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Diaphragmatic Breathing Training Program Improves Abdominal Motion During Natural Breathing in Patients With Chronic Obstructive Pulmonary Disease: A Randomized Controlled Trial

      Abstract

      Yamaguti WP, Claudino RC, Neto AP, Chammas MC, Gomes AC, Salge JM, Moriya HT, Cukier A, Carvalho CR. Diaphragmatic breathing training program improves abdominal motion during natural breathing in patients with chronic obstructive pulmonary disease: a randomized controlled trial.

      Objective

      To investigate the effects of a diaphragmatic breathing training program (DBTP) on thoracoabdominal motion and functional capacity in patients with chronic obstructive pulmonary disease.

      Design

      A prospective, randomized controlled trial.

      Setting

      Academic medical center.

      Participants

      Subjects (N=30; forced expiratory volume in 1s, 42%±13% predicted) were randomly allocated to either a training group (TG) or a control group (CG).

      Interventions

      Subjects in the TG completed a 4-week supervised DBTP (3 individualized weekly sessions), while those in the CG received their usual care.

      Main Outcome Measures

      Effectiveness was assessed by amplitude of the rib cage to abdominal motion ratio (RC/ABD ratio) (primary outcome) and diaphragmatic mobility (secondary outcome). The RC/ABD ratio was measured using respiratory inductive plethysmography during voluntary diaphragmatic breathing and natural breathing. Diaphragmatic mobility was measured by ultrasonography. A 6-minute walk test and health-related quality of life were also evaluated.

      Results

      Immediately after the 4-week DBTP, the TG showed a greater abdominal motion during natural breathing quantified by a reduction in the RC/ABD ratio when compared with the CG (F=8.66; P<.001). Abdominal motion during voluntary diaphragmatic breathing after the intervention was also greater in the TG than in the CG (F=4.11; P<.05). The TG showed greater diaphragmatic mobility after the 4-week DBTP than did the CG (F=15.08; P<.001). An improvement in the 6-minute walk test and in health-related quality of life was also observed in the TG.

      Conclusions

      DBTP for patients with chronic obstructive pulmonary disease induced increased diaphragm participation during natural breathing, resulting in an improvement in functional capacity.

      Key Words

      List of Abbreviations:

      CG (control group), COPD (chronic obstructive pulmonary disease), DB (diaphragmatic breathing), DBTP (diaphragmatic breathing training program), FEV1 (forced expiratory volume in 1 second), FVC (forced vital capacity), HRQOL (health-related quality of life), NB (natural breathing), RC/ABD ratio (amplitude of rib cage to abdominal motion ratio), RCT (randomized controlled trial), SGRQ (St. George's Respiratory Questionnaire), 6MWT (6-minute walk test), TG (training group)
      CHRONIC OBSTRUCTIVE PULMONARY disease (COPD) is characterized by an increased resistance to airflow, air trapping, and lung hyperinflation. As lung volume increases, the inspiratory muscles are passively shortened and thereby placed at a mechanical disadvantage.
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      Effect of hyperinflation on the diaphragm.
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      Hyperinflation and respiratory muscle interaction.
      Therefore, patients with COPD frequently have a reduction of diaphragmatic mobility and its relative contribution to thoracoabdominal motion,
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      Impaired respiratory mechanics in pulmonary emphysema: evaluation with dynamic breathing MRI.
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      Air trapping: the major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients.
      enhancing the activity of chest wall respiratory muscles as a compensatory mechanism.
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      Factors influencing ventilatory muscle recruitment in patients with chronic airflow obstruction.
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      Inspiratory muscular activation during threshold therapy in elderly healthy and patients with COPD.
      It has been previously shown that both a reduction in diaphragmatic mobility and a higher activity of chest wall respiratory muscles are associated with increased dyspnea and exercise intolerance.
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      Influence of diaphragmatic mobility on exercise tolerance and dyspnea in patients with COPD.
      Breathing strategies have been considered as part of self-management education actions in pulmonary rehabilitation
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      American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation.
      and include a range of techniques, including diaphragmatic breathing (DB). The principal aim of DB is to improve abdominal motion while reducing chest wall respiratory muscle activity.
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      Evidence underlying breathing retraining in people with stable chronic obstructive pulmonary disease.
      A systematic review
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      Efficacy of diaphragmatic breathing in persons with chronic obstructive pulmonary disease: a review of the literature.
      has pointed out some methodological problems in prior studies evaluating the benefits of DB for patients with COPD. Of 24 clinical investigations included in this review, only 3 were categorized as randomized controlled trials (RCTs).
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      An assessment of the value of breathing exercises in chronic bronchitis and asthma.
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      Adjunct treatment with yoga in chronic severe airways obstruction.
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      A study of short-term effect of rehabilitative therapy in chronic obstructive pulmonary disease.
      One of these studies included patients with asthma and bronchiectasis in addition to COPD, and the other investigations provided adjunctive therapies in addition to DB, which makes it difficult to determine the specific effects of DB for patients with COPD. Furthermore, the review demonstrated that the role of DB for patients with COPD remains controversial. Results from uncontrolled studies have demonstrated that DB might improve gas exchange,
      • Vitacca M.
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      Acute effects of deep diaphragmatic breathing in COPD patients with chronic respiratory insufficiency.
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      respiratory patterns,
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      and the oxygen cost of breathing.
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      Comparison of the oxygen cost of breathing exercises and spontaneous breathing in patients with stable chronic obstructive pulmonary disease.
      On the other hand, other investigators have suggested that DB may lead to detrimental effects in a specific population of patients with severe COPD.
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      • Ambrosino N.
      Acute effects of deep diaphragmatic breathing in COPD patients with chronic respiratory insufficiency.
      • Gosselink R.A.
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      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      Despite these conflicting results, an improvement in abdominal motion and a reduction in thoracic excursion during voluntary DB have been described as common findings in several studies.
      • Vitacca M.
      • Clini E.
      • Bianchi L.
      • Ambrosino N.
      Acute effects of deep diaphragmatic breathing in COPD patients with chronic respiratory insufficiency.
      • Sackner M.A.
      • Gonzalez H.F.
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      • Rodriguez M.
      Effects of abdominal and thoracic breathing on breathing pattern components in normal subjects and in patients with chronic obstructive pulmonary disease.
      • Gosselink R.A.
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      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      • Grimby G.
      • Oxhoj H.
      • Bake B.
      Effects of abdominal breathing on distribution of ventilation in obstructive lung disease.
      To our knowledge, no controlled studies have investigated the change in abdominal motion naturally adopted after a diaphragmatic breathing training program (DBTP). We hypothesized that a short-term DBTP could induce higher participation of the diaphragm during natural breathing (NB). This modification in habitual breathing pattern would relieve respiratory symptoms and improve exercise tolerance and health-related quality of life (HRQOL). Therefore, in this RCT, we aimed to test the effects of a short-term DBTP on thoracoabdominal motion, diaphragmatic mobility, and functional capacity in patients with COPD.

      Methods

      Participants

      Ninety-four patients with COPD diagnosed according to the Global Initiative for Chronic Obstructive Lung Disease criteria
      • Rabe K.F.
      • Hurd S.
      • Anzueto A.
      • et al.
      Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary.
      were recruited at a university hospital. Inclusion criteria were as follows: (1) age 50 to 80 years; (2) postbronchodilator forced expiratory volume in 1 second (FEV1) <80% of predicted and an FEV1 to forced vital capacity (FVC) ratio (FEV1/FVC ratio) <0.7; (3) stable respiratory condition without changes in medication or symptoms for at least 4 weeks before enrollment in the study; and (4) receiving regular treatment with inhaled bronchodilators and steroids. Exclusion criteria were (1) the presence of other cardiopulmonary or musculoskeletal diseases; (2) previous engagement in any exercise training program in the prior 2 years; and (3) current smokers. The hospital ethics committee approved the study (Protocol no. 0348/08), and all patients provided written informed consent.

