Use of Powerbreathe ® in inspiratory muscle training for athletes : systematic review

Introduction: Inspiratory muscle training (IMT) has been used as part of athletic training. It is bene icial due to an increase in respiratory capacity, and can be related to the optimization of exercise tolerance. There are a growing number of publications on the subject, however the methodological rigor of these publications is still unknown. Objective: To perform a systematic literature review in order to analyze the effects of Powerbreathe® on inspiratory muscle training by athletes. Methods: Original scienti ic studies published in English, from 2000 to 2015, were included. Their typology was classi ied. The literature search was performed in the Lilacs, Medline, Pubmed, and Scielo databases using the following keywords: inspiratory muscle training, athletes, and Sports medicine (in English), treinamento muscular inspiratório, atleta, medicina esportiva (in Portuguese). Results: Inspiratory muscle training with speci ic linear resistance has been used in some athletic training, and its results are promising. However, its application is still recent and generally supported by experiments with limited population and which do not properly de ine the confounding factors for the results. Conclusion: The state of the art suggests that IMT is useful as a respiratory therapy supporting the training of athletes for some speci ic sports. However, there is a scarcity of studies of high methodological quality, thus requiring further experiments on the subject.


Introduction
High-performance athletic training includes numerous variables, all of which have a signi icant in luence on inal performance in the sport (1,2).Physical training is crucial for optimization of exercise performance, either to gain strength and power, or to prevent musculoskeletal injuries (3,4).Cardiovascular conditioning focuses on maximizing perfusion capacity, thereby preventing lactic acidosis, which knowingly compromises performance (4,5).However, a forgotten facet is respiratory training (6,7).Its bene its are associated with a greater supply of oxygen to the tissues, thereby providing a differentiated physical performance (8 -16).
The respiratory system and its regulatory centers control the levels of oxygen (O 2 ) and carbon dioxide (CO 2 ), which is released at higher levels in bursts of activity or activity sustained for a long period (17 -19).Recent studies suggest that the inspiratory muscles can interfere in the performance of physical exercise in athletes, precisely because in physically stressful conditions, when the production of free radicals exceeds elimination capacity, a re lex sympathetic reaction of peripheral vasoconstriction would be triggered, leading to early fatigue in skeletal muscles and dramatically reducing performance in this activity.Conditioned muscles, on the other hand, have an increased tolerance, thereby slowing re lex activation (19 -21).
Inspiratory muscle training (IMT) is a therapeutic modality that overcomes resistance against muscles responsible for expanding the rib cage.This effort must be controlled, speci ic and repeated at regular intervals.Its application has been demonstrated as a viable strategy for optimizing the respiratory capacity (22 -28), thereby allowing this person to always expand his/her physical tolerance to adverse situations during practice (29 -36).
Powerbreathe ® is one of the existing linear load resistor models on the market, which generates resistance via a spring-loaded system or an electronic valve.The basic difference between this tool and the others is its ability to offer the largest load during the therapy, and to adapt inspiratory resistance to the pressure x lung volume curve (13,37), which could generate load stabilization along the breath, by providing a feeling of comfort to the patient.Up until now this concept has a physiological basis.
Currently, a growing amount of evidence on the use of IMT associated with various sports has been published (22, 29 -36).However it is necessary to systematically analyze the methodological rigor of these experiments in order to delimit the real bene it of IMT in athletic training.In addition, knowledge about this therapeutic resourceits indication, dosage and bene its -is still not familiar to most of the scienti ic community.Thus, the aim of this study is to perform a systematic review of the literature in order to analyze the effects of Powerbreathe ® on inspiratory muscle training by athletes.

Methods
This study was a systematic literature review on the use of inspiratory muscle training, using a speci ic linear resistor by athletes.The study was performed from October of 2013 to March of 2014.

Inclusion criteria
Original scienti ic studies were included, classi ied according to their typology as descriptive, experimental or causal-comparative; published between 2000-2015; inspiratory muscle training with Powerbreathe ® was a dependent variable in different protocols; athletic training was a dependent variable; various sports were included in their sample; had no athletes using another respiratory therapy in the studies; had a sample characterized by a group combination therapy with sports or an equivalent practice; was clear regarding the samples and the different analyses performed.

Search strategy
Initially these descriptors were established: inspiratory muscle training, athlete, sports medicine, when in the vernacular and in English language, "inspiratory muscle training", "athletes" and "Sports medicine" (in English), available in Descriptors of Health Sciences (DeCS) and the Medical Subject Headings (MeSH).In order to maximize the search, synonyms were adapted, as well as the related words used in the retrieved papers found previously.
By respecting the operational differences of each database, when possible, we decided to search in the primary ields "Title" or "Keywords" using "or" and "and" as connectors and the term "athletes" as a limitation.The survey was performed in the following databases: Lilacs, Medline, Pubmed, Scielo.

