Professional Documents
Culture Documents
Systematic review of
the effectiveness of
breathing retraining in
asthma management
Expert Rev. Respir. Med. 5(6), 789–807 (2011)
John Burgess1, In asthma management, complementary and alternative medicine is enjoying a growing
Buddhini Ekanayake1, popularity worldwide. This review synthesizes the literature on complementary and alternative
Adrian Lowe1, medicine techniques that utilize breathing retraining as their primary component and compares
evidence from controlled trials with before-and-after trials. Medline, PubMed, Cumulative Index
David Dunt2,
to Nursing and Allied Health Literature and the Cochrane Library electronic databases were
Francis Thien3 and searched. Reference lists of all publications were manually checked to identify studies not found
Shyamali C Dharmage*1 through electronic searching. The selection criteria were met by 41 articles. Most randomized
1
Centre for Molecular, Environmental, controlled trials (RCTs) of the Buteyko breathing technique demonstrated a significant decrease
Analytic and Genetic Epidemiology, in b2-agonist use while several found improvement in quality of life or decrease in inhaled
Melbourne School of Population
Health, The University of Melbourne,
corticosteroid use. Although few in number, RCTs of respiratory muscle training found a
Victoria 3010, Australia significant reduction in bronchodilator medication use. Where meta-analyses could be done,
2
Centre for Health Program Evaluation, they provided evidence of benefit from yoga, Buteyko breathing technique and physiotherapist-
Melbourne School of Population
led breathing training in improving asthma-related quality of life. However, considerable
Health, The University of Melbourne,
Victoria 3010, Australia heterogeneity was noted in some RCTs of yoga. It is reasonable for clinicians to offer qualified
3
Department of Respiratory Medicine, support to patients with asthma undertaking these breathing retraining techniques.
Box Hill Hospital and Monash
University, Nelson Road, Box Hill, Keywords : asthma • Buteyko breathing technique • complementary medicine • respiratory muscle retraining
Victoria 3138, Australia
• systematic review
*Author for correspondence:
s.dharmage@unimelb.edu.au
Complementary and alternative medicine Buteyko theorized that hyperventilation was the
(CAM) has been defined as “a broad domain pathological basis of many diseases including
of healing resources that encompasses all asthma, suggesting that hypocapnia consequent
health systems, modalities and practices and to hyperventilation initiates bronchospasm, and
their accompanying theories and beliefs, other patented a formula based on breath-hold time
than those intrinsic to the politically dominant which, he claimed, predicted end-tidal CO2
health system of a particular society or culture [201] . BBT utilizes shallow, controlled breathing
in a given historical period” [1] . CAM is popular and respiratory pauses in an attempt to increase
in the general community for the self-manage- alveolar and arterial CO2 tension, which BBT
ment of asthma. Between 20–30% of adults proponents suggest may reverse bronchospasm.
and 50–60% of children have been identified Other breathing retraining techniques
in more rigorously designed studies as having forming part of CAM include���������������
yoga, biofeed-
used CAM for asthma yet approximately half back and respiratory muscle training. Yoga
of CAM users do not inform their general prac- techniques include deep-breathing exercises
titioner of their CAM use [2] . Breathing retrain- (pranayama), postures (asanas), mucus expec-
ing, a popular form of CAM, is the subject of toration (kriyas), meditation, prayer and often
this review. dietary changes to reduce asthma symptoms.
Prominent among breathing retraining thera- Biofeedback aims to reduce symptoms through
pies is the Buteyko breathing technique (BBT), gain of voluntary control over autonomic pro-
based on the work of Konstantin Buteyko [3] . cesses. Direct biofeedback training consists of
790
Study† (year) Sample Design Intervention Withdrawals Follow-up Difference between groups Ref.
(intervention vs control)
Review
Bowler et al. 39 community RCT 1-week training with 2 (1 intervention, 12 weeks ↓ MV: 3.6 l/min (p = 0.004) [12]
(1998) volunteers with True randomization Buteyko representative 1 control) ↓ b2-agonist: 847 µg/day (p = 0.002)
asthma Double blind versus relaxation and ↑ AQOL score (p trend = 0.09)
asthma education No between-group difference in PEF or FEV1
No change in ETCO2 in either group
Opat et al. 36 community RCT 4 weeks BBT training 8 4 weeks ↑ AQOL: -1.29 for total score (p = 0.043) [20]
(2000) volunteers with Sample size estimate video versus nature video ↓ b2-agonist: 210 µg /day (p = 0.008)
asthma True randomization
Thomas et al. 33 volunteers with RCT 2 weeks retraining with 5 (1 intervention, 1 and At 1 month: ↑ AQLQ total score‡ [22]
(2003) asthma/ Sample size estimate physiotherapist versus 4 control [3 at 6 months At 6 months: ↑AQLQ activities score‡
dysfunctional True randomization nurse-led asthma 6 months]) At 6 months: ↓ Nijmegen score‡
breathing education
Cooper et al. 89 community RCT 2 weeks BBT with 20 (7 intervention, 6 months ↓ symptom scores by two points (p = 0.003) [15]
(2003) volunteers with Sample size estimate certified practitioner 6 PCLE, 7 placebo) ↓ b2-agonist: two puffs/day (p = 0.005)
asthma True randomization veruss PCLE or placebo No between-group difference in FEV1, ICS
Double blind use, asthma exacerbations or AQLQ scores
McHugh et al. 38 community RCT 1-week BBT with Buteyko 4 6 weeks, ↓ b2-agonist 6 weeks; 38% between-group [16]
(2003) volunteers with Sample size estimate representative versus 3 months, difference§
asthma True randomization asthma education 6 months 3 months: 35% between-group difference§
Double blind ↓ ICS 6 weeks: 24% between-group
difference§
Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
www.expert-reviews.com
controlled asthma True randomization method) plus usual (p = 0.007)
recruited from treatment versus usual ↓ HAD anxiety score at 6 and 12 months:
semirural general treatment between-group difference 1.5 points
practice (p = 0.006)
↓ HAD depression score at 12 months:
between-group difference 0.5 points
(p = 0.03)
↓ NQ total score at 6 and 12 months:
between-group difference 2.3 points
(p = 0.015)
No between-group difference in lung
function at either follow-up
Meuret et al. 12 adults with RCT Capnometry-assisted None 8 weeks in In intervention group: [13]
(2007) asthma recruited Not clear whether breathing retraining plus intervention ↓ ACQ score (p < 0.05)
by advertisement truly randomized usual treatment versus group (n = 8) ↓ Steen asthma symptom score (p < 0.01)
usual treatment ↓ PEF variability (p < 0.05)
No change in FEV1
Cowie et al. 129 subjects from RCT Five sessions of BBT from 11 (9 intervention, 3 and At 6 months: [21]
(2008) university-based Sample size estimate accredited practitioner 2 control) 6 months ↑ in asthma control (79 vs 72% controlled)
asthma program True randomization versus five sessions of BT but no between-group difference (p = 0.4)
from physiotherapist ↑ MAQOLQ scores same in both groups
(0.96 vs 0.95)
↓ ICS use: 317 vs 56 µg/day (p = 0.02)
Thomas et al. 183 general RCT Physiotherapist- 14 BT and 8 1 and ↑ AQLQ total score: between-group [14]
(2009) practice asthma True randomization supervised BT versus control following 6 months difference 0.38 units at 6 months.
