Inspiratory Muscle Training Program Using the PowerBreath ® : Does It Have Ergogenic Potential for Respiratory and/or Athletic Performance? A Systematic Review with Meta-Analysis

eview and meta-analysis aim to provide scienti c evidence regarding the effects of training on respiratory muscle training's impact with the PowerBreath ® . A systematic analysis based on thePRISMAguides and a conducted research structured around the bases of Web of Science, Scopus, Medline/PubMed, SciELO y Cochrane Library Plus. Six articles published before January 2021 were included. The documentation and quanti cation of heterogeneity in every meta- analysis

evidence regarding the effects of training on respiratory muscle training's impact with the PowerBreath ® . A systematic analysis based on thePRISMAguides and a conducted research structured around the bases of Web of Science, Scopus, Medline/PubMed, SciELO y Cochrane Library Plus. Six articles published before January 2021 were included. The documentation and quanti cation of heterogeneity in every meta- analysis were directed through Cochran's Q test and the statistic I 2 ; additionally, a biased publication analysis was made using funnel plots, whose asymmetry was quanti ed Egger's regression. The methodological quality was assessed through McMaster's. PowerBreath ® administering a 15% resistive load of the maximum inspiratory pressure (PIM) achieves signi cant improvements (54%) in said pressure within 4 weeks of commencing the inspiratory muscle training. The maximal volume of oxygen (VO 2max) considerable enhancements was achieved from the 6 weeks associated with the maximum inspiratory pressure 21.5% post inspiratory muscle training onwards. Conversely, a signi cant blood lactate concentration decrement occurred from the 4th week of inspiratory muscle training, after a maximum inspiratory pressure 6.8% increment. PowerBreath ® is a useful device to stimulate sport performance and increase pulmonary function. Keywords: sports performance; ergogenic aids; respiratory muscles; inspiratory muscle training; pulmonary function; PowerBreath ® 1. Introduction The main function of the respiratory system is to maintain alveolar ventilation (oxygen- (O2) intake) in proportion to the metabolic needs of the organism, which increase during physical activity (PA) [1]. Also, carbon dioxide (CO2) exhalation is the main driver of ventilation to prevent arterial blood carbon dioxide pressure (PaCO2) from increasing and arterial blood oxygen pressure (PaO2) from decreasing [2]. During an intense and prolonged PA, the muscular endurance of the respiratory tracts decreases as a response to an increase in the respiratory muscle work and dyspnoea [3]. This fact induces fatigue in the respiratory muscles (RM) and reduces the respiratory function, resulting in a lessening of respiratory endurance [4]. This reduced respiratory activity could be connected to the activation of the metabolic re ex mechanism of the respiratory muscles (RMRM) “metabore- ex”. The RMRM is initiated by the fatigue of the

respiratory muscle work and dyspnoea [3]. This fact induces fatigue in the respiratory muscles (RM) and reduces the respiratory function, resulting in a lessening of respiratory endurance [4]. This reduced respiratory activity could be connected to the activation of the metabolic re ex mechanism of the respiratory muscles (RMRM) “metabore- ex”. The RMRM is initiated by the fatigue of the respiratory muscles, which, through the Int. J. Environ. Res. Public Health2021,18, 6703.

Int. J. Environ. Res. Public Health2021,18, 6703 2 of 18 afferent pathways III and IV, reaches the supraspinal level, causing a sympathetic vasocon- strictor response in the locomotor peripheral musculature which intensi es the fatigue of the active muscles and, in addition, increases the perception of effort, contributing to an endurance limitation linked to intense aerobic exercise [5]. Furthermore, the respiratory fatigue prevents the RM from reaching a suitable pleural pressure, this is an endurance limiting factor especially in disciplines which require aerobic resistance [6]. Other limiting factors of high-intensity physical endurance are pulmonary mechanics and pulmonary diffusion themselves [3]. Elite athletes of diverse modalities tend to combine ergogenic strategies in the hopes of improving their physiological responses and their competitive endurance; however, scienti c evidence is occasionally limited [7]. One of the strategies employed is inspiratory muscle training (IMT), whose purpose is to enhance exercise tolerance [8]. IMT has been used to minimize and/or delay respiratory fatigue, the RMRM and the blood lactate concentration (LA) [9]. In this way, IMT could be considered a training method with a potential ergogenic effect to improve athletic performance [10]. Additionally, it has been suggested that other physiological mechanisms could explain the ergogenic effect of the IMT: diaphragm hypertrophy, an increase of the sanguine ow to locomotor muscles, a diminution in the subjective blood ow, reduction of fatigue, decreased dyspnoea, an increment in the ef ciency and respiratory endurance, an alteration in the composition of muscular bres to type I and augmentation of bres type II in intercostal muscles, optimization of neuro-motor control in respiratory muscles maintaining the production of pressure with a minor motor impulse and a higher economization of the respiratory muscles [11]. Moreover, IMT is employed as a treatment for patients with respiratory condition—such as asthma, dyspnoea, and chronic obstructive pulmonary disease—with a better standard of living of the patients as a result [12,13]. IMT devices, which perform sectorized training of the respiratory muscles, can be divided into three categories: of resistive charge, of voluntary isocapnic hyperpnea, and threshold devices [14]. PowerBreathe ® (PwB) [PowerBreathe International Ltd. Southam, Warwickshire; England

