**1. Introduction**

The physiological implications of reductions in physical activity due to an environment that is oversaturated with technological innovation are only beginning to be realized [1,2]. Adverse changes in respiratory patterns are just one of these deleterious adaptations, and dysfunctional breathing has become increasingly common with an expected prevalence of between 60–80% in otherwise healthy adults [3].

Gas exchange during normal activity is coordinated by inspiratory and expiratory processes involving synchronized movement of the upper and lower chest, abdomen, and diaphragm [4–7]. In the resting state, breathing is regulated by an expansion of the lower chest and anteroposterior movement of the sternal bones that is facilitated by the diaphragm and intercostal muscles that account for ~2–5% of whole-body oxygen consumption at rest. During intensive muscle work, respiratory energy demand can increase several times. In the case of trained athletes, it reaches up to 10% of the total energy consumption during moderately demanding activity [8–10]. Meanwhile, excess

**Citation:** Bahenský, P.; Bunc, V.; Malátová, R.; Marko, D.; Grosicki, G.J.; Schuster, J. Impact of a Breathing Intervention on Engagement of Abdominal, Thoracic, and Subclavian Musculature during Exercise, a Randomized Trial. *J. Clin. Med.* **2021**, *10*, 3514. https://doi.org/10.3390/ jcm10163514

Academic Editor: David Rodríguez-Sanz

Received: 4 July 2021 Accepted: 6 August 2021 Published: 10 August 2021

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involvement of areas of the upper chest distinctly characterizes respiratory inefficiency and potential breathing disorders [4,11], which may become increasingly relevant during high intensity work where ventilatory oxygen demand may comprise 15% (or more) of wholebody oxygen consumption [8–10].

Though inter-individual variability characterized by differential involvement of abdominal, thoracic, and subclavian body sectors in breathing patterns have been observed [12], systematic analysis of the effect of breathing technique on athletic performance is vastly understudied [13]. However, the influence of breathing patterns on performance has recently come to the forefront of physical activity research [14], and the role of the diaphragm during high-intensity work has received significant attention [13,15]. In individuals with dysfunctional respiration, the pain threshold is lowered, and control of motor functions and movement dysfunctions are impaired, all of which may adversely affect the individual s physical performance [16]. Pertinently, increasing diaphragmatic respiratory involvement reduces breathing effort, improves ventilation efficiency, reduces dyspnea, improves exercise tolerance, and can be trained [17–20]. Thus, there is great incentive to elucidate techniques to improve respiratory efficiency as a potential means to improve athletic performance [21–23].

Specific respiratory (inspiratory) muscle training (IMT) improves the function of the inspiratory muscles. According to literature and clinical experience, there are three established methods: (1) resistive load, (2) threshold load, and (3) normocapnic hyperpnea. Each training method and the associated devices have specific characteristics [24]. Setting up an IMT should start with specific diagnostics of respiratory muscle function and be followed by detailed individual introduction to training. Changing respiratory muscular activity through strengthening of inspiratory muscles may attenuate disease risk. Weakness or fatigue of the diaphragm and the accessory muscles of inspiration is widely recognized as a cause of failure to wean from mechanical ventilation [25]. The influence of IMT on exercise performance has also been surveyed. Faghy and Brown [22] provided evidence for the ability of IMT training to improve exercise performance (time trial) with thoracic load carriage.

Many methods can be used to evaluate the respiratory pattern [26], the most common of which are palpation, chest circumference, plethysmography of the whole body, chest skiagram, spirometry or various instruments recording changes in height of individual torso segments, or through a three-dimensional system [27–29]. Estimation of chest wall motion by surface measurements allows one-dimensional measurements of the chest wall by assessment with an optical reflectance system [30] or by three-dimensional tracking [31,32]. Chest wall volume changes can be assessed by optoelectronic plethysmography [33] or by optoelectronic plethysmography [34]. Building upon these techniques, our group used a respiratory muscle dynamometer to measure instantaneous values of involvement of the ventilatory musculature (MD03 muscle dynamometer) [11,35,36]. Using this dynamometer, the present study evaluated whether two-months of a yoga breathing exercise program may influence breathing characteristics during various intensities of exercise in young healthy athletes.

Based on previous work by our group [37], we hypothesized that the breathing exercise program would modulate respiratory musculature contribution. We anticipated greater involvement of the musculature of the lower torso (i.e., abdomen and thoracic sectors) and less upper-body contribution (i.e., subclavian) during exercise following the yoga-based breathing intervention.

#### **2. Materials and Methods**

#### *2.1. Subjects*

Forty-six adolescent distance runners (14–18 years) participated in our study: 23 males (age = 16.4 ± 1.1, height = 177.1 ± 5.8 cm, weight = 62.4 ± 5.8 kg) and 23 females (age = 16.8 ± 1.1, height = 168.5 ± 4.4 cm, weight = 55.9 ± 4.0 kg). All participants reported a history of endurance running of at least six times a week for the past year. They are all members of the same training group, and thus training volume and intensity were

comparable throughout the duration of the study. Participants were randomly allocated to an experimental group (*n* = 23), which took part in an eight-week breathing intervention, or a control group (*n* = 23), which continued training but did not carry out the yoga-based breathing intervention. One participant did not complete the intervention for medical reasons unrelated to the intervention and was excluded from the study. The two groups, both experimental and control, followed the same training program, the only difference being that the experimental group performed the yoga-based breathing intervention. A randomization sequence has been generated using Randomization.org. An independent person not involved in this study made the computer-generated randomization sequence. The study protocol was reviewed and approved by the local ethics committee on 19 October 2018 (002/2018) and followed the guidelines of the World Medical Assembly Declaration of Helsinki. This research is a clinical trial (NCT04950387). Written informed consent to participate was provided by guardians and verbal assessment was provided by the participants.
