Neural Respiratory Drive During Different Dyspnea Relief Positions and Breathing Exercises in Individuals With COPD

Abstract

BACKGROUND:

When the work load of the respiratory muscles increases and/or their capacity decreases in individuals with COPD, respiratory muscle activation increases to maintain gas exchange and respiratory mechanics, and perception of dyspnea occurs. The present study aimed to compare diaphragm and accessory respiratory muscle activation during normal breathing, pursed-lip breathing, and breathing control in different dyspnea relief positions, supine and side lying.

METHODS:

A cross-sectional study design was used. Sixteen individuals with COPD age between 40–75 y were included. Pulmonary function was evaluated by spirometry, muscle activation by surface electromyography, and dyspnea by the modified Borg scale. Muscle activation was measured in the diaphragm, scalene, sternocleidomastoid, and parasternal muscles. The evaluation was made in the dyspnea relief positions (sitting leaning forward, sitting leaning forward at a table, leaning forward with back against a wall, standing leaning forward, and high lying), seated erect, supine, and side lying.

RESULTS:

There were significant differences between the 8 positions (P < .001). There was no significant difference in muscle activation between sitting leaning forward and sitting leaning forward at a table position with analyzing post hoc test results (P > .99 for each muscle). However, muscle activation was lower in these 2 positions than in the other positions (P < .001 for each muscle). Muscle activation was greater in the supine position than in the other positions (P < .001 for each muscle). No difference was observed in muscle activation between the seated erect, leaning forward with back against a wall, standing leaning forward, high-lying, or side-lying positions (P > .05 for each muscle with a minimum P value of .09).

CONCLUSIONS:

The use of sitting leaning forward and sitting leaning forward at a table positions together with breathing control may help people with COPD to achieve more effective dyspnea relief and greater energy efficiency.

Introduction

COPD is a common, preventable, and treatable disease characterized by persistent air-flow limitation and respiratory symptoms. Chronic inflammation in COPD leads to structural changes, narrowing of the small airways, and destruction of the lung parenchyma. Accordingly, alveolar connections and elastic recoil decrease. ¹ Expiratory flow limitation, changes in diaphragm muscle fibers, reduction of the apposition zone, and deterioration in chest wall mechanics lead to air trapping and hyperinflation in the lungs. ² Mechanical abnormalities such as increased air-flow obstruction and static and dynamic hyperinflation in COPD increase the work load on the respiratory system. ³ When the work load of the respiratory muscles increases, the capacity of the respiratory muscles decreases; or when both are present together, respiratory effort and, thus, the feeling of dyspnea increase. Due to the imbalance between work load and capacity, the neural respiratory drive of the respiratory muscles increases to maintain gas exchange and respiratory mechanics. ^{4 - 6}

It is possible to measure the neural respiratory drive indirectly by electromyography (EMG) using respiratory muscle activation, which reflects electrical changes in the stimulus elicited by action potentials that propagate across muscle fiber membranes. ^{7 , 8} Dyspnea relief positions and breathing techniques are therapeutic methods used to relieve dyspnea and improve breathing. ^9-11 Although it has been reported that dyspnea relief positions are effective in increasing the mechanical efficiency of the respiratory muscles, it is not known which positions are effective for dyspnea in terms of respiratory muscle activation in people with COPD. ¹² Furthermore, although neural respiratory drive is known to be associated with dyspnea, no studies in the literature have compared the effects of different breathing techniques on respiratory muscle activation in different dyspnea relief positions. ⁶ The aim of the present study was to compare diaphragm and accessory respiratory muscle activation as a measure of neural respiratory drive during normal breathing, pursed-lip breathing, and breathing control in different dyspnea relief positions, seated erect, supine, and side lying.

QUICK LOOK.

Current knowledge

When the work load of the respiratory muscles increases and/or their capacity decreases in individuals with COPD, respiratory muscle activation increases to maintain gas exchange and respiratory mechanics, and the perception of dyspnea occurs. Dyspnea relief positions and breathing techniques are therapeutic methods employed to relieve dyspnea and improve breathing.

