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ORIGINAL ARTICLE
Diaphragmatic Breathing Training Program Improves
Abdominal Motion During Natural Breathing in Patients With
Chronic Obstructive Pulmonary Disease: A Randomized
Controlled Trial
Wellington P. Yamaguti, PhD, Renata C. Claudino, PT, Alberto P. Neto, PT, Maria C. Chammas, PhD,
Andrea C. Gomes, MD, João M. Salge, PhD, Henrique T. Moriya, PhD, Alberto Cukier, PhD,
Celso R. Carvalho, PhD
ABSTRACT.YamagutiWP,ClaudinoRC,NetoAP,Cham- DBTPthan did the CG (F15.08; P.001). An improvement
mas MC, Gomes AC, Salge JM, Moriya HT, Cukier A, Car- in the 6-minute walk test and in health-related quality of life
valho CR. Diaphragmatic breathing training program improves was also observed in the TG.
abdominal motion during natural breathing in patients with Conclusions: DBTP for patients with chronic obstructive
chronic obstructive pulmonary disease: a randomized con- pulmonary disease induced increased diaphragm participation
trolled trial. Arch Phys Med Rehabil 2012;93:571-7. during natural breathing, resulting in an improvement in func-
Objective: To investigate the effects of a diaphragmatic tional capacity.
breathing training program (DBTP) on thoracoabdominal mo- Key Words: Breathing exercises; Diaphragm; Exercise tol-
tion and functional capacity in patients with chronic obstructive erance; Pulmonary disease, chronic obstructive; Quality of life;
pulmonary disease. Randomized controlled trial; Rehabilitation.
Design: A prospective, randomized controlled trial. © 2012 by the American Congress of Rehabilitation
Setting: Academic medical center. Medicine
Participants: Subjects (N30; forced expiratory volume in
1s, 42%13% predicted) were randomly allocated to either a HRONIC OBSTRUCTIVE PULMONARY disease (COPD)
training group (TG) or a control group (CG). Cischaracterized by an increased resistance to airflow, air
Interventions: Subjects in the TG completed a 4-week super- trapping, and lung hyperinflation. As lung volume increases,
vised DBTP (3 individualized weekly sessions), while those in the inspiratory muscles are passively shortened and thereby
the CG received their usual care. 1,2 Therefore, patients
placed at a mechanical disadvantage.
Main Outcome Measures: Effectiveness was assessed by am- with COPD frequently have a reduction of diaphragmatic mo-
plitude of the rib cage to abdominal motion ratio (RC/ABD bility and its relative contribution to thoracoabdominal mo-
ratio) (primary outcome) and diaphragmatic mobility (second- tion,3-5 enhancing the activity of chest wall respiratory muscles
ary outcome). The RC/ABD ratio was measured using respi- as a compensatory mechanism.6,7 It has been previously shown
ratory inductive plethysmography during voluntary diaphragmatic that both a reduction in diaphragmatic mobility and a higher
breathing and natural breathing. Diaphragmatic mobility was activity of chest wall respiratory muscles are associated with
measuredbyultrasonography.A6-minutewalktestandhealth- 8-10
increased dyspnea and exercise intolerance.
