Received: 4 November 2019 Revised: 8 February 2020 Accepted: 29 April 2020

DOI: 10.1002/pri.1852

RESEARCH ARTICLE

Validity, intra and inter-reliability of manual evaluation of the

respiratory muscle strength in asthmatic patients

Cassia da Luz Goulart1 | Renata Trimer2 | Adriana Sanches Garcia-Araujo1 |

Flavia Rossi Caruso1 | Paula Angélica Ricci1 | Polliana Batista dos Santos1 |
Renata Gonçalves Mendes1 | Audrey Borghi-Silva1

1
Cardiopulmonary Physiotherapy Laboratory,
Physiotherapy Department, Federal University
of Sao Carlos, Sao Paulo, Brazil
2
Course of Physiotherapy, University of Santa
Cruz do Sul, Rio Grande do Sul, Brazil., Santa
Cruz do Sul, Brazil
Correspondence
Audrey Borghi–Silva, Cardiopulmonary
Physioterapy Laboratory, Federal University of
Sao Carlos, Rodovia Washington Luís, Km
235, Jardim Guanabara, 13656–905. Sao
Carlos, Sao Paulo, Brazil.
Email: audrey@ufscar.br
Funding information
Ministry of Education/CAPES-Brazil; FAPESP,
Grant/Award Numbers: 2015/26501–1 and,
2018/03233–0
Abstract
Objective: This study investigated the concurrent validity, inter and intra-reliability of
manual evaluation in Asthma patients.
Methods: Twenty six asthma patients were assessed. Maximal respiratory muscle
strength (Mrms) was tested by inspiratory and expiratory pressure (MIP and MEP,
respectively) trough manovacuometer. In addition, Mrms of diaphragm (anterior and
posterior), Intercostals (lower and upper portion) and Rectus abdominal were
obtained manually, according to Medical Research Council (MRC) scale. Two inde-
pendents evaluators, previously trained, made both measurements.
Results: Reproducibility of Mrms intra-evaluators: anterior diaphragm (ICCs, 0.79 and
0.67); Posterior portion of the diaphragm (ICCs, 0.43 and 0.51); Upper intercostals
(ICCs, 0.47 and 0.40); Lower intercostals (ICCs, 0.81 and 0.51) and rectus abdominal
(ICCs, 1.0). Inter-reproducibility of anterior diaphragm was low to moderate, while
intercostals (upper and lower portion) was relatively low. However, rectus abdominal
presented high reproducibility reflecting in almost perfect agreement. In addition, we
found positive correlations between MIP versus Lower Intercostals (r = .60, p = .007)
and MEP versus rectus abdominal (r = .41, p = .04).
Conclusion: In asthmatic patients, manual evaluation of the respiratory muscles is reli-
able. In addition, maximal respiratory pressures using manometer assessment were
related to manual evaluation, in special to diaphragm and rectus abdominal muscles.

KEYWORDS

asthma, manual evaluation, maximal respiratory pressures, respiratory muscle strength

1 | I N T RO DU CT I O N affecting the health and wellbeing of children and young adults

Asthma is a chronic inflammatory disease of the airways characterized
by reversible airflow obstruction and bronchial hyperresponsiveness
(Almeida et al., 2013). As the most common chronic disease, asthma
has been considered a serious public health problem worldwide,
All authors takes responsibility for all aspects of the reliability and freedom from bias of the
data presented and their discussed interpretation.
(Bateman, Hurd, & Barnes, 2006; Hellebrandová et al., 2016).
Changes in respiratory system of asthmatic patients may be
responsible for decreasing the efficiency of the respiratory muscle,
hyperinflation, which flattens the diaphragm and consequently
shortens the inspiratory muscle (Caruso et al., 2015; Cavalcante & da
Silva, 2010), worsening of pulmonary function and reducing of respi-
ratory muscle strength (RMS). Intermittent lung hyperinflation might
produce abnormal coordination of muscular and respiratory cycles