patients with respiratory condition—such as asthma, dyspnoea, and chronic obstructive pulmonary disease—with a better standard of living of the patients as a result [12,13]. IMT devices, which perform sectorized training of the respiratory muscles, can be divided into three categories: of resistive charge, of voluntary isocapnic hyperpnea, and threshold devices [14]. PowerBreathe ® (PwB) [PowerBreathe International Ltd. Southam, Warwickshire; England UK] is a threshold device that allows air ow during an inspiration only after reaching a certain inspiratory pressure, which is adjustable through the tension of a spring in accordance with the maximal inspiratory pressure (MIP) of a patient. Once this pressure is surpassed and the valve is opened, the lineal resistance to the ow increment must be inappreciable [15]. The PwB device enables higher charges between 186 and 274 centimetres of water (cmH2O) pressure to be generated by the lungs due to the force of the inspiratory muscles [3]. The inclusion of new elements in PA routines and/or training routines has recently been carried out by both professional and recreational athletes, with the aim of estab- lishing adjustments that would turn into a differential element in their performance [3]. Nevertheless, the results are contradictory, because while IMT has proved to be effective in team sports [4,9,16], cycling [11,17] and runners [18,19], in other studies its ef ciency has not been proved [7,20]. Discrepancies could be a result of the methodology (intensity and/or duration of the exercises), the design of the studies and the athletic expertise of the individual employing IMT. Likewise, it is important to consider the kind of improvements attainable in relation to physical endurance. Considering these circumstances, we decided to execute a systematic revision of these practices to critically evaluate the effects of IMT on respiratory parameters and athletic performance. A PwB device was employed on people who practice diverse types of physical activities. This study describes the magnitude of the inspiratory resistance, the frequency, and the duration of the IMT to establish an optimal programme which will allow improvements in respiratory and athletic endurance. 2. Methods 2.1. Search Strategy This systematic review with meta-analysis focuses on

and athletic performance. A PwB device was employed on people who practice diverse types of physical activities. This study describes the magnitude of the inspiratory resistance, the frequency, and the duration of the IMT to establish an optimal programme which will allow improvements in respiratory and athletic endurance. 2. Methods 2.1. Search Strategy This systematic review with meta-analysis focuses on analysing the impact of IMT in the athletic endurance of physically active subjects through a PwB device. The study was