      Study Design

      This was a prospective, parallel-group, randomized and blinded clinical trial. Patients were evenly allocated (1:1) to either a training group (TG) or control group (CG). Randomization was stratified according to sex using random block sizes of 2 and 4. Regular medical treatment was established in both groups before the first visit and remained unchanged throughout the study. Patients in the TG completed a 4-week DBTP, while those in the CG received their usual care. Patients in both groups were evaluated at baseline and at the end of a 4-week period. The technicians who collected data for all outcome measures (R.C.C. and A.C.G.) were blinded to the patients' group allocation.

      Training Program

      The TG completed a DBTP consisting of three 45-minute weekly sessions (12 sessions total). The program was individualized and supervised by a single physiotherapist (A.P.N.). In each session, the patients were instructed to perform a total of 150 breathing exercises in the following positions: supine, right and left lateral decubitus, sitting, and standing (3 series of 10 repetitions in each position). Between each series of DB exercises, patients were instructed to breathe normally for 1 minute. The following verbal instructions were given during inhalation and exhalation, respectively: “perform a slow maximal inspiration allowing the air to go to your belly,” and “perform a normal expiration without forcing abdominal retraction.” Tactile feedback was provided by positioning one of the patient's hands on the abdomen and the other hand on the upper rib cage. If necessary, visual and auditory stimulation was provided to correct uncoordinated respiratory patterns. DB competency was considered if the respiratory pattern adopted was associated with at least a doubling of the abdominal tidal excursion observed during NB.
      • Cahalin L.P.
      • Braga M.
      • Matsuo Y.
      • Hernandez E.D.
      Efficacy of diaphragmatic breathing in persons with chronic obstructive pulmonary disease: a review of the literature.
      • Gosselink R.A.
      • Wagenaar R.C.
      • Rijswijk H.
      • Sargeant A.J.
      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      No patient in the CG or TG was instructed to perform the exercises at home.

      Outcome Measures

      Primary and secondary outcomes

      Improvements in abdominal motion during NB and in diaphragmatic mobility, from baseline to post-DBTP, were used, respectively, as primary and secondary outcomes. Patients from the CG and TG were instructed to practice voluntary DB before the first evaluation of thoracoabdominal motion. This procedure aimed at evaluating whether a single instruction session was as effective to change abdominal motion during NB as a supervised DBTP. Dyspnea, HRQOL, and exercise tolerance were also evaluated.

      Thoracoabdominal motion

      Improvement in abdominal motion was evaluated by means of a reduction in the amplitude of the rib cage to abdominal motion ratio (RC/ABD ratio) recorded using a computer-assisted respiratory inductive plethysmography system (Respitrace).a Teflon-coated inductance bandsa of appropriate size were placed around the rib cage and abdomen and connected to an oscillator module and calibration unit.
      • Tobin M.J.
      • Jenouri G.
      • Lind B.
      • Watson H.
      • Schneider A.
      • Sackner M.A.
      Validation of respiratory inductive plethysmography in patients with pulmonary disease.
      Each subject was measured in a quiet, private room, and data acquisition was performed in a supine position
      • Bloch K.E.
      • Li Y.
      • Zhang J.
      • et al.
      Effect of surgical lung volume reduction on breathing patterns in severe pulmonary emphysema.
      for a total period of 9 minutes, equally distributed as follows: (1) at rest—basal NB; (2) during DB exercise—voluntary DB; and (3) post-DB exercise. Pulse oximetry was continuously monitored, and dyspnea sensations were evaluated every minute using the modified Borg scale.
      • Borg G.A.V.
      Psychophysical bases of perceived exertion.
      Rib cage and abdominal wall movement waveforms were digitized, and the RC/ABD ratio was calculated from the absolute changes in the circumference of these compartments.
      • Gosselink R.A.
      • Wagenaar R.C.
      • Rijswijk H.
      • Sargeant A.J.
      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.

