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The physiology of singing and implications for ‘Singing for Lung Health’ as a therapy for individuals with chronic obstructive pulmonary disease

Keir elmslie james philip, phoene cave, juliet russell, nicholas s hopkinson.

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Correspondence to Dr Adam Lewis; [email protected]

Corresponding author.

Received 2021 May 17; Accepted 2021 Oct 20; Collection date 2021.

This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See:  https://creativecommons.org/licenses/by/4.0/ .

Singing is an increasingly popular activity for people with chronic obstructive pulmonary disease (COPD). Research to date suggests that ‘Singing for Lung Health’ may improve various health measures, including health-related quality-of-life. Singing and breathing are closely linked processes affecting one another. In this narrative review, we explore the physiological rationale for ‘Singing for Lung Health’ as an intervention, focusing on the abnormalities of pulmonary mechanics seen in COPD and how these might be impacted by singing. The potential beneficial physiological mechanisms outlined here require further in-depth evaluation.

Keywords: complementary medicine, emphysema, perception of asthma/breathlessness, respiratory muscles

Introduction

Singing has become an increasingly popular approach for people with chronic respiratory disease and chronic obstructive pulmonary disease (COPD) in particular. 1–3 Various types of singing are being used within groups, including those living with respiratory disease, from community choirs with minimal disease-specific content adaptation to ‘Singing for Lung Health’ (SLH). ‘SLH’ incorporates breathing and vocal exercises comparable with those used by respiratory and speech and language therapists to support optimum breathing and vocalising. 4–7 The British Lung Foundation has previously trained approximately 120 singing leaders to run ‘SLH’ groups, and prior to the COVID-19 pandemic, 65 groups were run by these leaders in the UK. 8 Rather than a focus on learning repertoire for performance, a typical SLH session would integrate physical and vocal warm-ups, breathing exercises, relaxation and carefully chosen vocal repertoire all to support breath control. The performance of these components has previously been evaluated, establishing intervention fidelity. 9 In SLH, techniques aim to have physical benefits such as improving the use of respiratory and postural muscles, flexibility, reduced hyperinflation and improved breathing control. For example, participants extend sung phrases with appropriate repertoire and repeat-voiced fricatives performed with biofeedback techniques, which aim to synchronise breath and phonation and match the work of the primary muscles of respiration in a way that supports appropriate vocal effort. 4 ‘SLH’ repertoire intends to have therapeutic impacts, which includes a variety of voice qualities, extended vocal ranges, aiming to improve vocal efficiency and contribute to breath management strategies. 10 These techniques are delivered musically and creatively within the context of promoting full body movement.

‘SLH’ programmes are commonly run at least weekly for at least 6 weeks. There is some evidence to suggest that SLH may be clinically effective—improving quality of life and functional capacity for individuals with COPD. 4 11–17 However, large-scale randomised controlled trial (RCT) data are lacking and the overall research quality in the field has been low to very low as judged by a Cochrane systematic review. 11 Current SLH RCTs in progress are investigating SLH compared with standard care in people with COPD ( NCT04034212 , ISRCTN42943709) or comparing singing as the physical training intervention in pulmonary rehabilitation with the current gold-standard aerobic and strength exercise training in people with COPD ( NCT03280355 ). Multiple systematic reviews have highlighted the need to increase the evidence base for singing, both in relation to clinical effectiveness and underlying physiological impacts related to participation. 4 11

This narrative review was produced by a range of allied health and medical professionals, a singing group leader and vocal coach with a special interest in the field of SLH. The review explores the physiological rationale for SLH as an intervention in COPD, aiming to highlight potential physiological mechanisms requiring further research, focusing on:

The physiology of breathing and singing.

Abnormalities of pulmonary mechanics in COPD.

Potential physiological impact of singing in people with COPD.

We use the term ‘may’ both to raise potential interesting hypotheses for future research in SLH and where uncertainties in the literature remain due to a lack of quality evidence.

The physiology of breathing and singing

Breathing control while singing.

