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571 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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