related quality of life were also evaluated. Breathing strategies have been considered as part of self-
Results: Immediately after the 4-week DBTP, the TG 11
management education actions in pulmonary rehabilitation
showed a greater abdominal motion during natural breathing and include a range of techniques, including diaphragmatic
quantified by a reduction in the RC/ABD ratio when compared breathing (DB). The principal aim of DB is to improve abdom-
with the CG (F8.66; P.001). Abdominal motion during inal motion while reducing chest wall respiratory muscle ac-
voluntary diaphragmatic breathing after the intervention was
also greater in the TG than in the CG (F4.11; P.05). The
TG showed greater diaphragmatic mobility after the 4-week
List of Abbreviations
CG control group
COPD chronic obstructive pulmonary disease
From the Departments of Physical Therapy (Yamaguti, Claudino, Neto, Carvalho) DB diaphragmatic breathing
and Radiology, Service of Ultrasound (Chammas, Gomes), School of Medicine, DBTP diaphragmatic breathing training
University of São Paulo, São Paulo; Pulmonary Division, School of Medicine,
University of São Paulo, São Paulo (Salge, Cukier); and Biomedical Engineering program
Laboratory, School of Engineering, University of São Paulo, São Paulo (Moriya), FEV forced expiratory volume in 1 second
Brazil. 1
Presented in abstract form (preliminary study results) to the European Respiratory FVC forced vital capacity
Society, September 21, 2010, Barcelona, Spain. HRQOL health-related quality of life
Nocommercial party having a direct financial interest in the results of the research NB natural breathing
supporting this article has or will confer a benefit on the authors or on any organi- RC/ABD ratio amplitude of rib cage to abdominal
zation with which the authors are associated. motion ratio
Clinical Trial Registration No.: NCT-01223807. RCT randomized controlled trial
Reprint requests to Celso R. Carvalho, PhD, Dept of Physical Therapy, School of
Medicine, University of São Paulo, Av. Dr. Arnaldo, 455, Room 1210, 01246-903, SGRQ St. George’s Respiratory Questionnaire
Sao Paulo–SP, Brazil, e-mail: cscarval@usp.br. 6MWT 6-minute walk test
0003-9993/12/9304-00545$36.00/0 TG training group
doi:10.1016/j.apmr.2011.11.026
Arch Phys Med Rehabil Vol 93, April 2012
572 DIAPHRAGMATIC BREATHING IN CHRONIC OBSTRUCTIVE PULMONARY DISEASE, Yamaguti
12 13
tivity. Asystematic review has pointed out some method- Training Program
ological problems in prior studies evaluating the benefits of DB The TG completed a DBTP consisting of three 45-minute
for patients with COPD. Of 24 clinical investigations included weekly sessions (12 sessions total). The program was individ-
in this review, only 3 were categorized as randomized con- ualized and supervised by a single physiotherapist (A.P.N.). In
14-16
trolled trials (RCTs). Oneofthesestudiesincludedpatients each session, the patients were instructed to perform a total of
with asthma and bronchiectasis in addition to COPD, and the 150breathingexercises in the following positions: supine, right
other investigations provided adjunctive therapies in addition and left lateral decubitus, sitting, and standing (3 series of 10
to DB, which makes it difficult to determine the specific effects repetitions in each position). Between each series of DB exer-
of DB for patients with COPD. Furthermore, the review dem- cises, patients were instructed to breathe normally for 1 minute.
onstrated that the role of DB for patients with COPD remains The following verbal instructions were given during inhalation
controversial. Results from uncontrolled studies have demon- and exhalation, respectively: “perform a slow maximal inspi-
strated that DB might improve gas exchange,17,18 respiratory ration allowing the air to go to your belly,” and “perform a
patterns,19,20 and the oxygen cost of breathing.21 On the other normal expiration without forcing abdominal retraction.” Tac-
hand, other investigators have suggested that DB may lead to tile feedback was provided by positioning one of the patient’s
detrimental effects in a specific population of patients with handsontheabdomenandtheotherhandontheupperribcage.
severe COPD.17,22 If necessary, visual and auditory stimulation was provided to
Despite these conflicting results, an improvement in abdom- correct uncoordinated respiratory patterns. DB competency
inal motion and a reduction in thoracic excursion during vol- was considered if the respiratory pattern adopted was associ-
untary DB have been described as common findings in several ated with at least a doubling of the abdominal tidal excursion
17,20,22,23 observed during NB.13,22 No patient in the CG or TG was
studies. Toour knowledge, no controlled studies have instructed to perform the exercises at home.
investigated the change in abdominal motion naturally adopted
after a diaphragmatic breathing training program (DBTP). We Outcome Measures
hypothesized that a short-term DBTP could induce higher
participation of the diaphragm during natural breathing (NB). Primary and secondary outcomes. Improvements in ab-
This modification in habitual breathing pattern would relieve dominal motion during NB and in diaphragmatic mobility,
respiratory symptoms and improve exercise tolerance and from baseline to post-DBTP, were used, respectively, as pri-
health-related quality of life (HRQOL). Therefore, in this RCT, mary and secondary outcomes. Patients from the CG and TG
we aimed to test the effects of a short-term DBTP on thoraco- were instructed to practice voluntary DB before the first eval-
abdominal motion, diaphragmatic mobility, and functional ca- uation of thoracoabdominal motion. This procedure aimed at
pacity in patients with COPD. evaluating whether a single instruction session was as effective
to change abdominal motion during NB as a supervised DBTP.