During quiet breathing, inspiration is an active process engaging the muscles of respiration, while expiration is passive, driven largely by lung elastic recoil. During physical activity, as metabolic demands rise, minute ventilation increases by increasing both tidal volume and respiratory rate. This requires increased flow rates and the recruitment of abdominal muscles to deliver active expiration. Regulation of the glottic aperture by laryngeal muscle activity also helps to control ventilation. 18 The glottis widens on inspiration and narrows on expiration. 19 Glottic opening occurs prior to the descent of the diaphragm on inspiration, and the glottis acts as a valve to influence the expiratory time of the respiratory cycle. 20 Therefore, the larynx could be considered a key modulator of expiratory flow. 20

During speech and singing, breath duration and flow rates are controlled to support sound generation by the larynx. Thus, inspiration and expiration are both active in order to adjust lung volumes for phrase length and sound volume. 21 Herbst 10 critiqued the traditional linear relationship of the power-source-filter model, where the sung voice is determined by the lungs and then modified by the larynx and vocal tract. Rather he states that each system and vocal subsystem has a physical effect on the other. In this regard, changes in vocal function will alter exhalation accordingly. Singers partly control exhalation through the activity of the abdominal muscles including the rectus abdominus, internal and external obliques and transverse abdominus. 21 The internal intercostals also work to draw the ribcage during phonation. 21 During speech, inspiratory time is reduced and expiratory time is lengthened (compared with a passive breathing cycle). 22 Subglottic pressure is regulated more actively during speech and singing compared with unphonated breathing and even more so while singing. 23–25

Phonation requires sustaining-controlled exhalation. In a study using electrical impedance tomography, Traser et al 26 show that phonation modulates expiratory airflow in a more uniform pattern compared with unphonated breathing as phonation prevents the majority of air being exhaled at the start of the breath. Zhang 23 reports that subglottal pressures can be maintained throughout exhalation with minimal glottal resistance. This results in the lung volume at the end of the phrase being close to the residual volume. This requires higher expiratory pressures following inspiratory pressures to change lung volumes at this point in lung capacity. The respiratory and vocal mechanisms work synergistically to optimise efficiency in the work of singing.

Lung function parameters in singers

Total lung capacity depends on the balance between inspiratory muscle strength and the elastic recoil of the respiratory system as well as the individual’s size, sex, ethnicity and disease state. Respiratory muscle strength can be improved with specific training 27 28 or as a result of pulmonary rehabilitation. 29 Watson et al 30 studied professional singers comparing singing and non-singing ventilatory tasks. The study found that vocalisation required activation of additional muscles, such as latissimus dorsi, compared with non-singing ventilatory tasks, which may be relevant in relation to respiratory muscle strength. Furthermore, singers have been shown to have forced expiratory volumes and vital capacities greater than population norms. 31–34 Differences in lung function parameters between singers and non-singers likely result from multiple factors, including duration of singing participation 33 ; a propensity for people with pre-existing above-average respiratory function to become singers as is known from other physically demanding professions; and, potentially, lifestyle choices including smoking less and exercising more compared with peers. 34 However, it is speculated that repeated focus on controlled exhaled breath improves expiratory muscle strength. 32

A small study of nine professional singers showed that they were able to dynamically alter vocal fold aperture and abdominal volumes to control their breath. 35 Furthermore, a small study comparing seven classically trained singers to four untrained individuals suggested singers were able to substantially alter the coordination of abdominal and thoracic volume change during singing compared with quiet breathing, by using a greater percentage of abdominal contribution to lung volume change. 36 Solomini et al 36 comment that classically trained singers increase abdominal pressures to enable a more effective expiration by optimising muscular length-tension ratios and force-generation capacity. It is speculated that this is possible because during singing, the anterior diaphragm and ribcage, and the middle and posterior diaphragm and ribcage, act as different functional units. These separate units maintain subglottal pressures with changing recoil forces on expiration. 37

During singing, abdominal muscle activity increases. Macdonald et al 38 investigated the acute effects of singing on abdominal musculature in 25 healthy adults using ultrasound. During singing, the internal oblique and transverse abdominis (TA) muscles both contract and TA has a greater percentage contraction compared with baseline conditions at a comfortable inspiration. Salomoni et al 36 used respiratory inductance plethysmography bands, showing that trained singers use a greater abdominal contribution to change lung volumes during singing compared with untrained controls. It is important to recognise that the majority of singing studies have been conducted on classically trained singers, whose breathing requirements are specific to the style that they sing, and different to contemporary pop or global repertoire, often used in SLH.