      Diaphragmatic mobility

      An ultrasonography examination was used to assess the craniocaudal displacement of the left branch of the portal vein in order to measure diaphragmatic mobility.
      • Toledo N.S.
      • Kodaira S.K.
      • Massarollo P.C.
      • Pereira O.I.
      • Mies S.
      Right hemidiaphragmatic mobility: assessment with US measurement of craniocaudal displacement of left branches of portal vein.
      Patients were evaluated in the supine position using an ultrasound scannerb in B-mode. A 3.5-MHz convex transducer was positioned over the right subcostal region, and the position of the left branch of the portal vein was marked with the cursor during forced expiration and inspiration. Three reproducible measurements were performed, and the best value was used for the analysis.

      Functional capacity

      Spirometry and whole-body plethysmography were performed using standard equipmentc according to the American Thoracic Society and the European Respiratory Society recommendations.
      • Miller M.R.
      • Hankinson J.
      • Brusasco V.
      • et al.
      Standardisation of spirometry.
      Reported spirometry results were based on the best curve from 3 acceptable efforts (after the inhalation of 200μg of salbutamol); they are presented as a percentage of the predicted value.
      • Pereira C.A.
      • Sato T.
      • Rodrigues S.C.
      New reference values for forced spirometry in white adults in Brazil.
      Dyspnea symptoms at rest were assessed using the modified Medical Research Council dyspnea scale.
      • Mahler D.A.
      • Wells C.K.
      Evaluation of clinical methods for rating dyspnea.
      COPD-specific HRQOL was evaluated by means of a validated version of the St. George's Respiratory Questionnaire (SGRQ).
      • Jones P.W.
      • Quirk F.H.
      • Baveystock C.M.
      • Littlejohns P.
      A self-complete measure of health status for chronic airflow limitation The St. George's Respiratory Questionnaire.
      • Sousa T.C.
      • Jardim J.R.
      • Jones P.
      Validation of the Saint George′s Respiratory Questionnaire in patients with chronic obstructive pulmonary disease in Brazil.
      The 6-minute walk test (6MWT) was used to assess exercise tolerance and performed according to American Thoracic Society recommendations.
      ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories
      ATS statement: guidelines for the six-minute walk test.
      The largest distance from 2 tests was used in the analysis, and the normal values used were those described by Iwama et al.
      • Iwama A.M.
      • Andrade G.N.
      • Shima P.
      • Tanni S.E.
      • Godoy I.
      • Dourado V.Z.
      The six-minute walk test and body weight-walk distance product in healthy Brazilian subjects.
      The body mass index, airflow obstruction, dyspnea, and exercise capacity values were integrated into a score—the BODE index.
      • Celli B.R.
      • Cote C.G.
      • Marin J.M.
      • et al.
      The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease.

      Statistical Analysis

      Sample size was calculated using the results from the first 10 patients enrolled in our study for the primary outcome. A sample of 15 patients per group, for an alpha value of .05 and a power of 0.8, would allow for the detection of a reduction in the RC/ABD ratio during NB of up to .14 with an SD of .18 in the TG compared with the CG. An intention-to-treat approach with baseline values carried forward for any patient lost to follow-up was used for all analyses.
      • Moher D.
      • Hopewell S.
      • Schulz K.F.
      • et al.
      CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials.
      A per-protocol analysis was also performed as a sensitivity analysis. An independent t test was used to compare baseline values between groups, and a chi-square test was applied to evaluate sex. Analysis of covariance was used to test for intervention group differences with the baseline measure as the covariate. Effect sizes between the groups were calculated using the Cohen method.
      • Cohen J.
      Statistical power analysis for the behavioral sciences.
      An effect size of .20 was considered small, .50 medium, and .80 large. A linear relationship was evaluated by a Pearson correlation test. The level of significance used for all tests was 5%. Data are presented as means (95% confidence interval). All analyses were performed using SPSS version19.0.d