METHODS Dyspnea, HRQOL, and exercise tolerance were also evaluated.
Thoracoabdominal motion. Improvement in abdominal
motion was evaluated by means of a reduction in the amplitude
Participants of the rib cage to abdominal motion ratio (RC/ABD ratio)
Ninety-four patients with COPD diagnosed according to the recorded using a computer-assisted respiratory inductive pleth-
ysmography system (Respitrace).a Teflon-coated inductance
Global Initiative for Chronic Obstructive Lung Disease crite- bandsa of appropriate size were placed around the rib cage and
24
ria were recruited at a university hospital. Inclusion criteria abdomenandconnectedtoanoscillator module and calibration
were as follows: (1) age 50 to 80 years; (2) postbronchodilator 25
forced expiratory volume in 1 second (FEV ) 80% of pre- unit. Eachsubject was measured in a quiet, private room, and
1 26
dicted and an FEV to forced vital capacity (FVC) ratio (FEV / data acquisition was performed in a supine position for a total
1 1 period of 9 minutes, equally distributed as follows: (1) at
FVC ratio) 0.7; (3) stable respiratory condition without rest—basal NB; (2) during DB exercise—voluntary DB; and
changes in medication or symptoms for at least 4 weeks before (3) post-DB exercise. Pulse oximetry was continuously moni-
enrollment in the study; and (4) receiving regular treatment tored, and dyspnea sensations were evaluated every minute
with inhaled bronchodilators and steroids. Exclusion criteria using the modified Borg scale.27 Rib cage and abdominal wall
were (1) the presence of other cardiopulmonary or musculo- movement waveforms were digitized, and the RC/ABD ratio
skeletal diseases; (2) previous engagement in any exercise was calculated from the absolute changes in the circumference
training program in the prior 2 years; and (3) current smokers. of these compartments.22
Thehospital ethics committee approved the study (Protocol no. Diaphragmatic mobility. Anultrasonography examination
0348/08), and all patients provided written informed consent. was used to assess the craniocaudal displacement of the left
branch of the portal vein in order to measure diaphragmatic
Study Design 28 Patients were evaluated in the supine position using
mobility.
b
This was a prospective, parallel-group, randomized and an ultrasound scanner in B-mode. A 3.5-MHz convex trans-
blinded clinical trial. Patients were evenly allocated (1:1) to ducer was positioned over the right subcostal region, and the
either a training group (TG) or control group (CG). Random- position of the left branch of the portal vein was marked with
ization was stratified according to sex using random block sizes the cursor during forced expiration and inspiration. Three re-
of 2 and 4. Regular medical treatment was established in both producible measurements were performed, and the best value
groups before the first visit and remained unchanged through- was used for the analysis.
out the study. Patients in the TG completed a 4-week DBTP, Functional capacity. Spirometry and whole-body plethys-
while those in the CG received their usual care. Patients in both mography were performed using standard equipmentc accord-
groups were evaluated at baseline and at the end of a 4-week ing to the American Thoracic Society and the European Re-
period. The technicians who collected data for all outcome spiratory Society recommendations.29 Reported spirometry
measures (R.C.C. and A.C.G.) were blinded to the patients’ results were based on the best curve from 3 acceptable efforts
group allocation. (after the inhalation of 200g of salbutamol); they are pre-
Arch Phys Med Rehabil Vol 93, April 2012
DIAPHRAGMATIC BREATHING IN CHRONIC OBSTRUCTIVE PULMONARY DISEASE, Yamaguti 573
sented as a percentage of the predicted value.30 Dyspnea symp- protocol deviations in the CG because of either an acute COPD
toms at rest were assessed using the modified Medical Re- exacerbation or other health problems. These patients were
search Council dyspnea scale.31 COPD-specific HRQOL was retained to respect the intention-to-treat analysis (fig 1). There
evaluated by means of a validated version of the St. George’s was no difference between groups with regard to baseline
Respiratory Questionnaire (SGRQ).32,33 The 6-minute walk values of disease severity, functional capacity, anthropometric
test (6MWT) was used to assess exercise tolerance and per- data, or other baseline characteristics (table 1).