patients with nurse-led asthma randomization. ↓ NQ score, ↓ HAD anxiety and depression
moderate ↓ AQLQ education Further 7 BT and scores at 6 months
score 2 control did not (All between-group difference p ≤ 0.03)
attend 1-month No between-group difference in FEV1, MV or
follow-up ETCO2 at 1-month follow-up
†
Studies listed in order of year of publication.
‡
All p-values <0.02.
§
All p-values <0.04.
↑: Increase in ↓: Decrease in; ACT: Airway control test; AQLQ: Asthma Related Quality-of-Life Questionnaire; AQOL: Asthma-related quality of life; BBT: Buteyko breathing technique; BT: Breathing training;
Systematic review of the effectiveness of breathing retraining in asthma management
CCMAS: Chinese Children’s Manifest Anxiety Scale; ETCO2: End tidal carbon dioxide; FEV1: Forced expiratory volume in 1 s; GASCC: General Anxiety Scale for Chinese Children; HAD: Hospital Anxiety and
Depression Questionnaire; ICS: Inhaled corticosteroid; MAQOLQ: Mini Asthma Quality-of-Life questionnaire (Juniper); MV: Minute volume; NQ: Nijmegen questionnaire; PCLE: Pink City Lung Exerciser; PEF: Peak
expiratory flow; PEFR: Peak expiratory flow rate; RCT: Randomized controlled trial; SF-36v2 PC: Short Form-36 version 2 Health Survey physical component; SGRQ: St George Respiratory Questionnaire.
Review
791
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
[24]
‘rewards’ (visual or auditory signals) if the subject maintains a
[18]
Ref.
Depression Questionnaire; ICS: Inhaled corticosteroid; MAQOLQ: Mini Asthma Quality-of-Life questionnaire (Juniper); MV: Minute volume; NQ: Nijmegen questionnaire; PCLE: Pink City Lung Exerciser; PEF: Peak
Respiratory muscle training aims to strengthen muscles to meet
symptoms but no between-group differences
↑: Increase in ↓: Decrease in; ACT: Airway control test; AQLQ: Asthma Related Quality-of-Life Questionnaire; AQOL: Asthma-related quality of life; BBT: Buteyko breathing technique; BT: Breathing training;
CCMAS: Chinese Children’s Manifest Anxiety Scale; ETCO2: End tidal carbon dioxide; FEV1: Forced expiratory volume in 1 s; GASCC: General Anxiety Scale for Chinese Children; HAD: Hospital Anxiety and
the increased work of breathing in asthma.
expiratory flow; PEFR: Peak expiratory flow rate; RCT: Randomized controlled trial; SF-36v2 PC: Short Form-36 version 2 Health Survey physical component; SGRQ: St George Respiratory Questionnaire.
A Cochrane review updated in 2004 analyzed evidence for
ized controlled trials (RCTs) and only those with methods not
↓ overall asthma medication use
Difference between groups
6 months
11 (4 experimental 12 weeks
and 7 control)
from original
these techniques are less costly and have fewer unwanted side-
the study
Physiotherapist-led BT
plus usual treatment
Breathing/relaxation
Study design
Intervention
Search strategy
Medline, PubMed, Embase, Cumulative Index to Nursing and
Sample size estimate
True randomization
Not clear whether
RCT
asthma from a
hospital clinic
Inclusion criteria
All peer-reviewed journal articles related to the use of breathing
Sample
Chiang et al.