Abnormalities in pulmonary mechanics in COPD

COPD encompasses pathologies including chronic bronchitis and emphysema, which alter pulmonary mechanics. 39 Airflow obstruction occurs results from loss of small airways, airway inflammation and wall thickening, mucous hypersecretion, an impaired mucociliary escalator and airway muscle hypertrophy. Additionally, emphysema reduces lung elastic recoil, promoting premature airway closure and gas trapping. The combination of increased airflow resistance and increased lung compliance increases the time constant of lung units and leads to hyperinflation, which worsens with exercise. 40 41 As operating lung volumes increase, the inspiratory muscles develop a mechanical disadvantage with a reduced force generation capacity because of the length–tension relationship as the diaphragm has a shorter, flatter position. 42 43 Inspiratory reserve volume decreases as total lung capacity is approached and the flatter position on the pressure–volume relationship means that the work of inspiration increases. This leads to mechanical constraint on maximum ventilation, recruitment of accessory muscles of respiration, breathlessness and the premature termination of exercise. In addition, skeletal muscle weakness and loss of endurance are common and increase ventilatory demand during daily activities. 44–46 Forty seven per cent of patients with COPD have been shown to have dysfunctional breathing, which is more severe and prevalent than in asthmatics or healthy controls. 47 Furthermore, the Nijmegen Questionnaire score, a measure of hyperventilation syndrome (a type of dysfunctional breathing), is a strong independent determinant of disease-related quality of life in COPD as measured by the COPD Assessment Test. 48 Both the Nijmegen Questionnaire and COPD Assessment Test measure shortness of breath and chest tightness, and to the authors’ knowledge, divergent validity between these measures has yet to be established, which is a potential limitation to Brien et al ’s study. 48 Nevertheless, the findings from both Law et al 47 and Brien et al 48 indicate that breathing pattern retraining is indicated in COPD populations. Breathing pattern retraining has shown to improve physiological outcomes for individuals with COPD, including improvements in functional exercise capacity, respiratory pattern, respiratory rate, lung function, oxygenation, a reduction in dynamic hyperinflation on exertion and functional anatomical dead space volume. 49–55

Potential physiological impact of singing in people with COPD

There is a clear physiological link between the upper airway and lower airway, ventilation and voice quality. 10 It has been stated that dysphonia in COPD can be functional in origin and, therefore, corrected somewhat with therapy. 56

Techniques that slow down expiration allow a greater degree of lung emptying, which in turn lowers operating lung volumes and can make breathing more comfortable for individuals living with COPD. 57 Many breathing retraining techniques focus on slowing down exhalation. Singing activities can be adapted and performed in a similar fashion. In addition, singing may strengthen musculature, improve posture and work as an exercise modality as a structured, repetitive and goal-directed activity, all with potential impacts on symptoms. We explore such possibilities below.

Singing was first documented as a potential therapeutic intervention for individuals with COPD 35 years ago, 58 where it was suggested that singing enabled greater expectoration of sputum and improved blood gasses when the patients took larger breaths to sing. Goldenberg 59 has previously discussed how the increase in airway shear forces and oscillatory action of singing may help expectorate sputum. A further potential therapeutic mechanism is the alteration of breathing patterns for people living with COPD, which has potential clinical utility. 50 Binazzi et al 60 investigated the breathing pattern of people with COPD singing a Christmas carol using optoelectric plethysmography. None of the participants in the study had professional or amateur singing experience. Individuals listened to the Italian version of ‘O Christmas Tree’ once before performing all four verses three times—the third attempt used for analysis. The authors report singers adopted higher operating volumes to maintain adequate expiratory flow generation. Female singers showed greater volume changes in their chest wall, whereas male singers sung with greater abdomen volume changes compared with quiet breathing. In this study, singing altered breathing patterns in patients with COPD and there was wide variability in measured end expiratory chest wall volumes between individuals from a small sample size. It is not known whether the different volume changes between sexes was driven by different body shapes or different keys and registers used in singing the chosen repertoire.

Given that singing requires participants to consciously modulate their breathing patterns, it is plausible that appropriately selected singing repertoire and vocalisation tasks could be used to enable breathing pattern optimisation. Lord et al studied weekly ‘SLH’ training for 12 6 and 8 weeks. 13 Primary outcome measures relating to breath control 12 and physical activity 13 were not met. Though of note, the breath control measures were developed to assess hyperventilation rather than breathing control in COPD; therefore, their value in this context is questionable. However, concerning secondary outcome measures, both studies identified improvements in the physical component score of the SF-36 health status assessment tool. As discussed previously, improving respiratory strength could be useful for people with COPD, and inspiratory muscle strength has been shown to improve with singing for a group of older people, of whom a quarter were living with ‘respiratory disease’. 61 However, further research including individuals diagnosed with COPD is warranted.