Selection criteria
Developed by the Physiotherapy Evidence Database, the PEDro scale is a tool that quanti ies the methodological quality of randomized clinical trials (RCT), or quasi-randomized studies.It has external validity (criterion 1, not considered), internal validity criteria (2 -9, considered) and if there is suf icient statistical analysis in the results of the experiment, this should be considered (criteria 10 and 11) (38 -40).Thus, the criteria are classi ied dichotomously as "satis ied" or "not satis ied", and can have a maximum degree of methodological requirement, reaching a total of ten points.
Although this scale was adopted as a selection tool for this systematic review, considering the inability to blind those responsible for the intervention and the athletes who participated in experiments with IMT, the chosen cutoff point was > 3 (39).
The PEDro scale was also used as a tool for selecting non-experimental studies accepted according to the inclusion criteria.However, these studies needed to meet criteria 1, 10 and 11, at a minimum, to legitimize their potential generalization and interpretation of results (38,40).
The articles identi ied in the search strategy were evaluated independently and in a blinded fashion by two researchers (BRVNJ and TBG), strictly observing the inclusion criteria.The article selection was initiated using the key words, followed by the article selection according to the titles, which would focus on inspiratory muscle training in association with sports practice.In the next stage, the abstracts of the preselected articles were read and studies were included that satis ied the inclusion criteria described above.
Finally, due to the established cutoff point for the selection criteria, the most experienced researcher in this particular topic independently analyzed the experiments.

Results
Eight hundred thirty-six articles were found using the descriptors.After reading the titles, 36 articles remained on the use of the selected linear resistor in athletes.After methodological examination, eight articles were selected that met the established inclusion criteria; two were excluded because they had a PEDro score ≤ 3. Six clinical trials were included in this systematic review.Figure 1 shows the lowchart for article selection.

Study characteristics and quality
The evaluation of methodological quality using the PEDro scale had a mean score of 4.5 (4 -5).Table 1 shows details on the methodological and quality evaluation of the studies.Only one study used a third group with IMT association with expiratory muscle training (EMT) in this review (29), and one article was performed outside the United Kingdom (UK) (36).The low quality identi ied by the PEDro scale signals to the need for further studies with greater methodological rigor.(To be continued)

Characteristics of the population included in the studies
The studies used a population of young adults, with a mean age of 22.9 ± 2.8 years.There was gender balance in the studies; three studies included only male athletes, two included male athletes, and Kilding et al. (36) included athletes of both genders.

Inspiratory muscle training intervention program
The included articles had a standardized frequency of IMT.All studies used an inspiratory load of approximately 50% of maximal inspiratory pressure (MIP), one series of 30 breaths, repeated twice daily.At the same time, this uniformity did not extend to the time taken to perform the IMT protocols, with a period ranging from four to 11 weeks of training.Four studies, equivalent to 66.6% of the articles, adopted six weeks of IMT associated with sports training.

Measured outcomes
The article search addressing association of concomitant sports training to an IMT protocol suggests bene its to lung capacity, mainly expressed by the improvement of MIP, present in 62.5% of the articles.In addition, referred gains of associated training included reduced perceived exertion during sports practice, measured by the Borg scale.One study (31) found a statistically signi icant increase in the maximum volume of oxygen (MaxVO 2 ).The improved sports performance in regard to timed activity can also be related to the combination of therapeutic modalities (Table 3).Eligibility and randomization were implemented in all studies; however, only three of them clearly stipulated how randomization was performed.The therapists were not blinded in any article.Table 2 expresses the intervention protocols applied in each study, as well as the IMT program duration.This table also demonstrates that biking was the sport in 50% of studies, followed by rowing (33.3%), and swimming (16.6% of the studies).