et al. (2011)
www.expert-reviews.com
(1985) yoga clinic truly randomized usual management versus not stated) ↑ PEF
usual management All between-group comparisons: p < 0.01
Singh et al. 22 adults RCT (case-crossover) 2 weeks PCLE (I:E 1:2) 4 2 weeks ↑ histamine PD20 : 0.96 mg (p = 0.013) [29]
(1990) Not clear whether 2 weeks PCLE placebo 4 weeks No significant change in lung function
truly randomized or device
double-blind
Ceugniet 27 males with RCT Exercise training – three 3 from ‘no Immediate No between-group difference in FEV1/FVC [26]
et al. severe asthma Not clear whether groups: I:E 1:1 versus I:E instructions’ Trend for lesser fall in FEV1 with exercise in I:E
(1994) age <19 years truly randomized 1:3 versus no instructions group 1:1 and 1:3 groups (p = 0.041)
Ceugniet 16 asthma RCT Nine sessions of exercise None Immediate ↓ respiratory rate (p = 0.0002) [27]
et al. patients age Not clear whether training with I:E 2:1 ↑ tidal volume (p = 0.0009)
(1996) <19 years truly randomized breathing (group 1) ↑ tidal volume/FVC by 25%
versus no breathing ↓ dead space/tidal volume by 12%
instructions (group 2) ↓ SaO2 by 4% (p = 0.018)
Vedanthan 17 adult RCT 16 weeks None Results reported at No between-group difference in medication [32]
et al. asthma clinic True randomization 45 min three times a weeks 4 and 6 of study use, spirometry, morning and evening PEFR
(1998) outpatients week integrated yoga PEFR reported for 7 yoga at weeks 4 and 6 of the study
versus usual management and 7 controls only
Manocha 59 adults RCT Weekly for 4 months 2 h 12 (9 4 months ↓ methacholine PD20 : 1.5 doubling doses greater [33]
et al. symptomatic True randomization Sahaja yoga versus 2 h intervention, 6 months (p = 0.047). ↑ in AQLQ and POMS (p = 0.05)
(2002) on moderate/ Double-blind relaxation, discussion, CB 3 control) No between-group difference in any parameter.
high dose ICS exercises
Sabina 62 adults RCT 4 weeks 180 min/week 17 8 weeks At 16 weeks follow-up, significant improvement [34]
et al. with mild/ Sample size estimate integrated Iyengar yoga 12 weeks in AQOL, rescue inhaler use, spirometry in both
(2005) moderate True randomization versus stretching exercises 16 weeks groups but no between-group differences
asthma Double-blind
Sodhi et al. 120 adults RCT 45 min yoga training/ None 4 weeks ↑ all lung function parameters at 4 and 8 weeks [30]
(2009) (hospital clinic Not clear whether week for 8 weeks plus 8 weeks in intervention group (p < 0.01) compared with
and yoga truly randomized usual care versus usual baseline. No between-group comparisons done
camps) care only
Vempati 60 adults in RCT 40 h yoga teaching, diet, 3 (1 intervention, 8 weeks ↑ lung function only in yoga group (PEFR better [31]
et al. Integral Not clear whether lectures, regular phone 2 control), in yoga group at baseline; p = 0.03)
Systematic review of the effectiveness of breathing retraining in asthma management
(2009) Health Clinic truly randomized follow-up and usual care results for 29 in ↓ EIB
versus usual care yoga group, 28 No change in serum ECP
in control group ↑ total AQOL score (both groups)
↑: Increase in ↓: Decrease in; AQLQ: Asthma Related Quality-of-L ife Questionnaire; AQOL: Asthma related quality of life; CB: Cognitive behavior; ECP: Eosinophilic cationic protein; EIB: Exercise-induced bronchoconstriction;
FEV1: Forced expiratory volume in 1 s; FEV1/FVC: Forced expiratory volume/forced vital capacity (%); FVC: Forced vital capacity; ICS: Inhaled corticosteroid; I:E: Inspiratory:expiratory ratio; PCLE: Pink City Lung Exerciser;
Review
PD20: Provocation dose needed to cause a 20% fall in forced expiratory volume in 1 s; PEF: Peak expiratory flow; PEFR: Peak expiratory flow rates; POMS: Profile of mood states; RCT: Randomized controlled trials.
793
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
[40]
[41]
[42]
[43]
or asthma symptoms as outcomes.
↓ Borg score with increasing pressures monary disease), where chronic obstructive
No change in controls
No change in controls
No change in controls
PImax at RV: 30 cmH2O
Data extraction
↓ PMpeak /PImax: 6.7%
6 months
4 months
1 (intervention)
Table 3. Randomized controlled trials of respiratory muscle training.
truly randomized
Double-blind
Double-blind
Double-blind
RCT
RCT
RCT
(2000) outpatients
(2002) outpatients
Weiner 30 asthma
volunteers
Weiner 22 female
clinic
clinic
clinic
Data synthesis
Continuous outcomes were expressed as
(year)
(1992)
et al.
et al.
et al.
www.expert-reviews.com
allergy clinic truly randomized FEV1 monitoring ↓ asthma attacks 33.1/year
(p < 0.05)
Kahn et al. 80 RCT Five to eight sessions visual feedback of 4 12 months ↓ asthma severity [45]
(1977) 8–15 year olds Not clear whether FEV1 versus weekly monitoring ten ↓ attack number
attending truly randomized sessions of induced obstruction
allergy clinic
Janson- 16 asthma RCT Five sessions of contingent feedback 1 from control 2 weeks ↓ mean TRR by 40% at 2 weeks (p = 0.049) [44]
Bjerklie et al. subjects Double blind versus noncontingent (random) group
(1982) Not clear whether feedback
truly randomized
Mussell et al. 16 asthmatic RCT Five sessions of induced bronchospasm, None None ↑ nonsignificant improvement in rate of [50]
(1988) adults Double blind then TNBF, noncontingent TNBF, recovery from bronchospasm with TNBF
Not clear whether bronchodilator inhaler, placebo inhaler compared with no intervention
truly randomized response versus no intervention
Lehrer et al. 17 asthmatic RCT Six sessions RSA feedback versus None 6 weeks With RSA: [47]
(1997) adults Not clear whether thoracic EMG and incentive spirometry ↓ Ri 23%
truly randomized versus self-relaxation ↑ PEF by 203 ml (p < 0.003)
↓ ETCO2 by 0.91% (p = 0.15)
↓ RR (p < 0.0003)
↑ respiration depth (p < 0.006)
Lehrer et al. 94 volunteer RCT 1) HRV biofeedback and BT 18 10 weeks ↓ controller medication use in groups 1 and 2 [49]
(2004) adult asthma Not clear whether 2) HRV biofeedback only (6 from group 1 (p < 0.0001) and group 3 (p < 0.02)
subjects truly randomized 3) Placebo EEG biofeedback 5 from group 2 ↓ airway resistance in group 1 (p < 0.0007)
4) Waiting list 5 from group 3 and group 2 (p < 0.002)
2 from group 4) FEV1 unchanged any group
Lehrer et al. 45 volunteer RCT 1) HRV biofeedback and BT: age ≥40 9 10 weeks ↓ controller medication use in both groups [48]
(2006) adult asthma Not clear whether compared with age <40 (4 from group 1 (p < 0.001)
subjects truly randomized 2) HRV biofeedback only: 5 from group 2) No within-group difference by age.