      Results

      Ninety-four patients were assessed for eligibility, and 30 patients were randomly assigned to groups. There were 3 protocol deviations in the CG because of either an acute COPD exacerbation or other health problems. These patients were retained to respect the intention-to-treat analysis (fig 1) . There was no difference between groups with regard to baseline values of disease severity, functional capacity, anthropometric data, or other baseline characteristics (table 1).
      Table 1Baseline Characteristics of the Studied Patients
      CharacteristicsCG (n=15)TG (n=15)P
      Anthropometric data
       Sex (W/M)4/114/111.00
       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
       GOLD class (I, II, III, and IV) (n)0/4/7/40/3/8/4NA
       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 ratio0.57 (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
       SGRQ total score54.0 (25.9–84.6)53.6 (23.9–77.5).96
       BODE index score4.4 (0.2–7.0)4.3 (2.0–7.5).83
      NOTE. Values are presented as mean (95% confidence interval) or number of subjects (sex and GOLD class).
      Abbreviations: BMI, body mass index; BODE index, body mass index, degree of airflow obstruction and dyspnea, and exercise capacity index; DLCO, diffusing capacity of the lung for carbon monoxide; DM, diaphragmatic mobility; GOLD, Global Initiative for Chronic Obstructive Lung Disease; M, men; MVV, maximal voluntary ventilation; NA, not applicable; 6MWD, 6-minute walk distance; TLC, total lung capacity; W, women.

      Thoracoabdominal and Diaphragmatic Mobilities

      Immediately after the 4-week DBTP, the TG showed a greater abdominal motion during NB quantified by a reduction in the RC/ABD ratio when compared with the CG (F=8.66; P<.001). Abdominal motion during voluntary DB after the intervention was also greater in the TG than in the CG (F=4.11; P<.05) (fig 2) . DB competency was observed in all TG patients. Finally, the TG showed a greater diaphragmatic mobility after the 4-week DBTP than did the CG (F=15.08; P<.001) (fig 3) . Effect sizes were medium to large in favor of the TG on the diaphragmatic mobility (d=.46) and RC/ABD ratio during both voluntary DB (d=–.69) and NB (d=–96). The RC/ABD ratio and diaphragmatic mobility remained unchanged in CG patients.
      Figure thumbnail gr2
      Fig 2The RC/ABD ratio during NB and voluntary DB at baseline and after a 4-week follow-up period in the CG and TG. Reduction in the RC/ABD ratio reflects improvements in abdominal motion. Abbreviation: NS, not significant (compared with CG). *P<.05 compared with CG for both conditions (NB and DB).
      Figure thumbnail gr3
      Fig 3Diaphragmatic mobility in patients with COPD after the 4-week follow-up period in the CG and TG. The dotted line represents the threshold for diaphragmatic dysfunction.
      • Paulin E.
      • Yamaguti W.P.
      • Chammas M.C.
      • et al.
      Influence of diaphragmatic mobility on exercise tolerance and dyspnea in patients with COPD.
      Circles represent the mean, and whiskers represent 95% confidence intervals. *P<.001 compared with baseline.