Physiother Res Int. 2020;e1852. wileyonlinelibrary.com/journal/pri © 2020 John Wiley & Sons, Ltd 1 of 8
https://doi.org/10.1002/pri.1852
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(Black & Hyatt, 1969; Duiverman et al., 2009) and treatment with cor-
ticosteroids may additionally lead to a steroid-induced myopathy
(Black & Hyatt, 1971).
In this context, RMS evaluations may quantify and independently
characterize the clinical conditions of the patients. Maximal inspira-
tory pressure (MIP) and maximal expiratory pressure (MEP) are known
to reflect the weakness of respiratory muscles and can be assessed
through an analog or digital manovacuometer (Chaitow, Bradley, &
Gilbert, 2002). Such strategies have been used to evaluate the effects
of inspiratory muscle training on this population.
However, little is known about manual techniques to assess RMS
and there is no study that evaluated the reproducibility of manual
techniques in asthmatic patients. It is believed that due to the inter-
dependency between the respiratory and musculoskeletal systems,
several manual techniques have been proposed, aiming to increase
the mobility of the thoracic structures, which are involved in respira-
tory mechanics (De Bruin, Ueki, Watson, & Pride, 1997;
Decramer, 1997).
Manual evaluation of the diaphragm is a simple bedside tool and
it is frequently required for several professionals, such as physiothera-
pists, osteopaths and chiropractors. Bordoni, Marelli, Morabito, and
Sacconi (2016) found that the existing scientific literature had not
examined the manual evaluation on different portions of the
da LUZ GOULART ET AL.
diaphragm and manually assessed the diaphragm focusing on the ana-
tomical foundations. As a result, the authors conclude that manual
evaluation technique deserves to be further investigated. Further-
more, to our knowledge, validity, intra- and inter-reproducibility of
manual respiratory muscle strength (Mrms), have not been demon-
strated so far.
Thus, the aim of the present study was to test concurrent validity,
intra and inter-reproducibility of manual techniques for the evaluation
of the respiratory muscle strength in patients with asthma. We
hypothesized that, for the examined population, the Manual respira-
tory muscle evaluation (Mrms) would be valid and reproducible, for
both intra- and inter-evaluator comparisons.
2 | METHODS
2.1 | Study design
This cross-sectional comparative study was designed following the
COSMIN statement recommendations. The study was approved by
the Research Ethics Committee (protocol number 1.015.742/2014)
and all patients signed a written informed consent prior to
participation.
FIGURE 1 Flowchart of the study
da LUZ GOULART ET AL.
2.2 | Subjects
Adults of both sexes, aged between 18 and 50 years, diagnosed with
asthma and non-smokers were recruited. The individuals were consid-
ered asthmatic based on the clinical and spirometric diagnosis (con-
firmed by pre- and post-bronchodilator) and classified according to
severity (Almeida et al., 2013). The individuals were considered stable
asthmatics in the following conditions: absence of respiratory symp-
toms, absence of exacerbations (assessed through the necessity of
unscheduled medical visits) and no reports of respiratory infections
for a period of <3 weeks. Spirometry was performed to establish the
classification of asthma according to the standards of the American
Society of ATS Chest (ATS, 2002).
Patients were selected in the community through oral dissemina-
tion, explanatory posters and the indication of other patients of the
research. Thirty individuals were first screened with four exclusions
after the initial assessments (Figure 1).
The exclusion criteria involved individuals unable to perform the
proposed measurements, surgeries in the last year, osteoarticular or
neuromuscular diseases that influence respiratory mechanics, body
mass index (BMI) > 30 Kg/m2, acute asthma, present unstable medical
conditions or desire to leave the study.
2.2.1 | Evaluators training protocol
Prior to the beginning of the study, two physiotherapists were
selected and trained to standardize the evaluation protocols. For
1 week, the evaluators were separately prepared through a video
class, in which they learned the procedures for grading manual muscle
strength and the anatomical positions to be followed in each manoeu-
vre. Subsequently, in different moments, both evaluators performed
the training with a healthy volunteer. During the practice, a supervisor
was responsible for instructing, correcting and answer questions
about all manoeuvres and hand positioning, in order to reduce the var-
iability of the measure. After the training period, examiners started
the investigation in different moments. The details of the measure-
ments are following described.
3 | PROTOCOL
All experimental procedures were performed in our institution at the
same parts of the day to avoid the influence of circadian changes. The
assessments occurred in an acclimatized room with a temperature
between 22 and 24 C and relative air humidity between 40 and 60.
The experimental procedures were performed over 3 days:
Visit 1: Clinical evaluation by a physiotherapist, followed by pul-
monary function testing (spirometry) (Evaluator 1);
