You are here

Article Text

Article menu
Chronic obstructive pulmonary disease
Physiological changes related to 10 weeks of singing for lung health in patients with COPD
  1. Mette Kaasgaard1,2,
  2. Daniel Bech Rasmussen2,3,
  3. Anders Løkke3,4,
  4. Peter Vuust1,
  5. Ole Hilberg3,4 and
  6. Uffe Bodtger2,3
  1. 1Center for Music in the Brain, Department of Clinical Medicine, Aarhus University and the Royal Academy of Music, Aarhus/Aalborg, Aarhus University, Faculty of Health, Aarhus, Denmark
  2. 2Pulmonary Research Unit Region Zealand (PLUZ), Department of Respiratory Medicine, Zealand Univsersity Hospital Naestved and Roskilde, Naestved, Denmark
  3. 3Department of Regional Health Research, University of Southern Denmark Faculty of Health Sciences, Odense, Denmark
  4. 4Department of Respiratory Medicine, Lillebaelt Hospital, Vejle, Southern Denmark, Denmark
  1. Correspondence to Mette Kaasgaard; mk{at}clin.au.dk

Abstract

Background Singing for Lung Health (SLH) was non-inferior to physical exercise training in improving 6-minute walking test distance (6MWD) and quality of life (St. George’s Respiratory Questionnaire (SGRQ)) within a 10-week pulmonary rehabilitation (PR) programme for COPD in our recent randomised controlled trial (RCT) (NCT03280355). Previous studies suggest that singing improves lung function, respiratory control and dyspnoea, however this has not yet been convincingly confirmed. Therefore, this study aimed to explore the impact of SLH on physiological parameters and the associations with achieving the minimal important difference (MID) in 6MWD and/or SGRQ.

Methods We conducted post hoc, per-protocol analyses mainly of the SLH group of the RCT, exploring associations with 6MWD and SGRQ results by stratifying into achieving versus not-achieving 6MWD-MID (≥30 m) and SGRQ-MID (≤−4 points): changes in lung function, inspiratory muscle strength/control, dyspnoea, and heart rate response using logistic regression models. Further, we explored correlation and association in achieving both 6MWD-MID and SGRQ-MID (or in neither/nor) using Cohen’s κ and Cochran-Mantel-Haenszel Test.

Results In the SLH study group (n=108), 6MWD-MID was achieved by 31/108 (29%) and in SGRQ by 53/108 (49%). Baseline factors associated with achieving MID in either outcome included short baseline 6MWD and high body mass index. Achieving 6MWD-MID was correlated with improved heart rate response (OR: 3.14; p=0.03) and achieving SGRQ-MID was correlated with improved maximal inspiratory pressure (OR: 4.35; p=0.04). Neither outcome was correlated with significant spirometric changes. Agreement in achieving both 6MWD-MID and SGRQ-MID was surprisingly insignificant.

Conclusions This explorative post hoc study suggests that SLH is associated with physiological changes after short-term PR for COPD. Future physiological studies will help us to understand the mechanisms of singing in COPD. Our study furthermore raises concern about poor agreement between subjective and objective benefits of PR despite state-of-the-art tools.

  • emphysema
  • exercise
  • lung physiology
  • pulmonary rehabilitation
  • respiratory muscles

Data availability statement

Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information. Consent forms will not be available according to Danish legislation. De-identified data collected for the study will be available from 1 January 2023, upon reasonable request. Contact study investigator (MK), mk@clin.au.dk.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjresp-2022-001206

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    WHAT IS ALREADY KNOWN ON THIS TOPIC

    • Singing for lung health (SLH) as part of community-based pulmonary rehabilitation has shown effects on walking distance and quality of life (QoL) in COPD, but current knowledge on the impact of SLH on physiological parameters is scarce.

    WHAT THIS STUDY ADDS

    • This study suggests that improvements in 6-minute walking test and QoL during a short-term SLHprogramme is associated with diverse physiological changes in patients with COPD.

    HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE, AND/OR POLICY

    • Our findings support that SLH has physiological impact besides being a pleasant leisure time activity in COPD. However, further studies are needed to explore associations and to conclude on benefits of SLH for COPD.

    Introduction

    Singing has become widely acknowledged as a beneficial activity for people living with chronic respiratory disease and is proposed to improve physical, psychological, and social health.1 2 An initial body of research in respiratory disease suggests that singing addresses dyspnoea control,3–10 improves exercise capacity,4 11 12 enhances quality of life (QoL),3 4 13 14 and reduces anxiety and depression.14 Moreover, singing with peers builds meaningful cohesion and reduces experiences of isolation.1 3 4 15–20

    However, it is still unknown how singing exerts its effects, that is, which specific physiological parameters may change during an effective singing training course.2–4 A recent narrative review2 suggested that singing may improve aspects in breathing pattern, respiratory control, hyperinflation, dyspnoea, health-related QoL, interoception, and physical capacity and activity in COPD. However, the authors concluded that the present evidence suffers from severe between-study heterogeneity including definitions and parameters of effectiveness. The gold standard parameter of effectiveness in pulmonary rehabilitation (PR) research is walking test distance, either 6-minute walking test (6MWT) or incremental shuttle walking test.21 22 In contrast, the primary outcome of the majority of studies on singing is perceived effect (qualitative or semiquantitative outcomes) and not objective parameters such as exercise capacity and physiological mechanisms.2–4 12 Thus, there is a lack of research on physiological changes during singing and on the association between achieving objective and subjective improvement.

    We recently published results from the so-far largest randomised controlled trial (RCT) on singing compared with physical exercise training (PExT) as part of a 10 weeks’ community-based PR programme in COPD.12 As intervention, we used the current best-practice and disease-specific singing approach, Singing for Lung Health (SLH)3 10 23 24 and with the comparator (PExT) representing the gold standard training activity within PR. We included 270 patients with COPD and found that SLH was non-inferior to PExT in improving 6MWT distance (6MWD) (primary study outcome) and QoL (St. George’s Respiratory Questionnaire, SGRQ) (the first of several secondary study outcomes).12

    In the present study, we aimed to explore physiological changes related to SLH. Specifically, we aimed to investigate whether SLH was associated with physiological changes in lung function, inspiratory muscle strength and control, dyspnoea and breathing control, and exercise-induced changes in pulse and oxygen saturation. Further, we aimed to investigate associations and overlap between achieving minimal important difference (MID) in 6MWD and/or SGRQ.