Discussion
The use of IMT using a speci ic linear resistor showed bene its for respiratory capacity.In addition, the reviewed studies suggested that the association between IMT and speci ic athletic physical training could improve physical performance, when compared to a control group.
The exposure of inspiratory muscles to a training program with controlled and individualized load, repeated regularly, provides gain in sarcomeres, increasing muscle volume and its ability to generate strength.This information is still empirical, based on muscle physiology.However, in line with this reasoning, this review with athletes submitted to IMT led to an improvement in MIP compared to the placebo group, with a gain of between 17 -28% in the baseline studies.The heterogeneity between the time taken for the training protocol is a plausible explanation for this variability in the inal MIP.
The IMT protocol was useful when comparing the training of athletes in different sports.Swimming, rowing and cycling were the sports that were associated with respiratory training.In these experiments, there was a strong association between the associated program and the improvement in physical performance during the test against the clock.It should be noted that all six studies had small populations, with less than 20 athletes, which is insuf icient to rule out possible confounding factors.Studies were found that used IMT with soccer, running and tennis amateurs (22,34).However, they did not include the aim of this review.
The athletes treated with IMT with a linear load device had a minimized variability of heart rate (HR), respiratory rate (RR) and feeling of dyspnea, as reported by the Borg scale (20,31).These indings suggest that this treatment could improve tolerance during sports practice.Romer et al. (31), in studies with cyclists, improved MaxVO 2 following an associated program for six weeks, as compared to a placebo.Sheel et al. (19), in 2001, reported that inspiratory muscle fatigue activated a sympathetic re lex reaction of peripheral vasoconstriction, which would precipitate limb muscle fatigue during physical activity.This condition was known as metabore lex.
McConnell and Lomax (21), in a clinical trial using different IMT protocols associating lower limb (LL) exercises, observed early lower limb fatigue in the group exposed to severe respiratory muscle overload (greater than 70% of MIP).After the TMI protocol, the duration of fatigue with LL physical activity signi icantly increased.
All six studies included in this systematic review performed intervention protocols with thirty breaths under inspiratory resistance, equivalent to 56% of the MIP, repeated twice, seven days a week.This standardization facilitates comparison between studies and enables the adoption of this protocol in future studies.
Volianitis et al. (30) found an improvement in the six-minute all-out effort test with a rowing ergometer, in a study with rowers.The IMT program associated with ergometry found an improvement of 3.5 ± 1.2% in the distance covered in kilometers in the intervention group, compared with a 1.6 ± 1.0% gain in the placebo group, p < 0.05.The study by Grif iths and McConnell (29), using the same submaximal testing to assess gain between IMT and IMT/EMT groups, found that the IMT group had a mean improvement of 16.2 m in the inal distance in kilometers, with p = 0.02.The bene it was not evidenced for the IMT/EMT group.The alternating between IMT and EMT, associated with the small sample per group, are the main factors that could explain the lack of gain in the IMT/EMT group.
Of the six studies selected for this systematic review, ive were performed in the UK, the place in which Powerbreathe ® was created.Only the study by Kilding et al. (36) was performed in New Zealand.This observation could support the small propagation of scienti ic knowledge about the bene its of IMT for athletes.With regard to the choice of this linear resistor device for this population, it should be noted that the initial MIP of the population under study was 103 ± 7cmH2O.This magnitude, considered high compared to the mean of the general population, would impair the use of other resistors available on the market, since in most cases they have maximum inspiratory load lower than what is therapeutic for this MIP.
With regard to the strati ication with the PEDro scale, low methodological rigor was observed, with mean scores between 4 and 5.The similarity between the methods used probably is related to the fact that most of the studies were performed by the same group.Future studies are needed with larger populations that seek to blind investigators and athletes about the performed intervention.Of the eight studies selected as eligible for the review, two were excluded because they had a PEDro score ≤ 3.This criterion aimed to ensure the quality of evidence analyzed in this review.
Table 3 shows bene its of IMT using linear resistor for athletes.Kilding et al. (36) found a reduced swim time for 100m (p = 0.05) and 200m (p = 0.032) after IMT.Volianitis et al. (30), in studies with rowers, found an improvement in the 500m rowing time (reduction of 36' 69" in the IMT group versus a reduction of 11' 8" in the placebo group, with p < 0.05).Romer et al., in a study with cyclists, also evidenced an improved duration of 20km and 40km time-trials (p = 0.025 and 0.0009, respectively).This evidence is encouraging, and explains the need for further studies with larger populations and other sports.Only then will there be consensus for a recommendation to include IMT using a linear resistor in athletic training programs.

Conclusion
This systematic review has shown that the association between IMT and sports training favors the increase in MIP of athletes, but there is also a relationship with the improved performance in timed tests.The identi ied studies had a low methodological rigor, with small populations, and without the elimination of possible confounding factors.The IMT practice can be used in athletic training.However, it is necessary to eliminate gaps regarding the duration of the protocol, the sports for which it is bene icial, and studies that blind the population exposed to the intervention, thereby enabling elimination of psychological factors associated with the best inal performance.
The state of the art suggests that IMT is useful as an associated therapeutic resource in training for some speci ic sports.However, further studies with larger populations are necessary, which delineate the confounding factors and utilize greater methodological rigor.

Figure 1 -
Figure 1 -Flowchart of the article selection steps in the systematic review.

Table 2 -
Inspiratory muscle training protocols (TMI) and association with the sport.IMT = Respiratory Muscle Training; MIP = maximal inspiratory pressure

Table 3 -
Benefits of Inspiratory muscle training (IMT) with Powerbreathe ® in association with sports training Note: HR = Heart rate; IMT= Respiratory muscle training; MIP: Maximum inspiratory pressure; MEP: Maximum expiratory pressure; PETCO 2 = pressure of end-tidal carbon dioxide; EMT= Expiratory muscle training; TV= Tidal volume; VFC = Vital functional capacity.