Visit 2: The first assessment of respiratory muscle (manual and
digital), after a minimal interval of 24 hr (Evaluators 1 and 2);
Visit 3: The second assessment of respiratory muscle (manual and digi-
tal), after an interval of 7 days from the first evaluation (Evaluators 1 and 2).
3 of 8
3.1 | Pulmonary function
Pulmonary function was assessed using a digital spirometer
(EasyOne®, Model 2001, Zurich, Switzerland). Forced expiratory vol-
ume in 1 s (FEV1), forced vital capacity (FVC) and the association
between these variables (FEV1/FVC) were obtained. The test was per-
formed according to the American Thoracic Society guidelines and the
results were analysed according to the values predicted by Pereira,
Sato and Rodrigues (2007).
3.2 | Manual respiratory muscle evaluation
In supine position, the diaphragm, intercostal and rectus abdominis
muscles were evaluated as follow:
Diaphragm: The forearm of the evaluator was hold in parallel to
the abdomen of the patient, with the thenar and hypothenar emi-
nences of the hand at the level of the anterior margin of the costal
arch; a gentle push were performed in cranial direction to record the
elastic response of the tissue, for both right and left sides (Figure 2).
The Mrms was evaluated using the Medical Research Council (MRC)
muscle strength scale, graded from 0 to 5:
0—no contraction;
1—weak contraction, without movement and without expulsion
of the examiner's hand;
2—weak contraction, slight movement and attempt to expel the
examiner's hand;
3—movement against gravity and the patient's abdomen expels
the examiner's hand but without resistance;
4—movement against the resistance of the examiner's hand and
expulsion of the examiner's hand;
5—movement against a higher resistance of the examiner's hand
and expulsion of the examiner's hand.
External Intercostal: The first step is the assessment of the costal
movement; it consists of lateralization during inspiration with caudal
direction, and the opposite during expiration. The hands must gently
hold on the lateral sides of the costal margins, providing a palpatory
feedback of the costal behaviour (Figure 3).
Rectus abdominis: In Figure 4, rectus abdominis was evaluated in
dorsal decubitus, knees extended and during movement, hip flexion is
required while arms must be posted along the body.
3.3 | Maximal inspiratory and expiratory mouth
pressures
Respiratory muscle strength was determined by maximal inspiratory
(MIP) and maximal expiratory pressure (MEP) using a digital manome-
ter (MDI® model MVD300, Porto Alegre, Brazil).
The MIP values were obtained by the residual volume (RV), which
was repeated at least three times with a one-minute interval between
repetitions (ATS, 2002). The MEP was obtained by the total lung capac-
ity (TLC), as aforementioned for MIP. During the MIP manoeuvre, the
4 of 8
F I G U R E 4 Rectus abdominal protocol. Rectus abdominal was
evaluated in dorsal decubitus, knees extended and during movement
hip flexion is required and arms along the body”
subject maintained the mouthpiece in the oral cavity only during the
inspiration, whereas in the MEP manoeuvre, only during the expiration
(Jardim, Mayer, & Camelier, 2002). During the manoeuvres, the force
was maximally sustained for approximately 1 s. The highest value was
computed from a minimum of three repetitions for each manoeuvre (dif-
ferences of 10% or less between values for each repetition) (Neder,
Andreoni, Lerario, & Nery, 1999). To calculate the predicted RMS values,
we considered the equations of Neder et al. (1999).
da LUZ GOULART ET AL.
F I G U R E 2 (a) Manual anterior
diaphragm evaluation and (b) posterior
diaphragm evaluation
F I G U R E 3 (a) Manual evaluation
of superior Intercostal and (b) manual
evaluation of inferior Intercostal
3.4 | Statistical analysis
Data distribution were verified by the Shapiro–Wilk test. Descriptive
data were shown as mean and standard deviation. The Pearson's cor-
relation coefficients were analysed to investigate the associations
between the main variables, in which strong values ranged between
1.0 and .80, moderate values between .79 and .50 and weak values
less than .49, as significant.
The intra-evaluator reliability analyses were through intraclass
correlation coefficient (ICC), in continuous measurements. For reliabil-
ity of Mrms measured on an ordinal scale, Cohen's weighted kappa
was used. There were considered the following agreements: <0;
0–0.19, poor agreement; 0.20–0.39, slight agreement; 0.40–0.59,
moderate agreement; 0.60–0.79, substantial agreement and 0.80–1.0,
almost perfect agreement. Residuals were evaluated under the
assumptions of normality, constant variance and independence. The
r values were interpreted as follows: .00 to .19 = none to slight, .20 to
.39 = low, .40 to .69 = moderate, .70 to .89 = high and .90 to
1.00 = very high (Mills, Johnson, Barnett, Smith, & Sharpe, 2015). All
tests were made in Package for the Social Sciences (SPSS version
20.0) and values were accepted as p ≤ .05.
4 | RE SU LT S
Table 1 shows the sociodemographic, anthropometric and clinical vari-
ables. In majority, female, eutrophic, long-standing diagnosis, com-
pounded the sample. MIP and MEP values were slightly the predicted
for sex and age.
da LUZ GOULART ET AL. 5 of 8