An RCT in Brazil, comparing 24 group singing sessions to 24 handcraft work sessions for people with COPD, 62 suggested singing group participants experienced reduced dyspnoea and improved oxygen saturations during singing. However, these changes did not appear to be sustained beyond the end of the 24-week programme.

The perception of severity of breathlessness does not always match the degree of airway pathophysiology in COPD. 63 Herigstad et al 64 demonstrated significant correlations between improvements in how breathless and anxious patients felt following a course of pulmonary rehabilitation and the brain activity of multiple regions according to functional MRI, suggesting a potential role for modifications to interoception. They suggest that becoming breathless in a safe space under supervision may alter the perceptions of breathlessness. Approaches, such as SLH, focus on creating safe, supervised spaces, which may help to explain changes in breathlessness reported by SLH participants. The moderate physical activity of SLH is not only enjoyable, but one where the breath is used to create sound in music collaboratively within a group. The result of such activity can be profound: ‘When we sing, the breath enables creation of something new, promoting life not inhibiting it. It is the barrier that is forgotten, not the breath’. 8

Posture and the voice are coordinated during vocal effort, particularly with the correlation of forward sagittal movement of the trunk at increased sound pressure levels. 65 The ability for the diaphragm to act as a postural control muscle within the trunk is reduced in situations where individuals have increased neural respiratory drive, dead space ventilation and simultaneous arm movements. 66 Evidence suggests that singing challenges postural control and singing training improves postural control. 67 In the study by Peultier-Celli et al , 67 professionally trained singers challenged their balance by standing on a force plate in various conditions, including eyes-open, eyes-closed and singing chosen arias. Singers’ sway was greater when singing compared with standing with eyes open. However, better postural control was observed in those who had more years of singing experience. ‘SLH’ actively trains postural control to support singing. One of the 10 main competencies suggested for trained singing leaders is that they have ‘a holistic understanding of the kinaesthetics and whole body proprioception in breathing’. 9 It is not yet certain how SLH affects posture, but qualitative reports indicate that posture improves through participation 12 with pilot quantitative data, suggesting improvements to balance confidence. 68

‘SLH’ exercises have been compared with different speeds of treadmill walking in a small study in healthy individuals showing that singing is associated with a similar metabolic demand to moderately vigorous physical activity. 69 This study also demonstrated that tidal volumes during singing were greater than those performed for treadmill walking matched for physical activity intensity (Mean Difference: 1.18 L p=0.01), which is likely to relate to the additional volume of air needed for phonation in addition to metabolic requirements, and the phrasing of singing components which necessitated reduced breathing frequency compared with what might have been taken naturally. Further research is required to see if this is reproduced in older people and in people with COPD.

Liuzijue Qigong is a form of traditional Chinese martial art characterised by breathing, which focuses on the use of the primary muscles of respiration (diaphragmatic breathing), pursed-lip breathing and the production of different sounds during limb movements. 70 The physical and vocal warm-up exercises of ‘SLH’ are similar exercises to Liuzijue Qigong. Liuzijue Qigong has been shown to improve maximal inspiratory and expiratory pressures and specific airway conductance in patients with COPD. 70–72 The sounds produced in Liuzijue Qigong are similar to the voiced fricatives used as vocal warm-ups in SLH. Similar to Liuzijue Qigong, many repertoire choices in SLH include long phrases with open vowel sounds. Long phrases and open vowel sounds have been beneficial in reducing respiratory rate and increased heart rate variability via toning and repeated mantra singing. 73–75 Further research is needed to determine the physiological sustained effects once the singing stops. ‘SLH’ exercises also focus on semiocclusion for extended breaths, which also aim to control and support exhalation. ‘SLH’ leaders receive vocal training and toolkits prior to running groups. It is the skill of the trained singing leader to use the wide-ranging research-based techniques sensitively, within the flow of musical activity to engage individuals, making the experience fun and offer a perceived non-clinical environment, which promotes self-expression. The weekly repetition of exercises and games aim to reinforce the ability to use these techniques independently as self-management strategies.

Table 1 details the actions of singing and the potential mechanisms of benefit for individuals with COPD:

Singing actions and proposed/potential physiological basis of benefits for individuals with COPD

COPD, chronic obstructive pulmonary disease; SLH, Singing for Lung Health.