formed according to American Thoracic Society recommenda-
34 Thoracoabdominal and Diaphragmatic Mobilities
tions. The largest distance from 2 tests was used in the
analysis, and the normal values used were those described by Immediately after the 4-week DBTP, the TG showed a
35
Iwama et al. The body mass index, airflow obstruction, greater abdominal motion during NB quantified by a reduction
dyspnea, and exercise capacity values were integrated into a in the RC/ABD ratio when compared with the CG (F8.66;
36
score—the BODE index. P.001). Abdominal motion during voluntary DB after the
Statistical Analysis intervention was also greater in the TG than in the CG
(F4.11; P.05) (fig 2). DB competency was observed in all
Samplesizewascalculated using the results from the first 10 TG patients. Finally, the TG showed a greater diaphragmatic
patients enrolled in our study for the primary outcome. A mobility after the 4-week DBTP than did the CG (F15.08;
sample of 15 patients per group, for an alpha value of .05 and P.001) (fig 3). Effect sizes were medium to large in favor of
a power of 0.8, would allow for the detection of a reduction in the TG on the diaphragmatic mobility (d.46) and RC/ABD
the RC/ABD ratio during NB of up to .14 with an SD of .18 in ratio during both voluntary DB (d–.69) and NB (d–96).
the TG compared with the CG. An intention-to-treat approach The RC/ABD ratio and diaphragmatic mobility remained un-
with baseline values carried forward for any patient lost to changed in CG patients.
follow-up was used for all analyses.37 A per-protocol analysis
was also performed as a sensitivity analysis. An independent t Functional Capacity
test was used to compare baseline values between groups, and Dyspnea was lower in the TG after the 4-week DBTP
a chi-square test was applied to evaluate sex. Analysis of compared with the CG (F5.1; P.05) (table 2). An improve-
covariance was used to test for intervention group differ- ment in HRQOL for the TG was observed by a 10-point
ences with the baseline measure as the covariate. Effect reduction in the total SGRQ score (F9.7; P.001) (see table
sizes between the groups were calculated using the Cohen 2). The benefits in different SGRQ domains (symptom and
38 An effect size of .20 was considered small, .50
method. impact) for the TG were statistically significant compared with
medium,and.80large.Alinearrelationshipwasevaluatedby the CG, and they were also clinically relevant (reduction 4in
a Pearson correlation test. The level of significance used for the score) (fig 4). However, no change in the TG was observed
all tests was 5%. Data are presented as means (95% confi- for the activity domain. Finally, after the 4-week follow-up
dence interval). All analyses were performed using SPSS period, the TG showed a better performance in the 6MWT
d
version19.0. compared with the CG (F4.9; P.05) (see table 2). Effect
RESULTS sizes were small to medium in favor of the TG on the 6MWT
(d.31), dyspnea (d–.41), and HRQOL (d–.64). Spirome-
Ninety-four patients were assessed for eligibility, and 30 try values and lung volume data remained unchanged in both
patients were randomly assigned to groups. There were 3 groups (table 3). The statistical analysis performed when the 3
Fig 1. Study flow diagram.
Arch Phys Med Rehabil Vol 93, April 2012
574 DIAPHRAGMATIC BREATHING IN CHRONIC OBSTRUCTIVE PULMONARY DISEASE, Yamaguti
Table 1: Baseline Characteristics of the Studied Patients
Characteristics CG(n15) TG(n15) P
Anthropometric data
Sex (W/M) 4/11 4/11 1.00
Age (y) 66.4 (54.2–77.6) 66.5 (54.2–78.2) .97
BMI (kg/m2
) 27.2 (22.1–32.2) 27.5 (19.0–35.0) .87
Pulmonary function
GOLDclass (I, II, III,
and IV) (n) 0/4/7/4 0/3/8/4 NA
FEV1 (% predicted) 42.4 (18.2–74.8) 43.4 (24.0–63.0) .87
TLC (% predicted) 116.2(82.4–138.8) 122.4 (102.2–157.4) .36
DLCO (% predicted) 50.8 (12.8–102.0) 44.1 (19.0–87.5) .44
MVV(%predicted) 37.0 (16.6–74.4) 36.1 (18.5–60) .88
Thoracoabdominal
motion
DM(mm) 33.9 (20.8–51.6) 32.5 (25.5–58.6) .44
RC/ABD ratio 0.57 (0.37–0.95) 0.65 (0.25–0.89) .21
Functional capacity
6MWD(%predicted) 67.7 (32.9–94.2) 68.74(35.0–90.0) .87 Fig 3. Diaphragmatic mobility in patients with COPD after the
SGRQtotal score 54.0 (25.9–84.6) 53.6 (23.9–77.5) .96 4-week follow-up period in the CG and TG. The dotted line repre-
sents the threshold for diaphragmatic dysfunction.10 Circles repre-
BODEindex score 4.4 (0.2–7.0) 4.3 (2.0–7.5) .83 sent the mean, and whiskers represent 95% confidence intervals.