4.1 | Inter-evaluators reproducibility was high and substantial (Kappa of 0.79 and 0.67). Manual evaluation
of the posterior diaphragm was moderate (Kappa of 0.43 and 0.51),
When inter-evaluators reproducibility was contrasted through Kappa upper intercostal was low (Kappa of 0.47 and 0.40); lower intercostal
ICC, it was observed that manual evaluation of the anterior diaphragm was moderate to substantial (Kappa of 0.81 and 0.51) and rectus
abdominis was very high (Kappa of 1.0) (Table 2).
Table 3 shows the intra-evaluators reproducibility. Manual evalu-
TABLE 1 Socio-demographic, anthropometric and clinical
ation of the anterior diaphragm (day 1 and day 7) presented low con-
variables of the asthmatic
cordance (Kappa of 0.34 and 0.35). Posterior diaphragm was
Variables Asthmatic (N = 26)
moderate and low (Kappa of 0.50 and 0.13), upper intercostal was
Age (years) 29 ± 9
classified as low (Kappa of 0.13 and 0.03), lower intercostal was also
Sex (women) 17 (62%)
low concordant (Kappa of 0.37 and 0.28) and the rectus abdominis
Weight (kg) 70 ± 14
was very high (Kappa of 1.0; Table 3).
Height (cm) 166 ± 9
Regarding correlations between maximal inspiratory and expira-
BMI (kg/cm2) 23 ± 4
tory mouth pressures and manual respiratory muscle evaluation, we
Asthma time (years) 20 ± 6
found significant and moderate correlations between MIP versus
Asthma control
Lower Intercostal (r = .606, p = .007) and MEP versus rectus abdominis
Controlled 78%
(r = .419, p = .046; Figure 5).
No controlled 12%
MRC 1.53 ± 0.5
FEV1 (%) 94.5 ± 10
5 | DI SCU SSION
FVC (%) 100.1 ± 8
FEV1/FVC 0.81 ± 0.07
This was the first study that evaluated the validity and reproducibility
MIP (cmHO2) 106.3 ± 31
of manual respiratory muscle evaluation in asthma patients, comparing
MIP (% predicted) 80.2 ± 20
with respiratory mouth pressures obtained through a manometer. The
MEP (cmHO2) 99.3 ± 27
main findings of the present study were: (I) Inter-evaluators reproduc-
MEP (% predicted) 69.8 ± 19
ibility: anterior diaphragm and rectus abdominis were perfect;
Abbreviations: BMI, body mass index; FVC, slow vital capacity; FEV1, (II) Intra-evaluators reproducibility: rectus abdominis was almost per-
forced expiratory volume in 1 second; FEV1/FVC, ratio between FEV1 and fect (day 1 and day 7); (III) Correlations between MIP and lower inter-
forced vital capacity; MEP, maximum expiratory pressure; MIP, maximum
costals; MEP and rectus abdominis.
inspiratory pressure.