What this paper contributes to our knowledge

It was found that the neural respiratory drive decreased during breathing control and in sitting leaning forward and sitting leaning forward at a table position in individuals with COPD. Dyspnea was found to be associated with the neural respiratory drive. The use of sitting leaning forward and sitting leaning forward at a table position together with breathing control can help individuals with COPD to get more effective results from dyspnea relief treatment and use energy more efficiently.

Methods

An experimental study design was used. Sixteen individuals with COPD, followed up at the Department of Chest Diseases, Faculty of Medicine, Bolu Abant İzzet Baysal University, were evaluated. Individuals who were previously diagnosed with COPD according to the diagnostic criteria by chest disease specialists were evaluated. Their sociodemographic and physical characteristics were recorded using a medical history form. Individuals diagnosed with COPD and age between 40–75 y were included in the study, whereas those who additionally had pulmonary, cardiac, or neurological system involvement and individuals who had undergone major pulmonary and extrapulmonary surgery or had exacerbation of COPD in the last 3 months were excluded. The study was initiated after approval from the Bolu Abant Izzet Baysal University Clinical Research Ethics Committee (approval date: June 25, 2021; approval number: 236). Written informed consent was obtained from the participants before the study (clinical trial number: NCT04983472).

Pulmonary parameters were evaluated by spirometry according to American Thoracic Society/European Respiratory Society criteria (microQuark PC-based Spirometer, Cosmed, Rome, Italy). Evaluations were made with at least 3 attempts, and the best of 95% consistent maneuvers was used. The parameters evaluated were expressed as the percentage of the expected values according to the individuals’ age, height, body weight, and sex. FVC, FEV₁, peak expiratory flow, and flow value of 25–75% of the forced expiratory volume were measured and expressed as the percentages of the predicted values. ^{13 , 14} The modified Borg scale and the modified Medical Research Council (mMRC) dyspnea scale were used to determine the perception of dyspnea. The Borg scale assessed dyspnea during activities of daily living, such as walking and climbing stairs, and at rest. The Borg scale is a subjective scale that scores 0–10 for breathlessness at rest and during daily activities such as walking and climbing stairs. The lowest level of 0 means not at all and a level of 10 means very severe shortness of breath. The perception of dyspnea during activities of daily living was evaluated using the mMRC dyspnea scale. Individuals with COPD were asked to choose the statement that best described the severity of dyspnea among 5 statements scored between 0–4. In the mMRC dyspnea scale, breathlessness level 0 is scored as “no breathlessness except on strenuous exercise,” and level 4 is scored as “too breathless to leave the house, or breathless when dressing or undressing.” ^{15 , 16} Dyspnea was evaluated before starting EMG measurements. The assessments were completed in the sitting position.

Activation of the diaphragm, scalene muscles, sternocleidomastoid (SCM), and parasternal muscles of the participants was evaluated using surface EMG (Trigno wireless system, Delsys, Natick, Massachusetts). The software EMGworks Analysis 4.7.3.0 (Delsys) was used to analyze the signals. The transmission band of the amplifiers for each channel was 20–450 Hz. The rate of recovery from common noise was > 80 dB, and the signal sampling rate was 2,000 Hz. Movement and electrocardiogram artifacts are associated with very low frequencies and can be removed by filtering at 20 Hz. The signals were passed through a motion artifact filter with a 20–1,000 Hz bandpass filter (Butterworth, fourth order). The root mean square values of the filtered signals were calculated in μV at 0.1-s intervals ^17-20 (Fig. 1). EMG signals from inspiratory loop segments between QRS complexes were analyzed manually. The inspiratory activity was quantified both as peak activity and as rate of rise (slope). EMG measurements were started when the onset of inspiration was observed, and EMG measurement was stopped when the 2-min period expired. EMG signals were averaged for this 2-min period. ^{21 - 23} The maximum isometric contraction (MIC) % (MIC%) value was used for normalization. The time interval at the maximal inspiratory maneuver was evaluated for MIC. The maximal inspiratory maneuver was measured from functional residual capacity to total lung capacity in the seated erect position as a fast and strong maximum inspiration, and the highest measurement value was used. The MIC maneuver was performed at least 5 times until a variance of < 10% was acquired with 3 repeatable efforts. ^{4 , 24 - 26}

Fig. 1.