Int. J. Environ. Res. Public Health2021,18, 6703 3 of 18 conducted following thePreferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) guidelines. To select the studies, the PICOS question model was used as follows: P (population) “physical active practitioners”, I (intervention): “respiratory muscle training through the PwB device”, C (comparators): “some conditions with/without PwB”, O (outcome): “use protocol, employed methodology, respiratory parameters and sports performance” and S (studies design): “random design with/without placebo” [21]. A bibliographical structured research was carried out through the online search of original articles of three literary data bases (Web of Science, Scopus, Medline/PubMed, SciELO and Cochrane Library Plus). The search included original articles written in various languages and published before 31 January 2021. Apart from small variations in the mechanisms of the said databases, the same chain of research was used in every record. Search terms were a mix of medical subject headings (MeSH) and key words related to Powerbreath, inspiratory muscle training, exercise, and athletic performance. They were the following: (“Powerbreath”) AND (“muscle” OR “inspiratory muscle training” OR “inspiratory muscle strength”) AND (“performance” OR “athletic performance”) AND (“exercise” OR “physical activity” OR “aerobic capacity” OR “resistance”). Throughout this research, relevant articles were acquired by applying the snowball strategy. Every title and summary of the research were intersected to identify published articles and potential studies missing. The titles and summaries were examined afterwards for a later revision of the full text. The authors completed their investigation of the studies published independently and the discrepancies in relation to the physical parameters were resolved through a discussion. This process was conducted by two investigators (D.F.-L. andJ.M.-A.), who discussed discrepancies, and any disagreements were resolved by third-party evaluation (D.G.G.). 2.2. Selection of Articles: Inclusion and Exclusion Criteria To select the studies employed, the following inclusion criteria were applied: (1) Doc- uments should represent a well-designed experiment which includes respiratory mus- culature in a physical activity program via a PwB device in physically active subjects; (2) An identical situation in the subjects not employing a PwB; (3) Documents with no deadline restriction; (4) publications whose study subjects were physically

select the studies employed, the following inclusion criteria were applied: (1) Doc- uments should represent a well-designed experiment which includes respiratory mus- culature in a physical activity program via a PwB device in physically active subjects; (2) An identical situation in the subjects not employing a PwB; (3) Documents with no deadline restriction; (4) publications whose study subjects were physically active humans; (5) Speci c information related to PwB and physical activity; (6) Languages were limited to English, German, French, Italian, Portuguese and Spanish. Concerning the exclusion criteria, the following studies were not regarded: (1) Docu- ments not related to inspiratory muscle training with PwB; (2) Physically inactive individu- als or subjects with comorbidities which would avert respiratory training or the practice of physical activity; (3) Duplicated documents; (4) Experiments which were not performed in humans; (5) Studies that consisted of systematic or narrative revisions, editorials, letters to the editor or commentaries. 2.3. Data Extraction With the inclusion/exclusion criteria having been applied to every study, the data of the research source, including authors and date of publication, the participants' characteris- tics, the research design, the PwB device model employed, the inspiratory muscle training routine, the parameters analysed, and the results and conclusions of the experiments, were extracted independently by the authors using a spreadsheet (Microsoft Inc, Seattle, WA, USA). Subsequently, the discrepancies were resolved by having two authors (D.F.-L. and J.M.-A.) discuss among themselves until a consensus was reached. 2.4. Data Analysis Firstly, we proceeded to identify and quantify the heterogeneity of our data via Cochran's Q test and the I 2 statistic. Ap-value < 0.05 in the Q test was considered as a proof of the rejection of the null hypothesis regarding the homogeneity of the experiments. Additionally, I 2 values over 25%, 50% and 75% were selected to represent low, moderated,

Int. J. Environ. Res. Public Health2021,18, 6703 4 of 18 and high heterogeneity, respectively. Based on the results of these heterogeneity tests, we performed a xed-effect meta-analysis when the absence of heterogeneity was proved. Otherwise, a random effects meta-analysis model was employed. The variance among the studies in the random effects meta-analysis, also known as tau squared ( 2), was calculated using DerSimonian-Laird's method [22]. The effect size (ES) was estimated as the logarithmic transformed Ratio of Means (ROM) of the PwB and placebo groups. A z-test was implemented to determine the signi cance of the ES. Finally, a publication bias analysis was performed using funnel plots; these graphics' asymmetry was quanti ed employing the Egger's regression [23]. This bias analysis was carried out via the “Trim and ll” method. All the meta-analysis work ow was performed using the metaphor package (version 2.1-0) in R (The R Foundation for Statistical Computing, Vienna, Austria). 2.5. Quality Assessment The methodological quality evaluation of the selected articles was assessed using the McMaster's Critical Review Form [24]. The aim of this evaluation was to exclude studies with poor methodology, with a score less than or equal to 10 points. The methodological quality of the selected studies was assessed by the same two authors (D.F.-L. and J.M._A.), and any disagreements were resolved by third-party evaluation (D.G.G.). 3. Results 3.1. Selection of Studies We identi ed an initial total of 969 records of articles published after 2007. Among those, 695 were rejected for the lack of intervention and 256 because of not being related to the research topic. We also excluded 12 articles after full-text review. Reasons for exclusions after full-text review were unrelated outcomes (n= 7), unsuitable methodology (n= 1) and study design (n= 4). The remaining six studies (n = 6) [4,9,11,16,19,25] met our inclusion criteria and were included in the present systematic review (Figure). 3.2. Descriptive Information of the Selected Articles Included in the Systematic Review The characteristics of the studies included in the systematic review appear in Table. Table 1.Descriptive synthesis of the studies included in the systematic review. Subject's level Professional