TABLE 2 Inter-evaluators reproducibility of manual measurements of respiratory muscles

Evaluator 1 Evaluator 2

Muscle Kappa Standard error CI 95% Kappa Standard error CI 95%

Anterior diaphragm 0.799 0.097 0.608–0.989 0.675 0.128 0.425–0.926
Posterior diaphragm 0.438 0.180 0.0841–0.791 0.519 0.204 0.118–0.920
Upper intercostal 0.475 0.144 0.194–0.756 0.406 0.205 0.00421–0.808
Lower intercostal 0.816 0.101 0.619–1.000 0.517 0.135 0.252–0.782
Rectus abdominal 1.000 0.000 1.000–1.000 1.000 0.000 1.000–1.000

Abbreviations: CI, confidence interval; ICC, intraclass correlation coefficient.

TABLE 3 Intra-evaluators reproducibility (day 1–day 7) of manual measurements of respiratory muscles (online supplement)

Measure 1 Measure 2

Muscle Kappa Standard error CI 95% Kappa Standard error CI 95%

Anterior diaphragm 0.346 0.107 0.136–0.556 0.356 0.138 0.0862–0.626
Posterior diaphragm 0.506 0.191 0.132–0.880 0.136 0.206 0.268–0.541
Upper intercostals 0.135 0.242 0.340–0.610 0.034 0.199 0.356–0.424
Lower intercostals 0.372 0.180 0.0191–0.725 0.285 0.175 0.0586–0.628
Rectus abdominal 1.000 0.000 1.000–1.000 1.000 0.000 1.000–1.000
6 of 8
F I G U R E 5 Correlation coefficient (r) and p-value (p) between maximal inspiratory (MIP) and expiratory (MEP) mouth pressures and manual
respiratory muscle evaluation (online supplement). Online supplement; ICC, intraclass correlation coefficient; CI, confidence interval
5.1 | Inter and intra-evaluators reproducibility
In our study, we demonstrated a high reproducibility for the anterior
diaphragm and rectus abdominis muscles. However, the posterior por-
tion of the diaphragm and intercostal did not present the same results.
These results may be explained by the anatomic position of these
muscles, which are difficult to palpate and to obtain a good manual
evaluation (Bordoni et al., 2016). In addition, changes in rib cage
mechanics resulting from previous exacerbations may alter the
mechanics and variety the availability of fibres and portions of the dia-
phragm, and consequently, complicating manual evaluation18,19,20. In
this sense, the mechanical changes imposed by the disease may not
influence the anterior diaphragm and rectus abdominis muscles, which
presented high inter-evaluator reproducibility. In addition, the simply
palpation, localization and evaluation of rectus abdominis, compared to
other muscles, might explain our results rectus abdominis.
Regarding inter-evaluator errors, we believe that the measure of
intercostal is more likely to induce to a measurement error, particu-
larly when two independent examiners are compared. Our results
reinforce the necessity of trained examiners (preferentially the same
for pre and post) to perform manual measurement of inspiratory
strength in future interventional studies, in order to reduce the large
variability of this measurement.
Regarding intra-evaluators, we only found high reproducibility for
rectus abdominis, which may be justified by the previously described
findings, besides the authors' consideration that evaluators must be
experienced and trained to perform this measurement. We hypothesize
that this result may be justified by the different evaluation techniques.
In synthesis the evaluation of intercostal involves correct positioning of
the hands and perception of movement from the evaluator, which
requires concentration and similar execution of the patient's manoeuvre
(day 1 and 7). On the other hand, compared to intercostal, the abdomi-
nal evaluation is more visual and simple, once it depends on the move-
ment of the volunteer. Another hypothesis, due to the inexperience of
the evaluator, there is an inconsistency between the reliability of the
da LUZ GOULART ET AL.
measure and the inability to select the exact location of the evaluation
of the other muscles (Neves et al., 2014).
5.2 | Relationship between RMS and manual
respiratory muscle evaluation
We found a direct relationship between MIP and lower intercostal.
This result may be justified considering the musculature involved in
the inspiration. Several authors consider that MIP corresponds to the
strength of the set of all respiratory muscles (Heneghan, Adab,
Balanos, & Jordan, 2012; Salito, Luoni, & Aliverti, 2015). Furthermore,
the relationship between MEP and rectus abdominis might be
explained considering that MEP reflects the strength of the abdominal
and intercostal muscles (Heneghan et al., 2012; Salito et al., 2015).
The easiest evaluation of manual muscle strength compares the rectus
abdominis evaluation with MEP, facilitating the application of this
method in clinical practice, which also allows its strengthening, an
important aspect in the rehabilitation of asthmatic patients. This fact
is in agreement with some studies with other populations (Sarro,
Mombrini, & Tonole, 2018; Simões et al., 2010), which are focused in
the expiratory musculature strengthening, involved in coughing and
maintenance of the bronchial hygiene (To et al., 2012).
RMS was evaluated through a manometer, which is widely used
in clinical practice and considered an effective and reliable technique.
MIP and MEP reflect more significantly the respiratory muscle weak-
ness than forced vital capacity assessed by the spirometry (Weber &
Lamb, 1970). In addition, these techniques are widely used to measure
respiratory muscle strength. However, manual measurements to
assess respiratory muscle strength have no longer been validated for
the asthmatic population. Thus, we highlight the novelty of our study,
in which we validated a manual evaluation method for asthmatic
patients and considered the evaluation of rectus abdominis and lower
intercostal to quantify respiratory muscle strength. Manual methods
have been frequently used in clinical practice, once they are simple
da LUZ GOULART ET AL. 7 of 8