NOTE. Values are presented as mean (95% confidence interval) or *P<.001 compared with baseline.
number of subjects (sex and GOLD class).
Abbreviations: BMI, body mass index; BODE index, body mass in-
dex, degree of airflow obstruction and dyspnea, and exercise capac- (r–0.8; P.001) and baseline diaphragmatic mobility
ity index; DL , diffusing capacity of the lung for carbon monoxide;
CO (r.58; P.02) (fig 5). The bottom right area in figure 5A
DM, diaphragmatic mobility; GOLD, Global Initiative for Chronic reveals that most patients who improved their abdominal mo-
Obstructive Lung Disease; M, men; MVV, maximal voluntary venti- tion had a baseline predominance of costal breathing (RC/ABD
lation; NA, not applicable; 6MWD, 6-minute walk distance; TLC, total
lung capacity; W, women. ratio 0.5). Figure 5B reveals that patients with a lower
baseline diaphragmatic mobility demonstrated a higher im-
CG dropouts were excluded (per-protocol analysis) showed provement in abdominal motion after DBTP. Changes in ab-
results similar to those of the intention-to-treat analysis for all dominal motion did not correlate with any other baseline out-
outcomes (data not shown). comes in the TG. The RC/ABD ratio after a 4-week
follow-up period was not related to the baseline RC/ABD ratio
Linear Relationship Between the Improvement in or baseline diaphragmatic mobility in the CG (P.05).
Abdominal Motion and Baseline Characteristics DISCUSSION
Improvement in abdominal motion ( RC/ABD ratio) after This RCT was designed to investigate the isolated effects of
DBTP was inversely related to the baseline RC/ABD ratio a short-term DBTP in patients with COPD. It demonstrated an
improvement in abdominal motion during both NB and volun-
tary DB, as well as an increase in diaphragmatic mobility. We
also observed that DBTP leads to benefits in dyspnea symp-
toms, HRQOL, and exercise tolerance. These results support
the hypothesis that DBTP can induce a modification in habitual
breathing patterns and increase diaphragmatic excursion,
thereby relieving symptoms and improving the functional ca-
pacity of patients with COPD.
Our results demonstrate that during voluntary DB, patients
were able to increase abdominal motion, which is consistent
with previous findings.17,22 In addition, we also showed that
patients with COPD who completed DBTP demonstrated an
increase in abdominal motion during NB. However, Gosselink
et al22 did not report permanent changes in abdominal motion
after the diaphragmatic learning period, suggesting that DB
patterns may not be adopted naturally. Our study includes some
methodological differences that might elucidate the discor-
danceinresults between our study and Gosselink’s study. First,
our training program was longer (12 sessions vs 9 sessions).
Second, in their study, DB was performed only in the supine
and sitting positions, while in our program, DB was also
performed in the lateral decubitus and standing positions.
Fig 2. The RC/ABD ratio during NB and voluntary DB at baseline Third, our patients had less airflow obstruction compared with
andafter a 4-week follow-up period in the CG and TG. Reduction in those studied by Gosselink (43% vs 34% FEV ). Finally, all
the RC/ABD ratio reflects improvements in abdominal motion. Ab- 1
breviation: NS, not significant (compared with CG). *P<.05 com- our patients were considered competent to perform DB after
pared with CG for both conditions (NB and DB). the intervention, whereas no description of DB competency
Arch Phys Med Rehabil Vol 93, April 2012
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