age ≥40 compared with age <40 ↓ Airway resistance in group 2 with no
difference by age
↑: Increase in; ↓: Decrease in; BT: Breathing training; ED: Emergency department; EMG: Electromyography;ETCO2: End tidal carbon dioxide; FEV1: Forced expiratory volume in 1 s; HRV: Heart rate variability; PEF: Peak
expiratory flow; RCT: Randomized controlled trial; Ri: Respiratory impedance; RR: Respiratory rate; RSA: Respiratory sinus arrhythmia; TNBF: Trachea noise biofeedback; TRR: Total respiratory resistance.
Systematic review of the effectiveness of breathing retraining in asthma management
Review
795
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
Bowler (1998) [12] -9.00 (-79.48–61.48) 18, 374 (115) 19, 383 (103) 36.49
Holloway (2007) [19] 31.40 (-22.03–84.83) 40, 439 (109) 32, 408 (119) 63.51
-84.8 0 84.8
Favors Favors
control breathing retraining
Figure 2. Weighted mean difference in peak expiratory flow (l/min) from breathing retraining randomized controlled trials.
SD: Standard deviation; WMD: Weighted mean difference.
in asthma-related quality-of-life questionnaire (AQLQ) for one severity and were followed up over 6 months. Instructor contact
patient in 1 month (number needed to treat: 1.96; 95% CI: with the participants during follow-up was planned a priori and
not reported). There was some evidence that beneficial effects was the same in each group. While there was no change in lung
declined with time if breathing techniques were not maintained. function between groups, there was a significant reduction in ICS
After the end of 6 months treatment, the number needed to treat and b2-agonist use in the BBT group. However, the participants
had increased from two to four. A limitation of this study was in the BBT arm might have become aware of allocation as the
that lung function was not measured. use of the term ‘Buteyko’ was not prohibited during instruction,
Cooper et al. compared BBT taught by a certified BBT practi- possibly resulting in incomplete participant blinding.
tioner with controled breathing (to mimic ‘pranayama’ yoga) using Slader et al.’s video-based trial used hypoventilation, nasal
the ‘Pink City Lung Exerciser’ (PCLE) and a ‘placebo’ PCLE [15] . breathing and breath holding at functional residual capacity
The study found significant improvement in asthma symptoms mimicking BBT as the active intervention and a combination
and bronchodilator use in the BBT group compared with both the of nonspecific upper body exercises as the control intervention.
PCLE and placebo groups, but no between-group difference in The study found no significant change in FEV1, FVC or airway
forced expiratory volume in 1 s (FEV1) or provocation dose needed hyper-responsiveness (AHR) in either active or control group
to cause a 20% fall in FEV1 (PD20) for methacholine or ICS use. but significant and comparable reduction in bronchodilator and
McHugh et al. examined BBT taught by an accredited represen- ICS use and improvement in AQLQ in both groups [17] . The
tative versus asthma education and relaxation in 38 subjects with conclusion was that breathing techniques may be useful in the
asthma [16] . The groups were individually matched for asthma management of patients with mild asthma symptoms who use a
Bowler (1998) [12] 0.00 (-12.20–12.20) 18, 72 (22) 19, 72 (15) 12.43
Cowie (2008) [21] 3.96 (-3.37–11.29) 56, 82.9 (19.2) 63, 79 (21.6) 34.41
Grammatopoulou (2011) [18] 1.70 (-4.20–7.60) 20, 86.3 (8.21) 20, 84.0 (10.7) 53.17
-12.2 0 12.2
Favors Favors
control breathing retraining
Figure 3. Weighted mean difference in forced expiratory volume in 1 s (% predicted) from breathing retraining randomized
controlled trials.
SD: Standard deviation; WMD: Weighted mean difference.
www.expert-reviews.com 797
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
Fluge (1994) [59] -0.13 (-0.68–0.42) 12, 2.33 (0.67) 9, 2.46 (0.62) 6.86
Holloway (2007) [19] 0.10 (-0.25–0.45) 40, 2.8 (0.7) 32, 2.7 (0.80) 17.05
Meuret (2007) [13] -0.21 (-0.68–0.26) 8, 2.32 (0.33) 4, 2.53 (0.42) 9.53
Cowie (2008) [21] 0.14 (-0.17–0.45) 56, 2.72 (0.934) 63, 2.58 (0.803) 21.30
Thomas (2009) [14] -0.02 (-0.28–0.24) 73, 2.95 (0.83) 79, 2.97 (0.78) 32.08
Grammatopoulou (2011) [18] -0.13 (-0.53–0.27) 20, 2.33 (0.67) 20, 2.46 (0.62) 13.19
-685 0 685
Favors Favors
control breathing retraining
Figure 4. Weighted mean difference in forced expiratory volume in 1 s (l) from breathing retraining randomized
controlled trials.