methods of RMS evaluation and can be used as an alternative in hos- Bateman, E. D., Hurd, S. S., & Barnes, P. J. (2006). Global strategy for
pital in clinical settings. asthma management and prevention: GINA executive summary. The
European Respiratory Journal, 31, 143–178.
Black, L. F., & Hyatt, R. E. (1969). Maximal respiratory pressures: Normal
values and relationship to age and sex. The American Review of Respira-
5.3 | Limitations and relevance tory Disease, 103, 641–650.
Black, L. F., & Hyatt, R. E. (1971). Maximal respiratory pressures in general-
ized muscular disease. The American Review of Respiratory Disease,
Maximal static pressure measurements provide objective and repro-
103, 641–645.
ducible test results in COPD patients, are important for establishing Bordoni, B., Marelli, F., Morabito, B., & Sacconi, B. (2016). Manual evalua-
diagnosis and initiating the treatment (ATS, 2002; Weiner, Azgad, tion of the diaphragm muscle. International Journal of Chronic Obstruc-
Ganam, & Weiner, 1992). Thus, through the validation of manual mus- tive Pulmonary Disease, 11, 1949–1956.
Caruso, P., Albuquerque, A. L., Santana, P. V., Cardenas, L. Z.,
cle assessment methods, it can also be considered for the evaluation
Ferreira, J. G., … Carvalho, R. (2015). Diagnostic methods to assess
of weakness of the diaphragm and rectus abdominis muscles, and pro- inspiratory and expiratory muscle strength. Jornal Brasileiro de
posed treatment for these patients. Pneumologia, 41(2), 110–123.
The major limitations of our study were the non-evaluation of the Cavalcante, A. M. M., & da Silva, H. J. (2010). Role of maximal inspiratory
pressure in the evaluation of respiratory muscle strength in asthmatics
presence of hyperinflation in the patients and the necessary training
- systematic review. Revista Portuguesa de Pneumologia, 16(3),
time (Weiner, Suo, Fernandez, & Cherniack, 1990) for an evaluator to
463–470.
achieve excellence in the performance of measures. However, we Chaitow, L., Bradley, D., & Gilbert, C. (2002). Multidisciplinary approaches
emphasize the relevance of our study, once we validated and analysed to breathing pattern disorders (1st ed., p. 142). London: Churchill
the reproducibility of the evaluation of manual muscle strength in Livingstone.
De Bruin, P., Ueki, J., Watson, A., & Pride, N. (1997). Size and strength of
asthmatic patients.
the respiratory and quadriceps muscles in patients with chronic
In conclusion, manual evaluation of the respiratory muscle is reli- asthma. The European Respiratory Journal, 10, 59–64.
able for asthmatic patients, however, there is a high variance for inspi- Decramer, M. (1997). Hyperinflation and respiratory muscle interaction.
ratory muscles over time. In addition, maximal respiratory pressures The European Respiratory Journal, 10, 934–941.
Duiverman, M. L., de Boer, E. W., van Eykern, L. A., de Greef, M. H.,
obtained through a manometer were related to manual evaluation, in
Jansen, D. F., Wempe, J. B., … Wijkstra, P. J. (2009). Respiratory mus-
special to the diaphragm and rectus abdominis muscles. cle activity and dyspnea during exercise in pulmonary disease. Respira-
tory Physiology & Neurobiology, 167(2), 195–200.
ACKNOWLEDGEMEN TS Hellebrandová, L., Chlumský, J., Vostatek, P., Novák, D., Rýznarová, Z., &
Bunc, V. (2016). Airflow limitation is accompanied by diaphragm dys-
The authors would like to thank FAPESP (Grant numbers
function. Physiological Research, 65(3), 469–479.
2018/03233–0 and 2015/26501–1) and Ministry of Education/ Heneghan, N. R., Adab, P., Balanos, G. M., & Jordan, R. E. (2012). Manual
CAPES-Brazil, for financial support. therapy for chronic obstructive airways disease: A systematic review
of current evidence. Manual Therapy, 17(6), 507–518.
Jardim, J., Mayer, A., & Camelier, A. (2002). Musculos respiratorios y
CONF LICT OF IN TE RE ST
rehabilitacion pulmonar en asmaticos. Archivos de Bronconeumología,
The authors declare no potential conflict of interest. 38, 181–188.
Mills, D. E., Johnson, M. A., Barnett, Y. A., Smith, W. H., & Sharpe, G. R.
ORCID (2015). The effects of inspiratory muscle training in older adults. Medi-
cine and Science in Sports and Exercise, 47(4), 691–697.
Cassia da Luz Goulart https://orcid.org/0000-0001-8731-689X
Neder, J. A., Andreoni, S., Lerario, M. C., & Nery, L. E. (1999). Reference
Renata Trimer https://orcid.org/0000-0002-9635-1694
values for lung function tests. II. Maximal respiratory pressures and
Adriana Sanches Garcia-Araujo https://orcid.org/0000-0002-6491- voluntary ventilation. Brazilian Journal of Medical and Biological
6240 Research, 32(6), 719–727.
Flavia Rossi Caruso https://orcid.org/0000-0003-4240-1841 Neves, L. F., Reis, M. H., Plentz, R. D., Matte, D. L., Coronel, C. C., &
Sbruzzi, G. (2014). Expiratory and expiratory plus inspiratory muscle
Paula Angélica Ricci https://orcid.org/0000-0001-6629-7933
training improves respiratory muscle strength in subjects with COPD:
Polliana Batista dos Santos https://orcid.org/0000-0003-3354- Systematic review. Respiratory Care, 59(9), 1381–1388.
8913 Pereira, C. A. C., Sato, T., & Rodrigues, S. C. (2007). New reference values
Renata Gonçalves Mendes https://orcid.org/0000-0003-4683-2657 for forced spirometry in white adults in Brazil. Jornal Brasileiro de
Pneumologia, 33(4), 397–406.
Audrey Borghi-Silva https://orcid.org/0000-0002-3891-6941
Salito, C., Luoni, E., & Aliverti, A. (2015). Alterations of diaphragm and rib
cage morphometry in severe COPD patients by CT analysis. Confer-
RE FE R ENC E S ence Proceedings: Annual International Conference of the IEEE Engineer-
Almeida, V. P., Guimar~aes, F. S., Moço, V. J., Ferreira Ade, S., ing in Medicine and Biology Society, 1, 6390–6393.
Menezes, S. L., & Lopes, A. J. (2013). Is there an association between Sarro, K. J., Mombrini, C. L., & Tonole, T. B. (2018). Reliability and mini-
postural balance and pulmonary function in adults with asthma? mal detectable change of thoracoabdominal mobility measurements
Clinics, 68(11), 1421–1427. using photogrammetry. Physiotherapy Theory and Practice, 34(9),
ATS board of directors, ERS executive committee (ATS). (2002). ATS/ERS 730–739.
statement on respiratory muscle testing. American Journal of Respira- Simões, R. P., Deus, A. P., Auad, M. A., Dionísio, J., Mazzonetto, M., &
tory and Critical Care Medicine, 166, 518–624. Borghi-Silva, A. (2010). Maximal respiratory pressure in healthy 20 to
8 of 8 da LUZ GOULART ET AL.