Filtered electromyography, root mean square (A: diaphragm, B: sternocleidomastoid, C: scalene muscle, and D: parasternal muscle).

Respiratory muscle activation was evaluated in dyspnea relief positions (sitting leaning forward at a table, sitting leaning forward, leaning forward with back against a wall, standing leaning forward, high-lying), seated erect, supine, and side lying (see related supplementary materials at http://www.rcjournal.com). Normal breathing, pursed-lip breathing, and breathing control techniques were employed in the evaluation. For normal breathing, participants were asked to breathe normally. In pursed-lip breathing, they were asked to inhale and exhale through pursed lips without using their abdominal muscles. For breathing control, they were asked to breathe quietly (with the command as if asleep). Each breathing technique was repeated for 2 min for the breathing frequency to be determined for each individual before the tests. There were at least 5-min intervals between breathing techniques and between positions. ^{9-11 , 27 , 28} The same evaluator performed measurements in different orders, and the individuals were allowed at least 15 min of rest before evaluation. All breathing techniques were taught to the individual prior to the start of the tests, and an application trial was performed. After the rest period, the individual was positioned, and measurements were taken.

Figure 2 shows the placement of the electrodes. Muscle surface EMG recordings were made with right unilateral electrodes. For the diaphragm, the electrodes were placed at the intersections of the anterior axillary line with the sixth-eighth intercostal spaces. The reference ground electrodes were placed below and away from the recording electrodes. ⁷ For the parasternal muscle, the electrodes were placed unilaterally on the right, 3 cm from the sternum, in the second intercostal space. The reference ground electrode was placed at sternal angle. ²⁹ For the SCM, the electrodes were placed in the upper one-third and lower one-third of the SCM. The reference ground electrode was placed in the sternal fossa. ²⁹ For the scalene muscle, the electrodes were placed in the right posterior triangle of the neck at the level of the cricoid cartilage. ³⁰

Fig. 2.

Electrode placement. SCM = sternocleidomastoid.

Data analysis was performed using SPSS v.26 (IBM, Armonk, New York) and R 4.5 (R Foundation for Statistical Computing, Vienna, Austria). Descriptive statistics were presented as mean and SD or median and mode for numerical variables and as number and percentage for categorical variables. The Shapiro-Wilk test and residual analysis were used to determine whether the data were normally distributed. The sphericity assumption was tested. If the assumptions were met, the repeated-measures analysis of variance test was used. The level of correlation between dyspnea severity and MIC% was examined using Pearson or Spearman correlation test. The significance level was set at P ≤ .05.

Results

The study included 16 male subjects with COPD (61 ± 7 y). Table 1 shows the individuals’ clinical and demographic information. Table 2 shows a comparison of the results of MIC% values in different muscles and different positions. The results obtained were the same for all muscles. There was a significant difference in MIC% values between positions (P < .001 for all muscles). The lowest MIC% values were acquired in sitting leaning forward and sitting leaning forward at a table position. No significant difference was found between these 2 positions (P > .99 for each muscle). However, there was a significant difference between them and the other positions (P < .001 for all comparisons within each muscle). The supine position resulted in the highest MIC% values, which were significantly different from all other positions (P < .001 for all comparisons within each muscle). No significant difference was found between the seated erect, leaning forward with back against a wall, standing leaning forward, high-lying, or side-lying positions (P > .05 for all comparisons with a minimum P value of .09).

Table 1.

Clinical and Demographic Characteristics of Individuals With COPD

Table 2.