Table 1 highlights potential physiological benefits of singing for individuals with COPD. However, due to both the lack of high-quality evidence and relatively few studies specific to singing training which is not classically derived or studies specific to SLH, more definitive associations and causality statements cannot currently be made between physiological studies in COPD, singing and the practice of SLH. The findings from small studies in classically trained singers to date have limited external validity compared with the breath management required from different repertoire and training, such as pop singing, where singers move from speech, to belt-type singing and falsetto. The breath demands will vary accordingly. Herbst 10 provides a good review of how different voice subsystems contribute to breath support, which we do not cover in this review.

Recommendations from previous systematic reviews remain, 4 11 where more research is required in order to establish the clinical effectiveness and physiological mechanisms underpinning any beneficial effects achieved through SLH participation. Table 2 provides some research questions and types of clinical studies which are now required in order to further explore the physiological mechanisms of potential benefit and clinical effectiveness of SLH:

Physiological research questions and proposed clinical effectiveness studies required in SLH

COPD, chronic obstructive pulmonary disease; PR, pulmonary rehabilitation; SLH, Singing for Lung Health.

This review is specifically focused on physiological rationale and outcomes. However, we acknowledge that SLH is an intervention, which aims to provide holistic health benefit. Any health-related benefits, resulting from participation, are likely multifactorial with psychological and social components, which are known to be important in COPD. 12 16 68 76 77 Further research should continue to use a range of biopsychosocial outcomes in order to evaluate the different mechanisms of benefit effectively.

Breathing and singing are intimately related. There is a good theoretical rationale to support the therapeutic use of singing for people with COPD as a method of improving physiological parameters and breath control; however, the research in this area is limited and of generally low quality. Further research is required to more effectively assess the impact of SLH for people with COPD, and which physiological mechanisms underlie any improvements observed.

Acknowledgments

AL would like to thank Dr Mandy Jones and Professor Joy Conway for their support during this work.

Contributors: AL prepared the first draft of the manuscript. All other authors contributed to revisions and reviewed the final version.

Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

Competing interests: AL, PC and JR train singing leaders to run Singing for Lung Health groups specifically for individuals living with respiratory disease.

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

Data availability statement

No data are available. Not applicable.

Ethics statements

Patient consent for publication.

Not applicable.

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The Effectiveness of Singing or Playing a Wind Instrument in Improving Respiratory Function in Patients with Long-Term Neurological Conditions: A Systematic Review

Address correspondence concerning this article to Kexin Ang, MBBS, MMed (Int Med), MRCP (UK), Department of Neurology, National Neuroscience Institute, Singapore, 11 Jalan Tan Tock Seng, Singapore 308433. Phone: (65) 6357–7153. E-mail: [email protected]

The authors would like to thank Christina Ramsenthaler and Lim Ming Yi for their advice on earlier drafts, Diogo Branco for his help with translating the Portuguese study, “Função fonatória em pacientes com doença de Parkinson: uso de instrumento de sopro,” and Juliana Rosa, Marlene Wiens, and Jeanette Tamplin for patient clarificationson their papers.

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Kexin Ang, Matthew Maddocks, Huiying Xu, Irene J. Higginson, The Effectiveness of Singing or Playing a Wind Instrument in Improving Respiratory Function in Patients with Long-Term Neurological Conditions: A Systematic Review, Journal of Music Therapy , Volume 54, Issue 1, 1 March 2017, Pages 108–131, https://doi.org/10.1093/jmt/thx001

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Many long-term neurological conditions adversely affect respiratory function. Singing and playing wind instruments are relatively inexpensive interventions with potential for improving respiratory function; however, synthesis of current evidence is needed to inform research and clinical use of music in respiratory care.

To critically appraise, analyze, and synthesize published evidence on the effectiveness of singing or playing a wind instrument to improve respiratory function in people with long-term neurological conditions.

Systematic review of published randomized controlled trials and observational studies examining singing or playing wind instruments to improve respiratory function in individuals with long-term neurological conditions.

Articles meeting specified inclusion criteria were identified through a search of the Medline, Embase, PsycINFO, Cochrane Library, CINAHL, Web of Science, CAIRSS for Music, WHO International Clinical Trials Registry Platform Search Portal, and AMED databases as early as 1806 through March 2015. Information on study design, clinical populations, interventions, and outcome measures was extracted and summarized using an electronic standardized coding form. Methodological quality was assessed and summarized across studies descriptively.