SD: Standard deviation; WMD: Weighted mean difference.
reliever frequently, but there is no evidence to favor shallow nasal quality-of-life scores in both groups but no difference in FEV1%
breathing over nonspecific upper body exercises. predicted between the groups [21] . The improvement in medi-
Cowie et al. compared BBT taught by an accredited practitioner cation use and AQLQ score in both arms in these two studies
with breathing exercises taught by a physiotherapist and found suggested a common mechanism or that improvement was due
significant and comparable improvement in asthma control and to nonspecific effects.
Bowler (1998) [12] 1.19 (0.44–1.94) 18, 1.2 (0.9) 15, 0.4 (0.13) 13.05
Holloway (2007) [19] 0.13 (-0.33–0.60) 32, -15.2 (10.9) 40, -16.7 (11.6) 20.61
Cowie (2007) [21] -0.09 (-0.45–0.27) 56, 5.6 (1.17) 63, 5.7 (1) 24.17
Thomas (2009) [14] 0.37 (0.08–0.67) 94, 5.41 (1.23) 89, 4.94 (1.29) 26.50
Grammatopoulou (2011) [18] 0.60 (-0.04–1.23) 20, 52.3 (5.4) 20, 48.8 (6.31) 15.67
-1.94 0 1.94
Favors Favors
control breathing retraining
Figure 5. Standardized mean difference in asthma-related quality-of-life score from breathing retraining randomized
controlled trials. Asthma-related quality-of-life scores from the Holloway study (lower score is better) were attributed negative values to
be consistent with other studies (higher score is better). Weights are from random effects analysis.
SD: Standard deviation; SMD: Standardized mean difference.
Bowler (1998) [12] 2.30 (0.37–4.23) 18, 35.3 (3) 19, 33 (3) 24.60
Meuret (2007) [13] 3.20 (-2.35–8.75) 8, 38.5 (5.8) 4, 35.3 (3.9) 5.23
Holloway (2007) [19] -0.10 (-2.43–2.23) 40, 39.2 (3.4) 32, 39.3 (6) 19.97
Thomas (2009) [14] 0.60 (-1.19–2.39) 73, 33 (5.48) 79, 32.4 (5.78) 26.55
Grammatopoulou (2011) [18] 3.30 (1.29–5.31) 20, 37.9 (3.54) 20, 34.6 (2.91) 23.65
-8.75 0 8.75
Favors Favors
control breathing retraining
Figure 6. Weighted mean difference in end tidal CO2 (mmHg) from breathing retraining randomized controlled trials.
Weights are from random effects analysis.
SD: Standard deviation; WMD: Weighted mean difference.
Holloway et al. examined a physiotherapist-taught breathing function. The study was limited by the absence of a control inter-
technique (Papworth method) plus usual care versus usual care vention. Thomas et al. also examined physiotherapist-led breath-
only in a cohort with mild or well-controlled asthma from a ing training versus nurse-led asthma education in a larger cohort
semirural general practice [19] . At both 6- and 12-month follow- of subjects with reduced asthma-related quality-of-life (AQOL)
up, there was significant improvement in St George Respiratory recruited from general practice [14] . At 6-month follow-up, sig-
Questionnaire symptom score, hospital anxiety and depression nificant improvements in AQLQ score, Nijmegen questionnaire
(HAD) questionnaire anxiety and depression scores and Nijmegen score and HAD questionnaire anxiety and depression scores in the
questionnaire score but no between-group difference in lung breathing training group compared with the control group were
N, mean (SD) N, mean (SD)
Study WMD (95% CI) % weight
yoga control
Nagarantha (1985) [28] 72.00 (40.03–103.97) 44, 363 (108) 50, 291 (12.2) 31.64
Singh (1990) [29] 14.00 (-49.07–77.07) 18, 475 (99) 18, 461 (94) 17.17
Vedanthan (1998: am results) [32] 15.00 (-41.92–71.92) 7, 412 (60) 7, 397 (48) 19.38
Vedanthan (1998: pm results) [32] 4.00 (-58.39–66.39) 7, 406 (62) 7, 402 (57) 17.40
Manocha (2002) [33] 5.21 (-66.98–77.40) 21, 370 (140) 26, 365 (105) 14.41
-105 0 105
Favors Favors
control yoga
Figure 7. Weighted mean difference in peak expiratory flow (l/min) from yoga randomized controlled trials. Weights are from
random effects analysis.
SD: Standard deviation; WMD: Weighted mean difference.
www.expert-reviews.com 799
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
Singh (1990) [29] 40.00 (-515.48–595.48) 18, 3460 (870) 18, 3420 (830) 57.48
Vedanthan (1998) [32] -900.00 (-1803.55–3.55) 9, 3290 (820) 8, 4190 (1050) 42.52
-1804 0 1804
Favors Favors
control yoga
Figure 8. Weighted mean difference in forced expiratory volume in 1 s (ml) from yoga randomized controlled trials.
Weights are from random effects analysis.
SD: Standard deviation; WMD: Weighted mean difference.
found. However, there was no improvement in lung function in and were then offered the intervention, taken up by only two
either group. More recently, Grammatopoulou et al. examined the participants. At 8-week follow-up normocapnia (end-tidal pCO2
effect of physiotherapist-led breathing training plus usual treat- 40 mmHg), an improvement in asthma control, asthma symp-
ment in 40 adults with mild/moderate asthma recruited from a toms and a reduction in PEF variability with no change in FEV1
hospital asthma clinic [18] . They found significant improvement in were found in the intervention group. Follow-up was not done
airway control test (ACT) score, Short Form-36 version 2 Health in the control group. The small number in the study together
Survey (SF-36v2) physical component score, increased end tidal with the absence of useful data from the control group limits the
CO2 and reduced respiratory rate in the intervention group com- usefulness of the findings.
pared with controls who continued with usual treatment only. Chiang et al. examined the effect of breathing/relaxation
While there was no between-group change in lung function, there instruction in addition to a clinic-planned asthma self-man-
was a significant improvement in FEV1% predicted within the agement program compared with self-management only in
intervention group at 3 months follow-up compared with baseline. 48 Taiwanese children with moderate to severe asthma recruited
Meunert et al. conducted a pilot study in 12 asthma subjects from an asthma clinic [24] . PEF, asthma symptoms and medica-
recruited by advertisement [13] . The intervention was initial edu- tion use improved in both groups with no between-group differ-
cation in breathing patterns in asthma followed by capnometry- ences. There was a significant reduction in anxiety scores in the
assisted breathing training and home breathing exercises over a experimental group only. The adequacy of blinding in the study
4-week period, plus usual treatment (n = 8). The control group was in doubt in that the breathing/relaxation instruction was
(n = 4) continued with usual treatment for the 4-week period given by a ‘researcher’.