89 year-old sedentary individuals of Central S~ ao Paulo state. Revista subjects and patients with asthma. The American Review of Respiratory
Brasileira de Fisioterapia, 14(1), 60–67. Disease, 141, 1501–1505.
To, T., Stanojevic, S., Moores, G., Gershon, A. S., Bateman, E. D.,
Cruz, A. A., Boulet, LP (2012). Global asthma prevalence in adults:
Findings from the cross-sectional world health survey. BMC Public
Health, 12, 204. How to cite this article: da Luz Goulart C, Trimer R, Garcia-
Weber, J. C., & Lamb, D. R. (1970). Statistics and research in physical educa- Araujo AS, et al. Validity, intra and inter-reliability of manual
tion, (1), 240. St. Louis, Missouri: The C.V. Mosby Company.
evaluation of the respiratory muscle strength in asthmatic
Weiner, P., Azgad, Y., Ganam, R., & Weiner, M. (1992). Inspiratory muscle
training in patients with bronchial asthma. Chest, 102, 1357–1361.
patients. Physiother Res Int. 2020;e1852. https://doi.org/10.
Weiner, S., Suo, J., Fernandez, E., & Cherniack, R. M. (1990). The effect of 1002/pri.1852
hyperinflation on respiratory muscle strength and efficiency in healthy