From screening 584 references, 68 full texts were reviewed and five studies included. These concerned 109 participants. The studies were deemed of low quality, due to evidence of bias, in part due to intervention complexity. No adverse effects were reported. Overall, there was a trend toward improved respiratory function, but only one study on Parkinson’s disease had significant between-group differences.

The positive trend in respiratory function in people with long-term neurological conditions following singing or wind instrument therapy is of interest, and warrants further investigation.

Many long-term neurological conditions (LTNCs) adversely affect respiratory function, with pathology anywhere along the central and peripheral nervous system ( Mangera, Panesar, & Makker, 2012 ). A decline in respiratory function is an important negative prognostic indicator ( Hussain, Adams, Allgar, & Campbell, 2014 ; Perrin, Unterborn, Ambrosio, & Hill, 2004 ). Respiratory muscle weakness results in inadequate lung volumes and reduced ventilation, which in turn results in impairment of gas exchange, carbon dioxide retention, hypoxemia, and eventually respiratory failure ( Goyal & Mozaffar, 2014 ). Respiratory muscle strength is also vital for airway clearance, generating effective coughing ( Chang, 2006 ), which if left untreated, results in respiratory failure by secretion retention, chronic aspiration, and pneumonia ( Perrin et al., 2004 ). In Amyotrophic Lateral Sclerosis, which is referred to as an LTNC, respiratory failure is the usual cause of death ( Radunovic, Annane, Rafiq, & Mustfa, 2013 ). Many with Duchenne Muscular Dystrophy, the most common inherited progressive myopathy, die from respiratory failure ( Perrin et al., 2004 ; Rodger et al., 2014 ). In cervical spinal cord injury (SCI), the incidence of respiratory failure is as high as 83% ( Lemons & Wagner, 1994 ), and in Parkinson’s disease, aspiration pneumonia is a leading cause of death ( Mehanna & Jankovic, 2010 ).

The standard treatment options for respiratory insufficiency in people with LTNCs include salivation inhibition, secretion clearance, cough-assist techniques, and physical therapy, including inspiratory and expiratory muscle training ( Perrin et al., 2004 ; Smeltzer, Levietes, & Cook, 1996 ). In addition, assistance for ventilation using non-invasive positive pressure ventilation is offered to patients with advanced neuromuscular diseases and sleep-disordered breathing caused by nocturnal hypoventilation ( Goyal & Mozaffar, 2014 ; Perrin et al., 2004 ).

The training of inspiratory and/or expiratory muscles is collectively known as respiratory muscle training (RMT). RMT may increase inspiratory and expiratory muscle strength in LTNCs ( Pollock, Rafferty, Moxham, & Kalra, 2013 ; Reyes, Ziman, & Nosaka, 2013 ), including spinal cord injury ( Berlowitz & Tamplin, 2013 ; Van Houtte, Vanlandewijck, & Gosselink, 2006 ). This is based on the premise that respiratory muscles, being skeletal muscles, can be trained similarly to other peripheral skeletal muscles, by overcoming resistance. Training conducted at high load and low speed of contraction promotes the gain in muscle strength ( Romer & McConnell, 2003 ), enhancing the number and volume of the muscle fibers (hypertrophy) ( Pinto & de Carvalho, 2014 ). The duration and frequency of the training sessions establishes the time and magnitude of muscle response ( Pinto & de Carvalho, 2014 ), and levels of strength often return to baseline when the training stimulus is removed ( Hoffman, 2014 ).

Resistance-training-induced changes within the nervous system, referred to as neural adaptation ( Sale, 1988 ), are another plausible mechanism for improvement in volitional muscle strength. Changes include increased motor unit recruitment and synchronization, and enhanced muscular coordination ( Berlowitz & Tamplin, 2013 ; Sale, 1988 ; Sapienza & Wheeler, 2006 ). Musical experiences can promote neural adaptation. Singing training, considered to be a form of RMT, requires strong and fast inspirations, and extended, regulated expirations ( Berlowitz & Tamplin, 2013 ). Playing a wind instrument, which includes brass and woodwind instruments, for instance a harmonica, also mimics RMT, via its concept of inspiration and expiration through a device providing resistance ( Alexander & Wagner, 2012 ).