    To elucidate these aspects, we conducted post hoc analyses of our RCT exclusively focusing on the proportion of SLH study participants with complete data from both baseline and follow-up, thus representing the SLH per-protocol population.12 We hypothesised that attending SLH would be associated with positive changes in physiological parameters and mostly in persons who achieved either 6MWD-MID or SGRQ-MID. Moreover, we hypothesised that achieving 6MWD-MID and SGRQ-MID would be clearly overlapping.

    METHODS

    Study design, oversight, participants, randomisation and blinding, and data collection

    For this post hoc, explorative study, we included data retrieved from the per-protocol RCT population (n=195), that is, patients who completed both baseline and follow-up assessments. The main focus of this paper is on the SLH group (n=108), but we also included supplementary analyses of the overall RCT per-protocol population (n=195) and of the group receiving the gold standard, PExT, the PExT group (n=87) to assess basic comparability and for transparent reporting and exploratory investigation.

    The RCT was conducted between August 2017 and May 2019 (ClinicalTrials.gov; NCT03280355). Details on inclusion criteria, procedures for randomisation, blinding, and data collection are described in our previous paper.12

    Groups

    Participants were stratified accordingly:

    Stratum 1: Study group: SLH is the main focus of this paper, with PExT data mainly presented as supplementary data.

    Stratum 2: PR outcomes:

    1. Objective benefit of PR=achieving 6MWD-MID (≥30 metres)25 or not, and

    2. Subjective benefit of PR=achieving SGRQ-MID (≤−4.0 units)26 or not.

    Outcomes and measures

    Baseline characteristics included sociodemographic information, body mass index (BMI), medication usage, smoking history, expectations towards benefits of singing, forced expiratory volume in 1 s (FEV1 in L, and as percentage predicted (FEV1%)), forced vital capacity (FVC in L, and as percentage predicted (FVC%)), FEV1/FVC ratio (FEV1/FVC as percentage), forced expiratory flow (FEF25%–75% (L/s)), maximum inspiratory pressure (MIP), single breath count test, breath holding test, Modified Medical Research Council Dyspnoea Scale, modified BORG-CR10-Dyspnoea Scale, and baseline performance in 6MWD and SGRQ total score.

    Effect was reported as change from baseline to follow-up concerning the following study domains and related parameters:

    1. Performance in 6MWD and SGRQ, including achievement of MID (yes/no).25 26

    2. Lung function: FEV1 and FVC, both reported in litres (MID: ≥120 mL).27

    3. Inspiratory muscle strength and control: MIP (MID: ≥17 cm H2O;28–31 ≥10% change also explored).

    4. Dyspnoea and breathing control: single breath count test (≥10% and ≥50% change).19 32 33

    5. Exercise-induced changes in pulse and saturation: pulse (beats/min) and heart rate response (highest pulse reached minus baseline pulse) (≥10% and ≥50% change), and Oxygen Saturation Response and Chronotropic Index (exercise-induced oxygen desaturation (EID)).34

    See online supplemental table S1 for details and interpretation of study outcomes and measures.

    Trial interventions

    Information on content and delivery of the 10 weeks’ trial interventions and additional patient education as part of the PR programme are reported in our previous paper and appertaining supplementary files.12 Content, delivery and approach of SLH have also been described previously.2 12 23 24

    Patient and public involvement

    Participants were not involved in study development, recruiting or execution. We intend to enlist the support of participants in developing and implementing our dissemination strategy.

    Statistics

    To investigate comparability, the overall per-protocol population (n=195) was compared (SLH vs PExT). Subsequently, the SLH group (and supplementary, the PExT group) was stratified according to the two study outcomes, 6MWD and SGRQ, comparing achieved versus not achieved MID for each outcome. We used Student’s t-test in the primary analyses to test independence within continuous data (described results as mean±SD) regarding baseline, follow-up, and change values (=computed change from baseline to follow-up). Level of significance was reported as p value, and changes were presented with 95% CI. Pearson’s χ2 test (or Fisher’s test) was used to test independence in distribution within categorical data (results reported as number and percentage). Within-group changes from baseline to follow-up were analysed using paired-samples tests with level of significance reported as: no star: p>0.05, *: p<0.05, **: p<0.01; ***: p<0.001.

    Explanatory factors were explored in relation to the two study outcomes using logistic regression models. At first, significance was explored in all relevant variables using univariable models. Continuous variables were transposed into categories: age (transposed into tertiles), sex (male/female), BMI (transposed into tertiles), 6MWD at baseline (transposed into tertiles) and MID yes/no in FEV1. Change in MIP was explored in categories (yes/no): ≥17 cm H2O and ≥10% improvement. Change in single breath count test was explored in categories: ≥10% and ≥50% improvement, and changes in EID were explored in categories (yes/no): ≥10% and ≥50% improvement in heart rate and resolvement of baseline EID at follow-up (yes/no) (see online supplemental table S1 for elaborated outcomes and measures). Subsequently, multilevel mixed-effects logistic regression models were conducted and comprised variables displaying significance in the univariable regression models.

    To investigate correlation and association in achieving MID in both study outcomes (or in neither) in SLH, likelihood and chance-corrected proportional agreement were analysed using Cohen’s κ. Further, the Cochran-Mantel-Haenszel test for 2×2 xK tables was used to assess association and independence between 6MWD and QoL; this analysis included both overall study groups (SLH and PExT).

    Statistical analyses were performed using SPSS V.27.0 (IBM, Chicago, USA); and STATA/IC V.16.1 (StataCorp, Texas, USA). Statistical significance was reached at p<0.05.