The Maximum Isometric Contraction Percentage Comparison for Muscles With Normal Breathing in Different Positions

Figure 3 shows a comparison of the results for breathing types in different muscles and positions. A significant difference was found in breathing types in all muscles in the seated erect (P < .001 for the diaphragm, P = .002 for the scalene muscle, P < .001 for the parasternal muscle, and P < .001 for the SCM), sitting leaning forward (P = .007 for the diaphragm, P = .02 for the scalene muscle, P = .001 for the parasternal muscle, and P = .039 for the SCM), and supine (P = .002 for the diaphragm, P = .039 for the scalene muscle, P = .042 for the parasternal muscle, and P < .001 for the SCM) positions. The group that caused the difference was the breathing control group, which had the lowest values. There was no significant difference in the MIC% values in the scalene muscle and SCM in the standing leaning forward position according to breathing type (P = .09 and P = .09, respectively). Whereas breathing control in the diaphragm differed significantly, a difference was revealed between pursed-lip breathing and breathing control in the parasternal muscle (P < .001 and P = .007, respectively). There was no difference according to breathing type in the scalene muscle in the sitting leaning forward at a table position (P = .17). The difference in other muscles emerged in breathing control. No difference was detected in terms of breathing type in the diaphragm and parasternal muscle in the leaning forward with back against a wall position (P = .07 and P = .07, respectively). Whereas a difference was observed between normal and breathing control in the scalene muscle, there was a difference during breathing control in the SCM. There was no difference between breathing types in the diaphragm in the side-lying position (P = .30). Whereas there was a difference between normal and pursed-lip breathing in the parasternal muscle, breathing control in the scalene muscle and SCM caused a difference. There was no difference between breathing types in the parasternal muscle and the SCM in the high-lying position (P = .10 and P = .08, respectively). Whereas the breathing control group caused the difference in the diaphragm, the difference in the scalene muscle was between normal breathing and breathing control.

Fig. 3.

Respiratory muscle activation in different breathing types. SCM = sternocleidomastoid.

Table 3 shows the level of correlation between seated erect, normal breathing MIC% in different muscles and the severity of rest, activity, and mMRC dyspnea. There was a highly significant correlation between MIC% in the diaphragm and all severities of dyspnea (r = 0.83, P < .001 for rest; r = 0.76, P = .001 for activity; and r = 0.88, P < .001 for mMRC). A moderately significant correlation was detected between MIC% in the scalene muscle and the severity of dyspnea (r = 0.51, P = .042 for rest; and r = 0.58, P = .02 for activity). The level of correlation with the severity of mMRC dyspnea was low and insignificant only in the scalene muscle (r = 0.43, P = .10). In the parasternal muscle, there was a moderately significant correlation between MIC% and the severity of dyspnea (r = 0.58, P = .02 for rest; r = 0.56, P = .03 for activity; and r = 0.64, P = .008 for mMRC). There was also a moderately significant correlation between MIC% and dyspnea in the SCM (r = 0.55, P = .03 for rest; r = 0.70, P = .003 for activity; and r = 0.52, P = .040 for mMRC).

Table 3.

Examination of the Correlation Between the Maximum Isometric Contraction Percentage in the Seated Erect and the Severity of Rest Dyspnea, the Severity of Activity Dyspnea, and Modified Medical Research Council Dyspnea Scale

Discussion

In the present study, respiratory muscle activation was lower in the sitting leaning forward and sitting leaning forward at a table position compared to the other dyspnea relief positions, seated erect, supine, and side lying. Respiratory muscle activation was greater in the supine position than in the other positions. Muscle activation during breathing control applied in different positions was lower than during normal breathing and pursed-lip breathing. Furthermore, respiratory muscle activation was associated with dyspnea.

Obstructive airways disease increases the end-expiratory lung volume in individuals with COPD. The diaphragm flattens and descends as a result of hyperinflation. Changes in diaphragm position reduce the pressure-generating capacity of the diaphragm. ^{1 , 31} Mechanical loading in individuals with COPD causes increased diaphragm muscle activation. This increase in the neural respiratory drive shows a progressive decrease in the mechanical efficiency of the diaphragm. ³² In individuals with COPD, accessory respiratory muscles become more activated against the increased respiratory load and play a supporting role for the diaphragm. ¹² Abnormal increases in neural respiratory drive occur when there is airway obstruction or increased respiratory demand. ²⁵