      Functional Capacity

      Dyspnea was lower in the TG after the 4-week DBTP compared with the CG (F=5.1; P<.05) (table 2). An improvement in HRQOL for the TG was observed by a 10-point reduction in the total SGRQ score (F=9.7; P<.001) (see table 2). The benefits in different SGRQ domains (symptom and impact) for the TG were statistically significant compared with the CG, and they were also clinically relevant (reduction >4 in the score) (fig 4) . However, no change in the TG was observed for the activity domain. Finally, after the 4-week follow-up period, the TG showed a better performance in the 6MWT compared with the CG (F=4.9; P<.05) (see table 2). Effect sizes were small to medium in favor of the TG on the 6MWT (d=.31), dyspnea (d=–.41), and HRQOL (d=–.64). Spirometry values and lung volume data remained unchanged in both groups (table 3). The statistical analysis performed when the 3 CG dropouts were excluded (per-protocol analysis) showed results similar to those of the intention-to-treat analysis for all outcomes (data not shown).
      Table 2Functional Capacity of Patients With COPD Before and After the 4-Week Follow-up in the CG and TG
      OutcomesGroupBeforeAfterANCOVA
      FPEffect Size (TG vs CG)
      MMRC dyspnea scale scoreCG2.8 (1.0–4.0)2.5 (1.0–4.0)
      TG2.6 (0.25–4.0)2.0 (0.25–3.75)5.1.03
      P<.05 TG vs CG after intervention (group effect).
      –.41
      SGRQ total scoreCG54.0 (25.9–84.6)54.8 (26.1–74.9)
      TG53.6 (23.9–77.5)43.9 (19.0–72.1)9.7.004
      P<.05 TG vs CG after intervention (group effect).
      −.64
      BODE index scoreCG4.4 (0.2–7.0)4.1 (0.2–7.6)
      TG4.3 (2–7.5)3.6 (1.25–6.75)0.94.34−.20
      6MWD (m)CG375.7 (179.5–531.5)367.3 (168.0–499.0)
      TG371.2 (190.5–499.5)397.5 (248.5–539.0)4.9.03
      P<.05 TG vs CG after intervention (group effect).
      .31
      NOTE. Values are mean (95% confidence interval) or as otherwise indicated. Lower values were considered as an improvement for the MMRC dyspnea scale score, SGRQ score, and BODE index. Statistical analysis was performed using ANCOVA.
      Abbreviations: ANCOVA, analysis of covariance; BODE index, body mass index, degree of airflow obstruction and dyspnea, and exercise capacity index; MMRC, modified Medical Research Council; 6MWD, 6-minute walk distance.
      low asterisk P<.05 TG vs CG after intervention (group effect).
      Figure thumbnail gr4
      Fig 4Changes in SGRQ scores in patients with COPD after the 4-week follow-up in the CG and TG (negative difference is interpreted as an improvement). A difference >4.0 (deterioration) and <−4.0 (improvement) is considered clinically important. The dotted line indicates the minimal clinically important difference for SGRQ scores.
      • Jones P.W.
      Interpreting thresholds for a clinically significant change in health status in asthma and COPD.
      Circles represent the mean, and whiskers represent 95% confidence intervals. Abbreviations: A, activity; I, impact; NS, not significant (compared with CG); S, symptom; Total, SGRQ total score. *P<.05 compared with CG.
      Table 3Pulmonary Function of Patients With COPD Before and After the 4-Week Follow-up in the CG and TG
      OutcomesGroupBeforeAfterANCOVA
      FP
       FEV1 (% predicted)CG42.4 (18.2–74.8)42.7 (22.0–74.4)0.28.60
      TG43.4 (24.0–63.0)42.7 (22.25–66.25)
       FVC (% predicted)CG79.3 (49.8–113.8)78.4 (57.8–113.8)0.21.65
      TG80.6 (61.2–94.7)81.1 (61.5–111.0)
       FEV1/FVC (%)CG39.9 (22.2–64.4)40.8 (23.0–70.0)1.86.18
      TG40.3 (26.0–58.7)39.3 (26.5–56.0)
       MVV (% predicted)CG37.0 (16.6–74.4)38.0 (18.3–74.4)0.66.42
      TG36.1 (18.5–60.0)36.7 (18.5–58.0)
       RV (% predicted)CG194.8 (87.4–259.0)187.9 (89.9–259.0)0.62.43
      TG196.6 (131.2–285.5)195.6 (131.7–279.5)
       TLC (% predicted)CG116.2 (82.4–138.8)114.5 (83.3–137.9)0.06.79
      TG123.2 (102.2–157.4)119.1 (97.0–151.0)
      NOTE. Values are mean (95% confidence interval) or as otherwise indicated. Statistical analysis was performed using ANCOVA.
      Abbreviations: ANCOVA, analysis of covariance; MVV, maximal voluntary ventilation; RV, residual volume; TLC, total lung capacity.

      Linear Relationship Between the Improvement in Abdominal Motion and Baseline Characteristics