    The STrengthening the Reporting of OBservational studies in Epidemiology35 research checklist was used in accordance with recommendations for conduct and dissemination of observational studies.

    RESULTS

    Participants

    The SLH study group (n=108) was retrieved from the RCT per-protocol population (n=195; representing 72% of the RCT intention-to-treat population (n=270)). 6MWD-MID was achieved by 31/108 (29%) and SGRQ-MID by 53/108 (49%) (see figure 1).

    Figure 1
    Figure 1

    Consort flow diagram. 6MWD, 6-minute walking test distance; MID, minimal important difference; PExT, physical exercise training; SGRQ, St. George’s Respiratory Questionnaire; SLH, singing for lung health.

    Baseline characteristics

    The per-protocol populations of SLH and PExT were comparable. Overall, most were women (n=122; 62.2%), mean age was 68.9 (SD 7.9) years; mean pack years was 40.5 (SD 22.9); mean BMI was 28.2 (SD 5.9); and mean FEV1% predicted was 51.3 (SD 15.8). Both the SLH and the PExT groups showed comparability when stratified in outcomes: 6MWD and SGRQ (MID achieved vs MID not achieved), but differed in size (SLH: n=108; PExT: n=87). Online supplemental table S2 depicts supplementary analyses of baseline data for SLH vs PExT. Online supplemental tables S3 and S4 depict supplementary analyses of baseline characteristics in SLH and PExT, analysed in stratum 6MWD (online supplemental table S3) and stratum SGRQ (online supplemental table S4).

    At baseline, SLH participants achieving 6MWD-MID had higher BMI and lower 6MWD compared with those not achieving MID (online supplemental table S3A), and those achieving SGRQ-MID had higher BMI, higher SGRQ (=lower QoL), and had lower performance in 6MWD, single breath count test, and MIP (online supplemental table S3B).

    Comparing the SLH and PExT groups, we found no significant difference except that SLH participants achieving 6MWD-MID had higher BMI, lower FEV1/FVC ratio, and lower 6MWD (online supplemental table S3A), and SLH-participants achieving SGRQ-MID had lower BMI and lower value parameters related to lung function, inspiratory control and function, and dyspnoea control (online supplemental table S4A). In the PExT group, only educational level differed in those achieving SGRQ-MID (online supplemental table S4B).

    Physiological changes in SLH

    Table 1 depicts values and effects stratified by 6MWD and SGRQ in SLH (n=108) and substratified in MID achieved/not-achieved.

    View this table:
    Table 1

    Effect in SLH (n=108) (baseline/post/change): (1A) 6MWD-MID (≥30 m) achieved versus not achieved and (1B) SGRQ-MID total score (≤−4 units) achieved versus not achieved

    No significant between-group differences were observed in the 6MWD stratum (table 1). However, we observed a tendency favouring the proportion achieving SGRQ-MID and in physiological variables related to lung function, inspiratory control and function, dyspnoea and breathing control, and heart rate response, although not reaching statistical significance. Several significant within-group differences favouring the proportion achieving MID were further observed in both subgroups (SGRQ, single breath count test, and MIP).

    In the SGRQ stratum (table 1), we observed that the SLH group improved significantly in 6MWD and in physiological variables related to inspiratory control and function and to dyspnoea and breathing control. We observed several within-group changes favouring the proportion achieving MID in variables related to inspiratory control and function and to dyspnoea and breathing control.

    Values and effects for supplementary analyses of the PExT group are available in the supplementary files (online supplemental table S5). Briefly, in those achieving 6MWD-MID (online supplemental table S5A), we observed a tendency towards increased difference in change in QoL. Similarly, in those achieving SGRQ-MID (online supplemental table S5B), we observed a tendency towards improved EID. Compared with the SLH group, we observed fewer significant within-group differences in parameters related to inspiratory control, function, and dyspnoea or breathing control.

    Relationship between SLH and physiological changes in 6MWD and SGRQ MID strata

    The multivariable logistic regression analysis (table 2) included selected variables (oligo variables) based on display of significance in the initial univariable analyses, for each of the two strata: achieved 6MWD-MID (table 2) respectively SGRQ-MID (table 3).

    View this table:
    Table 2

    Univariable and multivariable logistic regression in SLH: baseline factors and change factors (change from baseline to post): factors associated with achieving SLH (6MWD-MID, n=31)

    View this table:
    Table 3

    Univariable and multivariable logistic regression in SLH: baseline factors and change factors (change from baseline to post): factors associated with achieving SGRQ-MID Total Score (n=53)

    Achieving 6MWD-MID was associated with short baseline 6MWD (OR: 6.07; 95% CI 1.4 to 0.5; p=0.01) and older age (OR: 0.13; 95% CI 0.1 to 0.6; p=0.01). We observed no baseline factors associated with achieving SGRQ-MID.

    Concerning changes from baseline to follow-up in physiological parameters, achieving 6MWD-MID was associated with ≥50% improvement in heart rate response, and achieving SGRQ-MID was associated with achieving ≥10% improvement in MIP.

    We found no associations in any study domain in the multivariable models PExT (online supplemental table S6).

    Agreement and association between 6MWD and QoL response

    Table 4 shows that achieving MID in both or neither 6MWD and SGRQ was observed in 57.4% in both the SLH and in the PExT groups, resulting in slight agreement using Cohen’s κ (SLH group: κ=0.14; p=0.14; PExT group: κ=0.11; p=0.32). In both groups, it was numerically more common to perceive an effect without improving 6MWD than to improve both.

    View this table:
    Table 4

    Association between achieving MID in both 6MWD and SGRQ (or in neither/nor) across overall study groups (SLH and PExT)

    Using the Cochran-Mantel-Haenszel test to assess association across overall study groups (SLH and PExT), we observed a tendency towards an association. The chance-corrected proportional agreement between achieving 6MWD-MID and SGRQ-MID is depicted in online supplemental table S7.