The remaining six studies (n = 6) [4,9,11,16,19,25] met our inclusion criteria and were included in the present systematic review (Figure). 3.2. Descriptive Information of the Selected Articles Included in the Systematic Review The characteristics of the studies included in the systematic review appear in Table. Table 1.Descriptive synthesis of the studies included in the systematic review. Subject's level Professional 3 studies [4,9,25] Amateur 3 studies [11,16,19] Subject's age Senior (20–30) 5 studies [4,9,11,16,25] N/A 1 study [19] Training method 2 daily sessions, 5 days/week (30 inspirations 50% MIP) 3 studies [4,9,11] 4 weeks IMT + 6 combined weeks (IMT + EMT) 1 study [25] 2 running weekly sessions + IMT (30 inspirations) 1 study [19] 2 days/weeks regular football training + IMT (2 times/day 30 inspirations at the subject's own pace) 1 study [16] 4 weeks 1 study [19] 6 weeks 3 studies [9,11,16] 10 weeks 1 study [25] 12 weeks 1 study [4] MIP: maximal inspiratory pressure; IMT: inspiratory muscle training; EMT: expiratory muscle training; IM: inspiratory musculature.

Int. J. Environ. Res. Public Health2021,18, 6703 5 of 18 Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) ow diagram study selection process for the systematic review. 3.3. Results of the Quality Assessment Then we conducted a quality assessment of the articles. The scores of the selected articles ranged from 12 to 14 points. Five studies were“very good”and one was“good”. No studies were excluded because of poor quality. Details about the results of the quality assessment are shown in Table.

Int. J. Environ. Res. Public Health2021,18, 6703 6 of 18 Table 2.Results of the quality assessment. Reference ITEMS T E % MC 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Hartz el al. 2018 [4] 1 1 1 1 1 1 1 1 1 1 0 0 1 1 1 1 14 87.5VG Grif ths et al. 2007 [25] 1 1 1 1 0 1 1 1 1 1 1 0 0 1 1 0 12 75.0G Salazar-Mart½nez et al. 2017 [11] 1 1 1 1 0 1 1 1 1 1 1 1 0 1 1 0 13 81.3VG Edwars et al. 2015 [19] 1 1 1 1 0 1 1 1 1 1 1 0 1 1 1 1 14 87.5VG Archiza et al. 2017 [9] 1 1 1 1 0 1 1 1 1 1 1 1 0 1 1 0 13 81.3VG Guy et al. 2014 [16] 1 1 1 1 1 1 1 1 1 1 0 0 1 1 1 1 14 87.5VG T 7 7 7 7 2 7 7 7 7 7 5 1 3 7 7 3 (T) Total items achieved. (TE) Total items/study (1) Accomplished criteria; (0) Unaccomplished criteria MC: Methodological quality [Low 8 points; Acceptable (A) 9–10 points; Good (G) 11–12 points; Very Good (VG) 13–14 points; Excellent (E) 15 points]. 3.4. Performance Measures Table information about the authors, publication year, study design, population, the type of PwB device employed, the training protocol, the analysed parameters, the results, and the nal conclusions. Table 3.Summary of the results of the studies included in the systematic review. Characteristics of the Studies Included in the Systematic Review Authors/Year Population Study Design PowerBreaht ® Respiratory Muscle Training Analysed Parameters Results Conclusion Hartz et al. 2018 [4] 19 (20 3 yo) professional handball players. Group PwB:n= 10, 19 4 yo Placebo group:n= 9, 22 1 yo Random, with Placebo PwB Plus Heavy Resistance Sports Model 2 h/session 5 sessions/weeks For 12 weeks RES increment 50–70% MIP MIP MEP MVV PP VO2max "MIP * "MEP "MVV "PP

The study evaluates the ergogenic potential of inspiratory muscle training using PowerBreath.