Increased dyspnea is associated with an increase in neural respiratory drive due to increased mechanical load on the inspiratory muscles, increased chemical drive, or a combination of both. A study of people with COPD, interstitial lung disease, and healthy volunteers showed that the intensity of dyspnea during exercise increased with increased respiratory effort, tidal volume/inspiratory capacity, and respiratory muscle activation. Mechanically, the intensity of dyspnea increased as tidal volume was restricted and inspiratory neural drive increased. Higher levels of dyspnea intensity in individuals with COPD and interstitial lung disease than in healthy controls reflect the increased inspiratory neural drive in the diaphragm due to the combined effects of increased ventilatory demand and intrinsic mechanical load. ⁶ In our study, respiratory muscle activation was associated with the perception of dyspnea. This finding confirms the relationship between respiratory neural drive and dyspnea, which occurs as a result of an imbalance between respiratory work and capacity in people with COPD.

Treatments that increase the strength of the inspiratory muscles (inspiratory muscle training) or reduce their mechanical load (eg, bronchodilators) reduce neural respiratory drive and the perception of dyspnea in people with COPD. ²⁰ Position changes in individuals with COPD also affect the mechanical efficiency of the respiratory muscles. Forward-leaning positions improve diaphragm function, the length-tension relationship, and thoracoabdominal movement and reduce dyspnea. ¹⁰ The forward-leaning position alters accessory respiratory muscle recruitment and decreases dyspnea by providing stronger abdominal contraction and increasing diaphragm support. ³³ Kim et al ³⁴ examined the activation of inspiratory accessory muscles (scalene, SCM, and pectoralis major) in individuals with COPD in arm-supported forward-bending, arm- and head-supported forward-bending, and neutral positions. They found that accessory respiratory muscle activation was greater in the supported positions compared to the neutral position. It has been suggested that this may be due to the advantage of overcoming the limitation of caudal descent of the diaphragm during inspiration with the increase in intra-abdominal pressure during forward bending and the stabilizing effect of the forearm. ³⁴ In their study on individuals with stage 2 and more severe COPD, Morrow et al ²⁸ asked subjects to stand in a comfortable position and in an upright supported sitting position for 2 min, perform diaphragmatic breathing, and rest for 5 min in the starting position, in that order. It was found that the starting position and the upright supported sitting positions had no effect on respiratory muscle activation. In addition, intercostal muscle activation did not change during diaphragmatic breathing, whereas diaphragm muscle activation increased. ²⁹ Another study found no difference in parasternal muscle activation or derived muscle activation indices between the sitting, 45° reclined, and supine positions. These findings suggest that the negative effects on lung volume and airway resistance of moving from the sitting to the supine position are offset by improvements in diaphragm function by adopting a more optimal position on the length-tension curve. ³⁵

In the supine position, the total load on the respiratory system increases, which is balanced by a reduced effect of the rib cage on respiration, resulting in unchanged parasternal muscle activity. ³⁵ In a study of people with advanced COPD, the imbalance between the inspiratory neural drive and the mechanical and ventilatory responses of the respiratory system, which was significantly increased compared to the control group, was further increased in the supine position. The sudden increase in acute elastic mechanical load revealed compensatory increases in inspiratory neural drive as the load/capacity imbalance of the inspiratory muscles increased. In addition, altered afferent inputs from sensory receptors abundant throughout the respiratory system in response to sudden increases in elastic load also influenced the intensity of dyspnea perception. Increased respiratory discomfort during the transition from sitting to supine and parallel increases in measures of inspiratory neural drive, impaired neuromechanical coupling, and neuroventilatory mismatch support this relationship. ¹⁸ Our study supports the notion that increased neural respiratory drive in the supine position may be related to the increased mechanical load reported in previous research. In our study, the neural respiratory drive was lower in sitting leaning forward and sitting leaning forward at a table position. We believe that this is due to a reduction in respiratory effort and dyspnea perception as the mechanical disadvantage of the diaphragm is reduced by leaning forward.

Dyspnea relief positions reduce the mechanical load on the diaphragm and result in decreased neural respiratory drive. The standing leaning forward position may not have improved the mechanical efficiency of the diaphragm as it did not provide enough trunk flexion as the sitting leaning forward and sitting leaning forward at a table. Our study is the first to compare all known dyspnea relief positions according to neural respiratory drive. These relief positions are effective for dyspnea because they improve the mechanical efficiency of the respiratory muscles. ¹² However, we believe that some of these positions are effective in reducing dyspnea by improving the mechanical efficiency of the respiratory muscles.