    DISCUSSION

    In this post hoc explorative study, we used per-protocol data from our recent RCT12 where we compared SLH with PExT within a 10 weeks community-based PR programme. We found that SLH provided physiological improvement in patients who achieved 6MWD-MID (=physical exercise capacity) and/or SGRQ (=QoL); however, we observed more improvements in those achieving SGRQ-MID. Specifically, SLH was associated with improved MIP and single breath count test. We found no significant overlap and/or close association between achieving 6MWD-MID and/or SGRQ-MID.

    Achieving 6MWD-MID and/or SGRQ-MID in SLH participants

    We observed that less than a third of SLH participants (31/108) achieved 6MWD-MID, whereas almost a half (53/108) achieved SGRQ-MID (table 1). Impact of singing/SLH on exercise capacity has not yet been established, and no previous studies have reported on the proportion of participants achieving MID in walking distance tests.19 36–40 The improvement in SGRQ, though, falls in line with reporting of impact of singing/SLH on QoL in previous studies.3 13 14 41 42 Interestingly, the change found in this study was much larger in the 6MWD stratum and in those achieving 6MWD-MID (61.8 m (SD 41.9)) than in the intention-to-treat analysis of the RCT.12 For the SGRQ stratum, change was also higher (24.8 m (SD 43.2)) but did not reach MID. Regarding SGRQ, however, MID was achieved in both outcomes (6MWD stratum: −6.7 (SD 12.0); SGRQ stratum: −11.8 (SD 7.5)).

    The SLH participants achieving 6MWD-MID had lower BMI, FEV1/FVC ratio, and 6MWD at baseline compared with those who did not achieve MID (online supplemental table S3A). Those achieving SGRQ-MID had lower BMI and lower parameters related to lung function, inspiratory control and function, and dyspnoea control (online supplemental table S4A). Evidently, it is easier to improve from a poorer and more challenged starting point, for example either with a very high or a very low BMI.43 Yet, interestingly, the same pattern was not present in the supplementary analyses of the PExT group, which, notably, however, represented a smaller sample size and, thus, this observation may not be valid. It would be interesting to investigate predictors associated with improvements as this might guide which activity a specific patient phenotype should be referred for and, thus, potentially might help to overcome usual barriers, for example regarding attendance.

    Physiological changes in ‘effective’ SLH

    A key element in singing is a controlled and coordinated breathing pattern with diaphragmatic breathing and extended expiration to support vocalisation.3 10 13 14 42

    The recent narrative review2 suggested that singing may improve aspects in breathing pattern, respiratory control, hyperinflation, dyspnoea, health-related QoL, and interoception. Improved physical capacity and activity has likewise been reported in some previous studies besides enhanced respiratory well-being.20 36 41 44 However, specific physiological changes have not been convincingly confirmed.2 4 20 42 In accordance with formerly posed requests,2 the present study explored whether SLH might be associated with change in any detectable physiological parameters specifically focusing on measures reflecting lung function, inspiratory muscle strength and control, dyspnoea and breathing control, and exercise-induced changes in pulse and saturation.

    Previous studies have reported that studies on singing lack consistency when addressing lung function, perception of dyspnoea, and improved breathing pattern, ranging from self-reported perception of improved lung function to guideline-based measurement of spirometry and inspiratory pressure.2 This lack of consistency in perceptions and clinical effects has also been addressed in previous studies4 20 42 and a more holistic view on effects may be relevant to consider due to the complex nature of SLH and other approaches to singing. For example, the notion of lung function may also need to include evaluation of dyspnoea, MIP and physical capacity.42 Previously, it has been suggested that singing improves lung function9 41 42 which we, however, did not observe in the present study - when measured solely by spirometry.

    Interestingly, in this study, achievement of SGRQ-MID was associated with improved MIP and single breath count test (table 1) which we did not observe in the proportion of patients achieving 6MWD-MID. Furthermore, achieving SGRQ-MID was associated with a more pronounced 6MWD improvement (table 1) than the corresponding improvement in SGRQ observed in patients achieving 6MWD-MID (table 1). Surprisingly, we observed no significant associated physiological changes in PExT neither when achieving 6MWD-MID nor SGRQ-MID (online supplemental tables S5 and S6). This could suggest that SLH might provide more benefits which, however, is only speculative, not at least as the overall study groups differed in size and as it was not the aim of this study to compare SLH and PExT. We are not aware of other PR studies measuring agreement and association between objectively and subjectively defined outcomes, but several previous studies on singing3 4 20 have addressed a discrepancy between physiological and psychosocial benefits and, further, between perceived and clinically observed benefits.

    MIP may express inspiratory muscle strength and control and may be correlated to detect changes in general muscle strength and physical capacity (6MWD).45 MIP has earlier been included in studies of singing and positive effects have been observed in diseases where respiratory function is also profoundly affected (for example cystic fibrosis;46 Parkinson’s disease),47 48 but not in COPD.13 42 This study found significant between-group changes in MIP, however, only in the SGRQ stratum.

    Changes in the single breath count test might be an indication of strength, control, and coordination in the respiratory muscles, tolerance of CO2 retention, efficiency and stability of subglottal pressure, and operating lung volumes.2 In our present study, single breath count test was included to indicate dyspnoea and breathing control and has previously been used in assessment of hyperventilation.19 Positive changes in single breath count test have been reported in some studies of singing in COPD,32 but not all.19 41 42 We observed significant improvements in both MIP and single breath count test in the SGRQ stratum (table 1) suggesting that SLH may improve inspiratory muscle strength and control and may lead to an experience of less dyspnoea and enhanced breathing control. This may be explained by the systematic training of the inspiratory and expiratory muscles during singing and the SLH programme’s focus on prolonging the expiration which may increase tolerance of hypoventilation. This training may induce lower operating volume with lower setting of tidal volume—closer to ideal resting position—and, thus, to reduction of hyperinflation and perception of dyspnoea. In any case, both the MIP and the single breath count tests would be easily implementable and might be considered relevant to supplement standard assessment in COPD.33

    It has been suggested that participants experience that singing/SLH provides similar effects as PExT.24 49 In the present study, we observed an association between achieving 6MWD-MID and improving heart rate response. This may reflect an increase in overall fitness and dynamics which may be in line with a recent study suggesting that physiological demands in SLH correspond to those of ‘brisk pace’ walking, however observed in healthy people.40

    Additional tendencies (in case of exploratory acceptance of p values between 0.05 and 0.10 and/or tendencies related to within-group changes) were observed in the proportion of participants achieving 6MWD-MID regarding measures FEV1, MIP, single breath count, and heart rate response (table 1). More observations and sufficiently powered studies are needed to clarify whether the observed trends are true effects with a type II error or not.