      Improvement in abdominal motion (Δ RC/ABD ratio) after DBTP was inversely related to the baseline RC/ABD ratio (r=–0.8; P<.001) and baseline diaphragmatic mobility (r=.58; P=.02) (fig 5) . The bottom right area in figure 5A reveals that most patients who improved their abdominal motion had a baseline predominance of costal breathing (RC/ABD ratio >0.5). Figure 5B reveals that patients with a lower baseline diaphragmatic mobility demonstrated a higher improvement in abdominal motion after DBTP. Changes in abdominal motion did not correlate with any other baseline outcomes in the TG. The Δ RC/ABD ratio after a 4-week follow-up period was not related to the baseline RC/ABD ratio or baseline diaphragmatic mobility in the CG (P>.05).
      Figure thumbnail gr5
      Fig 5Linear relationship between baseline RC/ABD ratio (A), baseline diaphragmatic mobility (B), and the improvement in abdominal motion (Δ RC/ABD ratio) during NB in patients that completed DBTP. Negative changes in the RC/ABD ratio reflect improvement in abdominal motion. In A, the points included in the bottom right area correspond to patients who improved their abdominal motion. Note that 92.9% of the patients who showed an improvement in abdominal motion after DBTP had a baseline predominance of costal breathing. Abbreviation: DM, diaphragmatic mobility.

      Discussion

      This RCT was designed to investigate the isolated effects of a short-term DBTP in patients with COPD. It demonstrated an improvement in abdominal motion during both NB and voluntary DB, as well as an increase in diaphragmatic mobility. We also observed that DBTP leads to benefits in dyspnea symptoms, 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 capacity of patients with COPD.
      Our results demonstrate that during voluntary DB, patients were able to increase abdominal motion, which is consistent with previous findings.
      • Vitacca M.
      • Clini E.
      • Bianchi L.
      • Ambrosino N.
      Acute effects of deep diaphragmatic breathing in COPD patients with chronic respiratory insufficiency.
      • Gosselink R.A.
      • Wagenaar R.C.
      • Rijswijk H.
      • Sargeant A.J.
      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      In addition, we also showed that patients with COPD who completed DBTP demonstrated an increase in abdominal motion during NB. However, Gosselink et al
      • Gosselink R.A.
      • Wagenaar R.C.
      • Rijswijk H.
      • Sargeant A.J.
      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      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 discordance in results 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. Third, our patients had less airflow obstruction compared with those studied by Gosselink (43% vs 34% FEV1). Finally, all our patients were considered competent to perform DB after the intervention, whereas no description of DB competency was provided in the other study.
      • Gosselink R.A.
      • Wagenaar R.C.
      • Rijswijk H.
      • Sargeant A.J.
      • Decramer M.L.
      Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive pulmonary disease.
      All those differences between the studies could explain the benefit observed in our patients.
      Diaphragmatic dysfunction is an important consequence of respiratory alterations in patients with COPD.
      • Dos Santos Yamaguti W.P.
      • Paulin E.
      • Shibao S.
      • et al.
      Air trapping: the major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients.
      We have previously reported that patients with reduced diaphragmatic mobility (≤33.99mm) have a lower exercise tolerance and increased dyspnea after physical effort.
      • Paulin E.
      • Yamaguti W.P.
      • Chammas M.C.
      • et al.
      Influence of diaphragmatic mobility on exercise tolerance and dyspnea in patients with COPD.
      In the present study, patients from both groups had an impairment of diaphragmatic mobility at baseline, evidenced by a lower excursion than the critical point for diaphragmatic dysfunction (≤33.99mm), and only patients who participated in DBTP showed improvement in diaphragmatic mobility beyond the point of impairment. Based on these findings, the increase in diaphragmatic mobility is expected to improve dyspnea symptoms and functional capacity.
      It has been demonstrated that both increased activity of chest wall respiratory muscles and the impairment of diaphragm activity are associated with higher sensations of dyspnea.
      • Ward M.E.
      • Eidelman D.
      • Stubbing D.G.
      • Bellemare F.
      • Macklem P.T.
      Respiratory sensation and pattern of respiratory muscle activation during diaphragm fatigue.
      • Breslin E.H.
      • Garoutte B.C.
      • Kohlman-Carrieri V.
      • Celli B.R.
      Correlations between dyspnea, diaphragm and sternomastoid recruitment during inspiratory resistance breathing in normal subjects.
      This suggests that interventions aimed at reversing the extensive use of chest wall respiratory muscles and enhancing diaphragmatic function might alleviate dyspnea in patients with COPD.
      • O'Neill S.
      • McArthy D.S.
      Postural relief of dyspnoea in severe chronic airflow limitation: relationship to respiratory muscle strength.
      • Easton P.A.
      • Hawes H.G.
      • Doig C.J.
      • Johnson M.W.
      • Yokoba M.
      • Wilde E.R.
      Parasternal muscle activity decreases in severe COPD with salmeterol-fluticasone propionate.
      Our results reveal that patients who participated in DBTP had higher abdominal motion during NB and higher diaphragmatic mobility after the training, as well as a reduction in dyspnea symptoms. Based on these findings, we can speculate that the reduction in dyspnea could be at least partially explained by a higher participation of the diaphragm and a lower activity of chest wall respiratory muscles.
      We also observed an improvement in HRQOL only in patients who completed DBTP. Interestingly, the benefits in SGRQ scores (total, symptoms, and impact) were statistically and clinically (changes >4 units) significant.
      • Jones P.W.
      Interpreting thresholds for a clinically significant change in health status in asthma and COPD.
      Unfortunately, we are not aware of any other trials that have investigated the benefits of DBTP on HRQOL for patients with COPD, which makes it difficult to compare our results. Finally, patients who participated in DBTP showed improvements in a 6MWT. Recent studies
      • Holland A.E.
      • Hill C.J.
      • Rasekaba T.
      • Lee A.
      • Naughton M.T.
      • McDonald C.F.
      Updating the minimal important difference for six-minute walk distance in patients with chronic obstructive pulmonary disease.
      • Puhan M.A.
      • Chandra D.
      • Mosenifar Z.
      • et al.
      The minimal important difference of exercise tests in severe COPD.
      have demonstrated that the minimal important difference for a 6MWT in patients with COPD is approximately 26m. The improvement of 26.3m observed in our study suggests that DBTP could be recommended as an adjunctive strategy to improve exercise tolerance in patients with COPD.
      Our results revealed that patients who started the program with lower diaphragmatic mobility and a predominance of costal breathing showed a greater improvement in abdominal motion. These results suggest that patients with a higher impairment of diaphragmatic function and a higher activity of chest wall respiratory muscles would experience greater benefits from DBTP and should be preferentially selected to participate in these programs.
      The new contribution of our study lies in the fact that DBTP not only improves respiratory mechanics at NB but also impacts functional outcomes. Furthermore, this strategy is feasible, inexpensive, and promising for application in group therapy and home-based pulmonary rehabilitation. However, further studies must be designed to test these applications of DB.