Breathing retraining techniques such as pursed-lip breathing and diaphragmatic breathing aim to reduce the work of breathing, and improve chest wall motion and ventilation distribution. These have been combined with RMT in patients with stroke ( Sutbeyaz, Koseoglu, Inan, & Coskun, 2010 ) and Myasthenia Gravis ( Fregonezi, Resqueti, Guell, Pradas, & Casan, 2005 ), with subsequent improvements in respiratory muscle strength. Not only is singing a form of RMT, but it also incorporates breathing retraining by maintenance of good posture and diaphragmatic breathing, and glossopharyngeal breathing by encouraging thoracic expansion ( Irons, Petocz, Kenny, & Chang, 2014 ). Glossopharyngeal breathing increases vital capacity (VC) ( Metcalf, 1966 ; Nygren-Bonnier et al., 2009 ) through a repetitive process that stretches the thoracic cage. Mouth and pharyngeal muscles are used in glossopharyngeal breathing to propel small volumes of air through the larynx into the lower airways; the glottis is used to trap air in the lung until the next breath is taken; this process is repeated until a satisfactory breath is obtained. Efficient use of singers’ lung capacity is optimized by diaphragmatic breathing engaging the intercostal and abdominal muscles for deep inhalation and slow exhalation ( Irons, Kenny, & Chang, 2010 ), as well as singing wide pitch ranges, ranges in sound volume known as dynamics, and long musical phrases with consequent long breath holding ( Collyer, Kenny, & Archer, 2009 ; Sundberg, 1987 ).

Singing and playing wind instruments are relatively inexpensive and enjoyable ( Stacy, Brittain, & Kerr, 2002 ) adjunct interventions with potential for improving respiratory function. This systematic review aimed to critically appraise, analyze, and synthesize published evidence on the effectiveness of singing or playing a wind instrument in improving respiratory function in patients with LTNCs. Through the findings obtained, it is intended to consider if a bigger role can be played by music in respiratory care for people with LTNCs, through music therapists improving respiratory function, setting up therapeutic choirs and music performing groups, or other non-performance-based treatment such as individual vocal instruction.

Study Inclusion and Exclusion Criteria

We considered all study designs, as it was anticipated that few randomized controlled trials would be available. All human participants with long-term neurological conditions were included. There were no restrictions, including age. An LTNC was defined according to the UK Department of Health definition, as a condition resulting from disease of, injury, or damage to the body’s nervous system that will affect the individual and their family for the rest of their life (Team, DH Long-Term Conditions NSF, 2005 ). LTNCs include spinal cord injury, multiple sclerosis, motor neurone disease, and Parkinson’s disease, and a complete list is shown in Appendix 1. The heterogeneity (i.e., dissimilarity in characteristics) of the different study populations was considered as part of the quality assessment. Studies with mixed populations were included if a subgroup analysis for patients with LTNCs was available in the primary publication.

All studies in which singing or playing of wind instruments was used and respiratory function was assessed were included. Objective measures of respiratory function were considered: (i) maximal inspiratory pressure (MIP) or maximal mouth-inspiratory force (MIF) (measured in centimeters of water, cm H2O, or kilopascal, kPa), (ii) maximal expiratory pressure (MEP) or maximal mouth-expiratory force (MEF), both measured in cm H2O or kPa, (iii) sniff nasal inspiratory pressure (SNIP, cm H2O or kPa), and (iv) spirometric measures such as forced expiratory volume in one second (FEV1, liter, (l)), forced vital capacity (FVC, l), and vital capacity (VC, l).

There was no language restriction. Publications without original data such as reviews, discussion papers, editorials, or book chapters were excluded. The eligibility criteria were piloted and refined to minimize bias when selecting studies.

Search Methods for Study Identification

Electronic databases covering different specialisms ensured a diverse and comprehensive search: Medline (1946 to March 23, 2015); Embase (1947 to Week 12, 2015); PsycINFO (1806 to March, Week 3, 2015); Cochrane Library (March 23, 2015); Cumulative Index to Nursing and Allied Health Literature (CINAHL) (1982 to March 24, 2015); Web of Science (March 24, 2015); Computer Assisted Information Retrieval Service System (CAIRSS) for Music (March 24, 2015); World Health Organization International Clinical Trials Registry Platform Search Portal (March 24, 2015); and Allied and Complementary Medicine Database (1985 to March 26, 2015).