    To sum up, our study does not convincingly support that singing improves lung function as previously indicated. Rather, the study may support previous suggestions that singing/SLH may be associated with improved inspiratory muscle strength and control, dyspnoea and breathing control, and QoL. Furthermore, our study may support previous indications of SLH being associated with improved physical fitness and exercise capacity.

    Strengths and limitations

    The present study has both strengths and weaknesses. Previous studies on singing in respiratory disease have mainly focused on perceived effect, and studies focusing on objective parameters have largely failed to confirm these perceived benefits.1 3 4 20

    Our study was based on data from a large-scale and rigorous RCT with well-described interventions and real-life delivery of community-based PR and with validated and established outcome variables commonly used in PR trials. Data were analysed and reported with transparent and basic methods,12 thus aiming to minimise selection, detection and reporting bias.

    We strived for transparent analyses, reporting and discussion aiming to reduce risk of reporting and publication bias. However, the present study was obviously not powered to detect changes being an explorative study based on post hoc analyses in a selected population and, thus, with low rating in the evidence hierarchy. There are several aspects that may cause measurement and reporting bias. The small and selected population, the difference between overall study group sizes, and potential overexaggerating of findings may lead to type I error. A type II error is also possible due to different samples between the 6MWD and SGRQ strata with a smaller subgroup of participants achieving 6MWD-MID than SGRQ-MID. Furthermore, the study reflected observations from a short-term, proof-of-concept study without long-term data and without potential to address persistence of any of the observed changes. The study did not include comprehensive assessment measurements of advanced lung function measurement,50 for example static lung volumes (total lung capacity, expiratory reserve volume, residual volume), diffusion capacity for carbon monoxide, impulse oscillometry, arterial or capillary blood gas measurement, or helium dilution lung volume measurement. Neither did we include assessment of biomarkers, high-resolution chest CT, body plethysmography or ultrasound-measurement of diaphragmatic thickness or mobility to assess emphysema, hyperinflation, airway resistance, small airways involvement, or diaphragmatic strength. Neither of these are, however, standard in assessment of outcome of PR for COPD yet; however, it would be interesting and relevant to include such parameters in future research on SLH besides testing of physical activity (although challenging to measure),51 EKG, and exercise stress test, for example chair stand test, in future studies.

    The study did not investigate SLH as an add-on to PExT, a combination that may likely be superior to each modality alone in providing benefits and effects and which should also be addressed in future studies. Lastly, several findings and aspects in our study remain to be sufficiently explained and are rather to be regarded as observations. Further studies are needed to investigate these aspects.

    Conclusion

    This study suggests that SLH as part of PR for COPD confers positive physiological changes besides being a pleasant leisure time activity. Future studies focusing on physiology may help us to better understand how singing works and how SLH can be used to improve the lives of patients with COPD. There is also a need to explore the apparent gap between subjective and objective benefits of SLH.

    Data availability statement

    Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information. Consent forms will not be available according to Danish legislation. De-identified data collected for the study will be available from 1 January 2023, upon reasonable request. Contact study investigator (MK), mk@clin.au.dk.

    Ethics statements

    Patient consent for publication

    Ethics approval

    Ethical approval for the overall RCT was obtained by the Regional Committee on Health Research Ethics, Region Zealand, Denmark (no. SJ-597) and the Danish Data Protection Agency (no. REG-049-2017). The trial was conducted in accordance with the Helsinki Declaration and according to the Act on Processing of Personal Data. Trial protocol is available at ClinicalTrials.gov (number NCT03280355).

    Acknowledgments

    The authors thank all study participants for their participation in the overall project. Additional acknowledgements related to the RCT are stated in their previous paper.