      Study Limitations

      The present study has some limitations. First, we did not evaluate the long-term benefits of DBTP, and it remains unknown for how long patients will continue to have higher participation of the abdomen during NB. Second, patients in the CG did not undergo a sham treatment and received only usual care; however, this experimental design has been widely used to evaluate the effects of pulmonary rehabilitation programs.
      • Ries A.L.
      • Bauldoff G.S.
      • Carlin B.W.
      • et al.
      Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based clinical practice guidelines.
      Third, patients with missing outcomes were included in the analyses, with baseline values carried forward for any patient lost to follow-up. Although imputation of the missing data might enhance the likelihood of finding no reliable change in the CG, in our study both analyses (intention-to-treat and per-protocol) showed similar results. Fourth, the use of inductance bands could lead patients to change their breathing pattern; however, a greater diaphragmatic mobility in the TG was also confirmed using ultrasound. Despite these limitations, to our knowledge this is the first RCT investigating the clinical benefits of DBTP in patients with stable COPD.

      Conclusions

      We conclude that DBTP in patients with COPD leads to improvements in abdominal motion during NB and in functional capacity. We also showed that patients with a baseline level predominance of costal breathing and worse diaphragmatic mobility experienced a greater improvement in abdominal motion. These patients are probably stronger candidates for DB training. Therefore, this study underscores the importance of DB as an adjunctive treatment modality for patients with COPD.
      • a
        Ambulatory Monitoring Inc, 731 Saw Mill River Rd, Ardsley, NY 10502.
      • b
        Logiq 500, Pro Series; GE Medical Systems, 8200 West Tower Ave, Milwaukee, WI 53223.
      • c
        GS II; Collins, 908 Main, Braintree, MA 02184.
      • d
        SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

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