N, mean (SD) N, mean (SD)
Study WMD (95% CI) % weight
yoga control
Vempati (2009) [31] 18.00 (8.28–27.72) 28, 77.9 (17.2) 26, 59.9 (19.1) 30.72
Manocha (2002) [33] 2.13 (-11.57–15.83) 21, 76.6 (21.8) 26, 74.4 (26.1) 21.88
Sodhi (2009) [30] 5.90 (2.26–9.54) 60, 83.2 (10.5) 60, 77.3 (9.86) 47.39
-27.8 0 27.8
Favors Favors
control yoga
Figure 9. Weighted mean difference in forced expiratory volume in 1 s (% predicted) from yoga randomized controlled trials.
Weights are from random effects analysis.
SD: Standard deviation; WMD: Weighted mean difference.
Vempati (2009) [31] -0.73 (-1.27– -0.19) 29, -5.46 (1.1) 28, -0.45 (1.5) 54.99
Manocha (2002) [33] -0.46 (-1.05–0.14) 21, 0.66 (0.42) 24, 0.91 (0.64) 45.01
-1.27 0 1.27
Favors Favors
yoga control
Figure 10. Standardized mean difference in asthma-related quality-of-life score from yoga randomized controlled trials.
Asthma-related quality-of-life score from Vempati study (lower score is better) were attributed negative values to be consistent with
Manocha study (higher score is better).
SD: Standard deviation; SMD: Standardized mean difference.
McHugh et al. examined breathing retraining using BBT on intervention arm were included in the final analysis, which was
eight asthmatic children using a before-and-after (B&A) design not intention-to-treat.
(Table 5) [25] . At 3-month follow-up, the main findings were a Singh et al. utilized pranayama by enforcing the 1:2
decrease in b2-agonist and ICS use, a reduction in missed school inspiratory:expiratory ratio with the PCLE device (a disk with a
days and oral steroid courses and an improved asthma symptom one-way valve that imposes a 1:2 ratio) compared with an other-
score compared with baseline. However, confidence intervals and wise identical (non-pranayama) device in a case-crossover study of
tests of significance were not reported and lung function was not 22 adults with mild asthma [29] . There was a significant increase
examined. The authors conceded that self-selection of the partici- in the doubling dose for PD20 for histamine with the active com-
pants and the small number in the study precluded meaningful pared with the control device but no significant difference in lung
interpretation of the results. function parameters between the devices.
It was not possible to include data from all studies in a meta- Although their research question addressed exercise training
analysis of breathing retraining owing to differences in outcome rather than yoga in asthma management, Ceugniet et al. incor-
reporting. However, where such analyses could be done, no effect porated a pranayama technique into their study of exercise train-
of breathing retraining on lung function could be demonstrated ing in children with severe asthma [26] . They reported a trend
(Figures 2–4) but a favorable effect of breathing retraining on AQOL towards better FEV1 but no significant effect on FEV1/FVC ratio
and on end-tidal CO2 was shown (Figures 5 & 6) . following exercise training with pranayama. No change was found
in lung function in the control group following similar exercise
Yoga training without pranayama. In a later study on a similar par-
Randomized controlled trial studies ticipant group, the same authors [27] found that the same inter-
A total of 14 studies examined yoga in asthma management and vention significantly reduced respiratory frequency, dead space/
nine used an RCT design (Table 2) . In six out of the nine studies tidal volume ratio and increased tidal volume in the group using
[26–31] it was not clear whether true randomization had been car- exercise with pranayama. However, postexercise oxygen satura-
ried out and in seven studies [26–32] double blinding was either not tion in the intervention group was reduced from pretest values
clear or not done. Follow-up times in these studies varied from by a clinically important amount, whereas it did not change in
immediate to 54 months and study numbers ranged from 16–120. the control group.
Two studies found a significant between-group difference in lung Vedanthan et al. found that 16 weeks of integrated yoga com-
function or AQOL [27,31] . pared with usual treatment had no effect on lung function as mea-
The longest study in terms of follow-up [28] , found significant sured at 4 and 6 weeks after study commencement [32] . Manocha
benefit from integrated yoga exercises as well as usual treatment et al. examined Sahaja yoga compared with relaxation, discussion
with increased PEFR, decreased medication use and a decrease and cognitive behavior training [33] . They found an improvement
in attack severity. However, the study participants were from a in AHR, AQOL mood subscale and the profile of mood states
yoga clinic, with the associated risk of selection bias, and while score at the end of the 4-month study period in the intervention
both active and control groups continued with usual prescribed group only but no significant between-group differences in any
bronchodilator medication, the control group did not receive measure 2 months later. Sabina et al. trialed 16 weeks of integrated
a ‘placebo’ intervention. There was a high attrition rate (47%) yoga versus stretching exercises and found no between-group dif-
as only ‘frequent’ practitioners (>16 days per month) in the ference in FEV1, rescue inhaler use and AQOL at 16 weeks [34] .