    References

    1. ↵
      1. Kaasgaard M,
      2. Andersen IC,
      3. Rasmussen DB, et al
      . Heterogeneity in Danish lung choirs and their singing leaders: delivery, approach, and experiences: a survey-based study. BMJ Open 2020;10:e041700.doi:10.1136/bmjopen-2020-041700pmid:http://www.ncbi.nlm.nih.gov/pubmed/33257493
      OpenUrlAbstract/FREE Full Text
    2. ↵
      1. Lewis A,
      2. Philip KEJ,
      3. Lound A, et al
      . The physiology of singing and implications for 'Singing for Lung Health' as a therapy for individuals with chronic obstructive pulmonary disease. BMJ Open Respir Res 2021;8:e000996.doi:10.1136/bmjresp-2021-000996pmid:http://www.ncbi.nlm.nih.gov/pubmed/34764199
      OpenUrlAbstract/FREE Full Text
    3. ↵
      1. Lewis A,
      2. Cave P,
      3. Stern M, et al
      . Singing for lung Health—a systematic review of the literature and consensus statement. NPJ Prim Care Respir Med 2016;26:16080.doi:10.1038/npjpcrm.2016.80
      OpenUrl
    4. ↵
      1. McNamara RJ,
      2. Epsley C,
      3. Coren E, et al
      . Singing for adults with chronic obstructive pulmonary disease (COPD). Cochrane Database Syst Rev 2017;12:CD012296.doi:10.1002/14651858.CD012296.pub2pmid:http://www.ncbi.nlm.nih.gov/pubmed/29253921
      OpenUrlPubMed
    5. ↵
      1. Gick ML,
      2. Nicol JJ
      . Singing for respiratory health: theory, evidence and challenges. Health Promot Int 2016;31:725–34.doi:10.1093/heapro/dav013pmid:http://www.ncbi.nlm.nih.gov/pubmed/25784304
      OpenUrlCrossRefPubMed
    6. ↵
      1. Salomoni S,
      2. van den Hoorn W,
      3. Hodges P
      . Breathing and singing: objective characterization of breathing patterns in classical singers. PLoS One 2016;11:e0155084.doi:10.1371/journal.pone.0155084pmid:http://www.ncbi.nlm.nih.gov/pubmed/27159498
      OpenUrlPubMed
    7. ↵
      1. Leanderson R,
      2. Sundberg J,
      3. von Euler C
      . Role of diaphragmatic activity during singing: a study of transdiaphragmatic pressures. J Appl Physiol 1987;62:259–70.doi:10.1152/jappl.1987.62.1.259pmid:http://www.ncbi.nlm.nih.gov/pubmed/3558185
      OpenUrlPubMedWeb of Science
    8. ↵
      1. Tamplin J,
      2. Baker FA,
      3. Grocke D, et al
      . Effect of singing on respiratory function, voice, and mood after quadriplegia: a randomized controlled trial. Arch Phys Med Rehabil 2013;94:426–34.doi:10.1016/j.apmr.2012.10.006pmid:http://www.ncbi.nlm.nih.gov/pubmed/23103430
      OpenUrlCrossRefPubMed
    9. ↵
      1. Fancourt D,
      2. Finn S
      . What is the evidence on the role of the arts in improving health and well-being? A scoping review (health evidence network (hen) synthesis report 67). Copenhagen: WHO Regional Office for Europe, 2019.
    10. ↵
      1. Heydon R,
      2. Fancourt D,
      3. Cohen AJ
      . The Routledge Companion to Interdisciplinary Studies in Singing. In: Wellbeing. Part I singing and health. Volume III. 1st ed. Routledge, 2020: 86–97.
      OpenUrl
    11. ↵
      1. Holland AE,
      2. Hill CJ,
      3. Jones AY, et al
      . Breathing exercises for chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2012;10:CD008250.doi:10.1002/14651858.CD008250.pub2pmid:http://www.ncbi.nlm.nih.gov/pubmed/23076942
      OpenUrlCrossRefPubMed
    12. ↵
      1. Kaasgaard M,
      2. Rasmussen DB,
      3. Andreasson KH, et al
      . Use of singing for lung health as an alternative training modality within pulmonary rehabilitation for COPD: an RCT. Eur Respir J 2021:2101142.doi:10.1183/13993003.01142-2021pmid:http://www.ncbi.nlm.nih.gov/pubmed/34625480
      OpenUrlPubMed
    13. ↵
      1. Bonilha AG,
      2. Onofre F,
      3. Vieira ML, et al
      . Effects of singing classes on pulmonary function and quality of life of COPD patients. Int J Chron Obstruct Pulmon Dis 2009;4:1–8.pmid:PMID: 19436683; PMCID: PMC2672787.
      OpenUrlPubMed
    14. ↵
      1. Liu H,
      2. Song M,
      3. Zhai Z-H, et al
      . Group singing improves depression and life quality in patients with stable COPD: a randomized community-based trial in China. Qual Life Res 2019;28:725–35.doi:10.1007/s11136-018-2063-5pmid:http://www.ncbi.nlm.nih.gov/pubmed/30612266
      OpenUrlPubMed
    15. ↵
      1. Panigrahi A,
      2. Sohani S,
      3. Amadi C, et al
      . Role of music in the management of chronic obstructive pulmonary disease (COPD): a literature review. Technol Health Care 2014;22:53–61.doi:10.3233/THC-130773pmid:http://www.ncbi.nlm.nih.gov/pubmed/24398814
      OpenUrlPubMed
    16. ↵
      1. Gebauer L,
      2. Vuust P
      . Music Interventions in Health Care. White Paper. [Internet], 2014. Available: http://www.petervuust.dk/wp-content/uploads/2014/03/whitepaper_digital_enkelsidet_0.pdf
    17. ↵
      1. Stewart NAJ,
      2. Lonsdale AJ
      . It’s better together: The psychological benefits of singing in a choir. Psychol Music 2016;44:1240–54.doi:10.1177/0305735615624976
      OpenUrlCrossRef
    18. ↵
      1. Pentikäinen E,
      2. Pitkäniemi A,
      3. Siponkoski S-T, et al
      . Beneficial effects of choir singing on cognition and well-being of older adults: evidence from a cross-sectional study. PLoS One 2021;16:e0245666.doi:10.1371/journal.pone.0245666pmid:http://www.ncbi.nlm.nih.gov/pubmed/33534842
      OpenUrlPubMed
    19. ↵
      1. Lord VM,
      2. Cave P,
      3. Hume VJ, et al
      . Singing teaching as a therapy for chronic respiratory disease--a randomised controlled trial and qualitative evaluation. BMC Pulm Med 2010;10:41.doi:10.1186/1471-2466-10-41pmid:http://www.ncbi.nlm.nih.gov/pubmed/20682030
      OpenUrlCrossRefPubMed
    20. ↵
      1. Yoeli H,
      2. Macnaughton J
      . 'To more than I can be': a phenomenological meta-ethnography of singing groups for people with chronic obstructive pulmonary disease. Health 2021;25:574–95.doi:10.1177/1363459320978520pmid:http://www.ncbi.nlm.nih.gov/pubmed/33317354
      OpenUrlPubMed
    21. ↵
      1. Rochester CL,
      2. Vogiatzis I,
      3. Holland AE, et al
      . An official American thoracic Society/European respiratory Society policy statement: enhancing implementation, use, and delivery of pulmonary rehabilitation. Am J Respir Crit Care Med 2015;192:1373–86.doi:10.1164/rccm.201510-1966STpmid:http://www.ncbi.nlm.nih.gov/pubmed/26623686
      OpenUrlCrossRefPubMed
    22. ↵
      1. McCarthy B,
      2. Casey D,
      3. Devane D, et al
      . Pulmonary rehabilitation for chronic obstructive pulmonary disease. Cochrane Database Syst Rev 2015;3:CD003793.doi:10.1002/14651858.CD003793.pub3
    23. ↵
      1. Lewis A,
      2. Cave P,
      3. Hopkinson NS
      . Singing for lung health: service evaluation of the British lung Foundation programme. Perspect Public Health 2018;138:215–22.doi:10.1177/1757913918774079pmid:http://www.ncbi.nlm.nih.gov/pubmed/29757080
      OpenUrlCrossRefPubMed
    24. ↵
      1. Lewis A,
      2. Cave P,
      3. Hopkinson NS
      . Singing for lung health: a qualitative assessment of a British lung Foundation programme for group leaders. BMJ Open Respir Res 2017;4:e000216.doi:10.1136/bmjresp-2017-000216pmid:http://www.ncbi.nlm.nih.gov/pubmed/29071079
      OpenUrlAbstract/FREE Full Text
    25. ↵
      1. Holland AE,
      2. Nici L
      . The return of the minimum clinically important difference for 6-minute-walk distance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013;187:335–6.doi:10.1164/rccm.201212-2191EDpmid:http://www.ncbi.nlm.nih.gov/pubmed/23418323