Our results suggest that compared to all other positions tested perceived dyspnea in patients with COPD is relieved in the sitting leaning forward and sitting leaning forward at a table position due to a reduction in neural respiratory drive. In addition to positioning, breathing techniques are also frequently used to reduce the perception of dyspnea in individuals with COPD. Breslin ³⁸ compared 2-min tidal breathing and pursed-lip breathing in an upright position at rest in individuals with COPD. The results showed an increase in accessory respiratory muscle activation and thoracic cage movement in pursed-lip breathing. Moreover, pursed-lip breathing provided an advantage against diaphragm fatigue by reducing diaphragm activation against the increased respiratory load. ³⁶ In another study in which pursed-lip breathing and normal breathing were compared in the arm-supported forward bending, arm- and head-supported forward bending, and neutral positions, the scalene muscle and SCM activation were higher with pursed-lip breathing. ³⁴ In a study that included individuals with mild COPD, while diaphragm muscle activation was higher in diaphragmatic breathing there was no significant change in SCM, scalene, and external intercostal muscle activation. In the feedback breathing exercise, whereas the SCM and scalene muscle activation decreased, the diaphragm muscle activation increased. The feedback breathing exercise reduced the SCM and scalene muscle activation more than diaphragmatic breathing did. As with the feedback breathing exercise, deep and slow inhalation reduces SCM activity and is effective in preventing the overuse of respiratory muscle synergists. ³⁷ In another study performed with 17 healthy individuals, higher SCM activity was observed in flow-oriented incentive spirometry (Triflow) compared to volume-oriented incentive spirometry (Voldyne) and diaphragmatic breathing; however, no significant difference was detected between diaphragmatic breathing and volume-oriented incentive spirometry.

Considering the respiratory pattern variables, SCM activity, and the physiology of techniques based on deep and slow inspiration, flow-oriented incentive spirometry showed disadvantages in comparison with other techniques. ³⁸ Costa et al ³⁹ assessed SCM activation during deep inspiration in healthy young adults. In individuals with rapid inspiration and costal breathing, higher SCM muscle activation was observed compared to slow inspiration, mixed, and diaphragmatic breathing. ³⁹ In our study, the neural respiratory drive during breathing control was lower. Breathing control and pursed-lip breathing are frequently used to reduce dyspnea. ¹⁰ To the best of our knowledge, the present study is the first to compare breathing control and pursed-lip breathing with normal breathing in terms of neural respiratory drive. Based on our results, we think that breathing control may be more effective in reducing the perception of dyspnea in individuals with COPD since breathing control decreases the neural respiratory drive more than pursed-lip breathing does. Limitations of the study: dyspnea severity in different postures and breathing conditions was not assessed, and dyspnea was not induced by allowing subjects to perform an activity before adopting one of the different positions. Second, differences in breathing patterns (tidal volume and breathing frequency) and minute ventilation that would affect respiratory muscle activation were not evaluated. Finally, the small number of participants was another limitation.

Conclusions

In the present study, it was found that the neural respiratory drive decreased during breathing control and in sitting leaning forward and sitting leaning forward at a table position in individuals with COPD. Furthermore, dyspnea was associated with the neural respiratory drive. Respiratory muscle activation in COPD may be a useful physiological marker of dyspnea. The management of dyspnea is difficult and requires effective management, combined interventions, and a patient-tailored multidisciplinary approach. To reduce dyspnea in COPD, dyspnea relief positions and breathing exercises should not be neglected in the pulmonary rehabilitation program. The use of sitting leaning forward and sitting leaning forward at a table position together with breathing control can help individuals with COPD to get more effective relief from dyspnea and provide greater energy efficiency. Further studies to assess the long-term impact of different types of exercise training on neural respiratory drive in key respiratory muscles are recommended to improve the management of dyspnea and exercise tolerance in patients with COPD.