www.expert-reviews.com 801
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
[38]
[35]
[36]
[37]
[39]
cises in addition to usual treatment versus
usual treatment only in a cohort of asthma
subjects recruited from a hospital clinic and
↑ FEV1: 11.8% predicted; ↑PEFR: 8.3 l/min
↑: Increase in; ↓: Decrease in; FEV1: Forced expiratory volume in 1 s; MMFR: Maximal mid-expiratory flow rate; MVV: Maximum voluntary ventilation; PEFR: Peak expiratory flow rate; VC: Vital capacity.
yoga camps [30] . They reported significant
3–54 months ↓ attacks/week: 2.6; ↓ severity: 0.45
↑ FEV1/FVC: 14.02%
pants from a hospital-based ‘Integral Health
↑ MVV: 18.2 l/min
↑ PEFR: 53.9 l/min
↑ FEV1: 1.4l
nificant improvement in lung function and
exercise-induced bronchoconstriction in the
intervention group compared with the con-
trol group and improvement in AQOL in
Withdrawals/ Follow-up
1 year
None
None
follow-up
follow-up
20 lost to
11 lost to
None
None
lectures
Before-and-
Before-and-
Before-and-
Before-and-
after trial
after trial
after trial
after trial
Design
outpatients
outpatients
(1996)
(2001)
(1991)
Weiner (2000) [42] -1.30 (-2.41– -0.19) 11, 1.6 (1.33) 11, 2.9 (1.33) 73.45
Weiner (2002) [43] -0.90 (-2.75–0.95) 10, 2.1 (1.58) 9, 3 (2.4) 26.55
-2.75 0 2.75
Favors Favors
RMT control
Figure 11. Weighted mean difference in b2-agonist use from respiratory muscle training randomized controlled trials.
RMT: Respiratory muscle training; SD: Standard deviation; WMD: Weighted mean difference.
although for many participants, persistence with the exercise A limitation in these studies was the use of a forced expiratory
program was short-lived [40] . maneuver as the biofeedback instrument. Any improvement could
Weiner et al., in three separate RCTs, found that specific not necessarily be attributed to genuine operant conditioning as
inspiratory muscle training using either an externally weighted the maneuver is partly dependent on motivation and effort, which
device or a purpose-designed threshold inspiratory muscle trainer might vary between individuals.
(HealthScan; NJ, USA) compared with ‘sham’ muscle training Mussell et al. in a study of trachea–bronchial noise reduction
significantly increased inspiratory muscle strength as measured as the biofeedback instrument to reverse induced bronchospasm,
by maximal inspiratory mouth pressure at residual volume (PImax found that trachea–bronchial noise reduction as the biofeedback
at residual volume). With 4–6 months training, subjects with the instrument was modestly and nonsignificantly more effective than
active intervention improved FEV1, FVC, symptoms and Borg no intervention [50] . Janson-Bjerklie et al. trialed contingent bio-
dyspnea score and decreased bronchodilator use. The most recent feedback versus random feedback and found that total respiratory
of these studies that compared female to male asthmatics [43] resistance (TRR) across five training sessions was greater in their
found that using the same training method to allow females to intervention group than the control group [44] . Lehrer et al. found
attain a PImax equal to that of males resulted in a significant and that respiratory sinus arrhythmia as a feedback tool compared
highly correlated decrease in both dyspnea score and medication with electromyography biofeedback plus incentive inspirometry or
use in the active intervention group only. self-relaxation reduced respiratory impedance by 23% in a small
A meta-analysis (Figure 11) showed a favorable effect of respiratory group of adults with asthma but the authors did not report results
muscle training on b2-agonist use. of any statistical tests [47] . Two later studies by Lehrer et al. found
that heart rate variability biofeedback plus breathing training
Biofeedback training or heart rate variability biofeedback alone significantly reduced
A total of seven RCTs [44–50] and five B&A studies [51–55] were controller medication use and improved airway resistance, inde-
identified (Tables 4 & 7) . Six RCTs [44–49] and two B&A studies [52,53] pendent of increasing age in asthmatic adults but produced no
found significant improvement in lung function, medication use change in lung function [48,49] .
or asthma symptoms. Participant numbers were generally small One uncontrolled study [52] showed a significant improvement
and follow-up times were short. in mid-expiratory flow rate and TRR compared with baseline
Kahn et al. trained 20 children with asthma attending an using an auditory signal reflecting TRR as the biofeedback tool
allergy clinic to induce bronchoconstriction using inhalation, while another [53] found improvement in FEV1 and FEF50 in 17 out
suggestion or medication methods previously known to induce of 20 asthmatic children taught to use respiratory sinus arrhyth-
bronchoconstriction [46] . Bronchodilatation via FEV1 biofeedback mia feedback to prolong expiration. On the other hand, Erskine-
reinforcement was then taught weekly to the intervention group Millis et al. found no benefit for TRR from either short-term or
(n = 10). Compared to ten controls who received weekly FEV1 more intensive biofeedback training compared with baseline and
measurement but no biofeedback reinforcement, the intervention even a deterioration in FEV1 after more intensive training. It was
group experienced significant reductions in medication use, num- concluded that no benefit was to be had from biofeedback training
ber of emergency room visits and asthma attacks over the 1-year in adults with moderate/severe chronic asthma [51] .
follow-up period. Lung function was not reported. However, Steptoe et al. showed that nonasthmatic subjects were able to
when Khan et al. repeated the study in 80 similar children over decrease airways resistance significantly and consistently over
a 12‑month period, these findings could not be replicated [45] . biofeedback training sessions, but asthmatic subjects’ airways
www.expert-reviews.com 803
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
[55]
Ref.
[51]
[54]
[53]
↑: Increase in; ↓: Decrease in; FEV1: Forced expiratory volume in 1 s; FEF50 : Forced expiratory flow at 50% of forced vital capacity; MMEF: Maximal mid-expiratory flow; RSA: Respiratory sinus arrhythmia; TRR: Total
trend towards a decrease (p = 0.059) [55] .