      OpenUrlCrossRefPubMed
    26. ↵
      1. Jones PW
      . St. George's respiratory questionnaire: MCID. COPD 2005;2:75–9.doi:10.1081/COPD-200050513pmid:http://www.ncbi.nlm.nih.gov/pubmed/17136966
      OpenUrlCrossRefPubMedWeb of Science
    27. ↵
      1. Donohue JF
      . Minimal clinically important differences in COPD lung function. COPD 2005;2:111–24.doi:10.1081/COPD-200053377pmid:http://www.ncbi.nlm.nih.gov/pubmed/17136971
      OpenUrlCrossRefPubMed
    28. ↵
      1. Khalil M,
      2. Wagih K,
      3. Mahmoud O
      . Evaluation of maximum inspiratory and expiratory pressure in patients with chronic obstructive pulmonary disease. Egyptian Journal of Chest Diseases and Tuberculosis 2014;63:329–35.doi:10.1016/j.ejcdt.2014.01.010
      OpenUrl
    29. ↵
      1. Sachs MC,
      2. Enright PL,
      3. Hinckley Stukovsky KD, et al
      . Multi-Ethnic Study of Atherosclerosis Lung Study. Performance of maximum inspiratory pressure tests and maximum inspiratory pressure reference equations for 4 race/ethnic groups. Respir Care 2009;54:1321–8.pmid:http://www.ncbi.nlm.nih.gov/pubmed/19796411
      OpenUrlAbstract/FREE Full Text
    30. ↵
      1. Neves LF,
      2. Reis MH,
      3. Plentz RDM, et al
      . Expiratory and expiratory plus inspiratory muscle training improves respiratory muscle strength in subjects with COPD: systematic review. Respir Care 2014;59:1381–8.doi:10.4187/respcare.02793pmid:http://www.ncbi.nlm.nih.gov/pubmed/24782553
      OpenUrlAbstract/FREE Full Text
    31. ↵
      1. McCool FD,
      2. Conomos P,
      3. Benditt JO, et al
      . Maximal inspiratory pressures and dimensions of the diaphragm. Am J Respir Crit Care Med 1997;155:1329–34.doi:10.1164/ajrccm.155.4.9105075pmid:http://www.ncbi.nlm.nih.gov/pubmed/9105075
      OpenUrlCrossRefPubMedWeb of Science
    32. ↵
      1. Engen RL
      . The Singer's breath: implications for treatment of persons with emphysema. J Music Ther 2005;42:20–48.doi:10.1093/jmt/42.1.20pmid:http://www.ncbi.nlm.nih.gov/pubmed/15839731
      OpenUrlCrossRefPubMedWeb of Science
    33. ↵
      1. Kumari A,
      2. Malik S,
      3. Narkeesh K, et al
      . Single breath count: a simple pulmonary function test using a mobile APP. Indian J Thorac Cardiovasc Surg 2017;33:369–70.doi:10.1007/s12055-017-0555-5
      OpenUrl
    34. ↵
      1. MacDonald DM,
      2. Helgeson ES,
      3. Adabag S, et al
      . Chronotropic index and acute exacerbations of chronic obstructive pulmonary disease: a secondary analysis of block COPD. Ann Am Thorac Soc 2021;18:1795–802.doi:10.1513/AnnalsATS.202008-1085OCpmid:http://www.ncbi.nlm.nih.gov/pubmed/33784233
      OpenUrlPubMed
    35. ↵
      1. von Elm E,
      2. Altman DG,
      3. Egger M, et al
      . The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg 2014;12:1495–9.doi:10.1016/j.ijsu.2014.07.013pmid:http://www.ncbi.nlm.nih.gov/pubmed/25046131
      OpenUrlCrossRefPubMed
    36. ↵
      1. Lord VM,
      2. Hume VJ,
      3. Kelly JL, et al
      . Singing classes for chronic obstructive pulmonary disease: a randomized controlled trial. BMC Pulm Med 2012;12:69.doi:10.1186/1471-2466-12-69pmid:http://www.ncbi.nlm.nih.gov/pubmed/23145504
      OpenUrlCrossRefPubMed
    37. ↵
      1. Clift S,
      2. Skingley A,
      3. Price S
      . Singing for better breathing: findings from the Lambeth & Southwark singing and COPD project. Canterbury Canterbury Christ Church University, 2017.
    38. ↵
      1. Cahalan R,
      2. Green J,
      3. Meade C, et al
      . “SingStrong”: Singing for better lung health in COPD – A pilot study. Physiother Theory Pract 2021;63:1–9.doi:10.1080/09593985.2021.1907825
      OpenUrl
    39. ↵
      1. McNaughton A,
      2. Weatherall M,
      3. Williams M, et al
      . Sing your lungs Out-a community singing group for chronic obstructive pulmonary disease: a 1-year pilot study. BMJ Open 2017;7:e014151.doi:10.1136/bmjopen-2016-014151pmid:http://www.ncbi.nlm.nih.gov/pubmed/28119393
      OpenUrlAbstract/FREE Full Text
    40. ↵
      1. Philip KE,
      2. Lewis A,
      3. Buttery SC, et al
      . Physiological demands of singing for lung health compared with treadmill walking. BMJ Open Respir Res 2021;8:e000959.doi:10.1136/bmjresp-2021-000959pmid:http://www.ncbi.nlm.nih.gov/pubmed/34045239
      OpenUrlAbstract/FREE Full Text
    41. ↵
      1. Skingley A,
      2. Page S,
      3. Clift S, et al
      . “Singing for Breathing”: Participants’ perceptions of a group singing programme for people with COPD. Arts Health 2014;6:59–74.doi:10.1080/17533015.2013.840853
      OpenUrl
    42. ↵
      1. Goldenberg RB
      . Singing lessons for respiratory health: a literature review. J Voice 2018;32:85–94.doi:10.1016/j.jvoice.2017.03.021pmid:http://www.ncbi.nlm.nih.gov/pubmed/28461167
      OpenUrlPubMed
    43. ↵
      1. Kerti M,
      2. Balogh Z,
      3. Kelemen K, et al
      . The relationship between exercise capacity and different functional markers in pulmonary rehabilitation for COPD. Int J Chron Obstruct Pulmon Dis 2018;13:717–24.doi:10.2147/COPD.S153525pmid:http://www.ncbi.nlm.nih.gov/pubmed/29535512
      OpenUrlPubMed
    44. ↵
      1. Skingley A,
      2. Clift S,
      3. Hurley S, et al
      . Community singing groups for people with chronic obstructive pulmonary disease: participant perspectives. Perspect Public Health 2018;138:66–75.doi:10.1177/1757913917740930pmid:http://www.ncbi.nlm.nih.gov/pubmed/29160737
      OpenUrlPubMed
    45. ↵
      1. Oancea C
      . Clinical relevance of maximal inspiratory pressure: determination in COPD exacerbation. COPD, 2010: 119.
    46. ↵
      1. Irons JY,
      2. Kenny DT,
      3. McElrea M, et al
      . Singing therapy for young people with cystic fibrosis: a randomized controlled pilot study. Music Med 2012;4:136–45.doi:10.1177/1943862112452150
      OpenUrlCrossRef
    47. ↵
      1. Di Benedetto P,
      2. Cavazzon M,
      3. Mondolo F, et al
      . Voice and choral singing treatment: a new approach for speech and voice disorders in Parkinson's disease. Eur J Phys Rehabil Med 2009;45:13–19.pmid:http://www.ncbi.nlm.nih.gov/pubmed/18987565
      OpenUrlPubMed
    48. ↵
      1. Stegemöller EL,
      2. Radig H,
      3. Hibbing P, et al
      . Effects of singing on voice, respiratory control and quality of life in persons with Parkinson's disease. Disabil Rehabil 2017;39:594–600.doi:10.3109/09638288.2016.1152610pmid:http://www.ncbi.nlm.nih.gov/pubmed/26987751
      OpenUrlPubMed
    49. ↵
      1. Lewis A,
      2. Thomas J
      . Copd and singing for lung health: a patient and clinician perspective. Pulm Ther 2018;4:121–4.doi:10.1007/s41030-018-0063-9pmid:http://www.ncbi.nlm.nih.gov/pubmed/32026394
      OpenUrlPubMed
    50. ↵
      1. Vogelmeier CF,
      2. Criner GJ,
      3. Martinez FJ, et al
      . Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease 2017 report. gold executive summary. Am J Respir Crit Care Med 2017;195:557–82.doi:10.1164/rccm.201701-0218PPpmid:http://www.ncbi.nlm.nih.gov/pubmed/28128970
      OpenUrlCrossRefPubMed
    51. ↵
      1. Rist C,
      2. Karlsson N,
      3. Necander S, et al
      . Physical activity end-points in trials of chronic respiratory diseases: summary of evidence. ERJ Open Res 2022;8:00541-2021–2021.doi:10.1183/23120541.00541-2021pmid:http://www.ncbi.nlm.nih.gov/pubmed/35295234
      OpenUrlAbstract/FREE Full Text

