enrolled in this study and were divided equally into a pressure-threshold IMT or sham-hypoxic placebo group [41].

In addition, Geddes et al. [42] indicated that IMT showed significant improvement of PImax, inspiratory muscle endurance, and exercise capacity.

As the diaphragmatic breathing was a considerable part of our exercise program, it is valuable to focus on its role in improving diaphragmatic dysfunction and thus, dyspnea in COPD patients.

In contrast, in several studies, it is difficult to investigate the specific effect of breathing exercises as they are usually considered as adjuvant modalities to general exercise in most exercise programs for COPD patients [43]. But, it was documented that diaphragmatic breathing can improve gas exchange [44], oxygen cost of breathing [45], and respiratory pattern [46]. Expectedly, a recent study has reported an increase of abdominal movement as a result of a complete training program of diaphragmatic breathing in COPD patients [43]. In contrast, Gosselink et al. [47] demonstrated no change in breathing pattern in similar patients. This variation can be explained by different training periods in both studies.

Expiratory muscle weakness is considered one of the manifestations of generalized muscle weakness in COPD patients [48]. In this context, some important features are detected in these muscles such as decreased lactate threshold [49] and reduced oxidative capacity of muscle fibers [50].

In line with our results, Cortopassi et al. [51] proved that a comprehensive exercise program which included a global warm-up, upper and lower limb endurance exercise as well as stretching and relaxation lead to a statistically significant increase of PImax 64.7±22.9 versus 75.5±23.7 cmH2O (P=0.001) and PEmax 110.8±28.1 versus 120.4±28.1 cmH2O (P=0.004).

This study illustrated the value of ultrasonographic assessment of diaphragmatic excursion as an applicable method to assess the effect of any intervention such as pulmonary rehabilitation on respiratory muscle function.

There is a proved evidence that ultrasound has been used since the 1960s to examine diaphragm structure and function [10]. To date, there is a clinical importance of ultrasonography as a useful tool for the evaluation of diaphragm because of being of no risk of radiation [52].

From the clinical point of view, ultrasonographic imaging has some limitations as it is examiner dependent; in addition, the accuracy of this method may be affected by the patient condition [12]. In this line, ultrasonographic assessment of diaphragmatic excursion cannot provide full visualization of diaphragmatic hemicopula [53].

Finally, exercise training is considered very effective in improving respiratory muscle functions in COPD patients. Also, diaphragmatic excursion assessment is considered a valuable tool to detect the effect of pulmonary rehabilitation program and various medications.

Also, the previously mentioned data relates to future consideration of ultrasonographic assessment of diaphragm as a proper method to predict COPD exacerbation early and to evaluate the efficacy of using noninvasive ventilation [54].

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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