Finally, Mass et al. found no change in lung
in 17 out of 20 children
feedback to reduce respiratory resistance in
a cohort of 15 asthmatics [54] .
No change in FEV1,
Discussion
The BBT has been the most widely pub-
licized among the CAM techniques used
in asthma management. Individual stud-
ies using BBT consistently demonstrated a
S1: 4 weeks
Follow-up
4 weeks
3 weeks
together with respiratory physiotherapy
None
None
None
None
None
controlled study)
completed as a
diagnosis of asthma
15 outpatients with
emotional trigger)
Erskine-Millis Study 1: 9 adults
16 nonasthmatic
asthma
(1993)
(1976)
(1981)
improved lung function and quality of life, and a meta-analysis treatments for asthma. However, there were too few well-designed
showed a significant reduction in medication use, warranting studies with adequate power and length of follow-up to allow defi-
further examination of this technique. nite conclusions to be drawn. On the existing evidence, and pro-
Methods in yoga were highly heterogeneous, ranging from vided that prescribed medications were continued, it would be rea-
comprehensive inpatient programs to short-term outpatient sonable for clinicians to offer qualified support to asthma patients
training. Comparing RCTs to non-RCTs, we found that non- intending to undertake such techniques under the supervision of
RCTs involving yoga training tended to yield higher therapeutic a qualified instructor.
effects than RCTs. Studies that isolated a component of yoga Given the rising popularity of complementary and alternative
found some benefit, whereas the only RCT of integrated yoga medicine in asthma, further studies of breathing retraining are
that yielded significant improvement was limited by a high and warranted so that clinicians and patients alike can make informed
selective drop-out rate. Nonetheless, a meta-analysis showed a treatment decisions.
favorable effect of yoga on AQOL and a similar, although limited,
effect was seen on one measure of lung function. We attempted Expert commentary
to perform sensitivity analyses by incorporating non-RCTs of Asthma management can be difficult. As is often the case in
yoga in some of the meta-analyses. However this was not possible chronic disease for which a cure cannot always be offered,
owing to unavailability of data from non-RCTs in a form suitable patients with asthma will turn to CAMs in an attempt to self-
for inclusion in a meta-analysis. help. The literature on CAMs in asthma management is not
Biofeedback training was limited by heterogeneity in meth- extensive and that which exists may report findings that are not
odology and often limited by small sample sizes. The need for always based on robust study design. However, clinicians would
specialized equipment in patient training limits the more general do well not to prejudge complementary methods but evaluate the
use of this technique among asthma patients. empirical evidence for the benefits and risks of these methods,
Nearly all systematic reviews are restricted to RCTs and the and if such evidence is lacking, take the lead in implementing
inclusion of B&A trials in this review is novel. In a B&A trial, adequately powered trials that employ the scientific method that
it is difficult to link improvements in outcome measures to the might provide the evidence.
intervention as the outcome may have multiple determinants and There is evidence indicating possible benefit from several tech-
it is difficult to know what proportion of a given outcome is niques, the BBT, yoga and respiratory muscle retraining. All are
determined by the intervention and what is due to patient-related readily available, not difficult to learn and may be cost-effective.
factors. With that limitation, it is notable that the B&A trials These techniques will not replace asthma medication or a care-
of yoga techniques tended to show improvement in outcomes fully designed asthma plan, but their use should not be dismissed
such as medication use and lung function parameters, which were out of hand. Further well-designed trials of these techniques are
sometimes statistically significant. It would be of interest to see the needed to properly evaluate their place in asthma management.
results of an adequately powered, well-designed RCT of a clearly
defined yoga intervention in asthma management. Five-year view
Owing to differences in study design, sample size, participant Patient-driven asthma self-help will not lessen in the near future
retention and adequacy of follow-up it was difficult to draw firm and clinicians should take the lead in setting up scientific tri-
conclusions about the benefits of these treatments. als of self-help methods, particularly breathing retraining.
Consequently, we anticipate that the body of evidence for breath-
Conclusion ing retraining in asthma management will grow over the next
The BBT and similar breathing retraining techniques, yoga and few years and result in the establishment of clear guidelines as to
respiratory muscle training all showed some benefit as alternative whether and when such techniques should be employed.
Key issues
• Despite their popularity among asthma patients, breathing retraining techniques are controversially regarded by clinicians.
• The Buteyko breathing technique (BBT), physiotherapist-led breathing retraining, respiratory muscle retraining, yoga and biofeedback
have been trialed in asthma management.
• In pooled estimates, asthma-related quality of life was significantly improved by BBT or physiotherapist-led breathing retraining and by
yoga. No evidence was found for improvement in lung function from BBT or physiotherapist-led breathing retraining. However, there is
limited evidence for improvement in lung function from yoga and for the reduction in b2-agonist use from respiratory muscle
retraining.
• On current evidence, it is reasonable for clinicians to offer qualified support to patients intending to use BBT, physiotherapist-led
breathing retraining, yoga or respiratory muscle retraining, provided there is supervision by a qualified instructor, usual prescribed
medication is continued and limitations of the interventions are understood.
• Biofeedback is unlikely to be of practical use in asthma management.
• Further well-designed, adequately powered randomized controlled trials of breathing retraining techniques in asthma management
are warranted.
www.expert-reviews.com 805
Review Burgess, Ekanayake, Lowe, Dunt, Thien & Dharmage
Financial & competing interests disclosure employment, consultancies, honoraria, stock ownership or options, expert
The authors have no relevant affiliations or financial involvement with any testimony, grants or patents received or pending, or royalties.
organization or entity with a financial interest in or financial conflict with No writing assistance was utilized in the production of this
the subject matter or materials discussed in the manuscript. This includes manuscript.
10 Seaton A, Seaton D, Leitch AG. Crofton and • Another large RCT with interesting and
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