    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • Collaborators Not applicable.

    • Contributors MK (study investigator), UB (principal investigator and guarantor), DBR and OH designed the scope and plan for this study. Statistical analyses and were performed by MK and DBR, and UB and OH gave feedback. MK drafted the manuscript, and UB, DBR, OH, AL and PV provided important intellectual input and feedback and approved the final version of the manuscript.

    • Funding This study was funded, as part of a Danish PhD project, by the Tryg Foundation, ID 111562 (DKK 967,470), the Danish Health Foundation, 18-B-0067 (DKK 200,000), Aase og Ejnar Danielsen’s Foundation, ID 10-001745 (DKK 75,000), The Moller Foundation, ID 16-204 (DKK 40,000), the Danish Lung Foundation, ID 179031-24-03-2017 (DKK 125,000), Naestved, Slagelse and Ringsted Hospitals’ Research Fund (DKK 790,190), Danish Central Region, ID 1-30-72-141-12 (100,000 DKK), Region Zealand, ID 180886, 13-000835 (DKK 314,500), and Aarhus University (DKK 793,727). Grants were used for study investigator MK’s salary, running costs and equipment. Center for Music in the Brain is funded by the Danish National Research Foundation (DNRF117).

    • Competing interests MK holds a Diploma Graduate Degree from the Royal Danish Academy of Music in Voice and Voice Pedagogy. PV is leader of the research centre, Center for Music in the Brain. The other authors had no experience of—or knowledge within—singing.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.