The search strategy was adapted from Cochrane reviews of similar studies ( Bradt & Dileo, 2014 ; Irons et al., 2014 ), and final search terms are as shown in Appendix 1. Reference lists and cited references for all included studies and conference abstracts were searched. Hand-searching was not done, as initial hand-searches did not yield any additional evidence.

Selection of Studies, Data Extraction, and Synthesis

Studies were selected based on the predetermined inclusion criteria. A record of both the study and the reason for exclusion was kept. When there was insufficient information to make a decision, the organizations or authors were approached if contact details were available. If authors could not be contacted, we recorded the references as “unable to obtain further information required to make assessment” and excluded the studies.

Data extraction errors were minimized using an electronic standardized coding form that included adverse effects and assessment of quality. The pilot and subsequent use of the electronic standardized coding form ensured that only necessary data was extracted, and that there was consistent completion and ease of analysis. The forms were also checked for accuracy and completeness. The study authors were contacted, where possible, for missing information.

Study selection and data extraction were done by only one researcher (the first author). Due to the diversity in the included studies, meta-analysis was not considered appropriate and a narrative synthesis was completed.

Assessment of Risk of Bias

Methodological quality of included studies was judged quantitatively and qualitatively using the quality assessment tool for quantitative studies ( Thomas, 2003 ). This considered the risk of bias in selection of sample, study design, measurement of outcomes (information bias), follow-up rate, data analysis, implementation of intervention (including presence of co-interventions), and level of reporting.

Results of the Search

A total of 584 references were retrieved by the electronic searches, and 68 were considered as potentially eligible after screening. Upon reviewing full texts, five publications were included in this review ( Figure 1 ).

Study flow diagram

Included Studies

A total of five studies involving 109 participants were included, and characteristics are summarized in Table 1 . Two were randomized controlled trials (RCTs) ( Tamplin et al., 2013 ; Wiens et al., 1999 ), and three were pretest/posttest quasi-experimental studies ( Brim, 1951 ; Di Benedetto et al., 2009 ; Rosa et al., 2009 ). Two studies concerned adults with Parkinson’s disease ( Di Benedetto et al., 2009 ; Rosa et al., 2009 ), while the remaining three involved adults with quadriplegia ( Tamplin et al., 2013 ), multiple sclerosis ( Wiens et al., 1999 ), or children with post-respirator poliomyelitis ( Brim, 1951 ). Four studied the effectiveness of singing interventions ( Brim, 1951 ; Di Benedetto et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ), while the fifth studied the playing of a wind instrument (a recorder) ( Rosa et al., 2009 ). Three of the singing interventions were delivered with participants in a group ( Brim, 1951 ; Di Benedetto et al., 2009 ; Tamplin et al., 2013 ), as opposed to one-on-one ( Wiens et al., 1999 ). All the interventions were made up of different components, and spanned at least 12 weeks. Four studies incorporated physical therapy ( Brim, 1951 ; Di Benedetto et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ), for which three specifically mentioned that these included respiratory training exercises ( Di Benedetto et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ). Pooling of the data for meta-analysis was not deemed possible due to the wide differences between studies.

Characteristics of included studies

ASIA: American Spinal Injury Association; EDSS: Expanded Disability Status Scale; FEV1: forced expiratory volume in 1 second; LTNC: long-term neurological condition; SD: standard deviation; UPDRS: unified Parkinson’s disease rating scale

Risk of Bias in Included Studies

Methodological quality of studies was generally low since each study had component ratings that indicated high risk of bias, a cause of inaccuracy in research ( Thomas, 2003 ), as summarized in Table 2 and as particularized in Table 1 and in the paragraph below. Four studies ( Di Benedetto et al., 2009 ; Rosa et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ) were judged to be of higher quality than the fifth ( Brim, 1951 ), though all were deemed low in quality.

Component ratings on methodological quality based on the quality assessment tool for quantitative studies (Thomas, 2003)

1: strong; 2: moderate; 3: weak

In terms of sample selection, four studies ( Brim, 1951 ; Rosa et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ), had evidence of volunteer bias ( Warden, 2015 ) from high refusal rates from potential participants (the refusal rates were deciphered either through the reviewed studies or by contacting the authors; see Table 1 ), which suggests that study participants are not representative of the target population. The three quasi-experimental studies ( Brim, 1951 ; Di Benedetto et al., 2009 ; Rosa et al., 2009 ), lacking random assignment, were considered to have high risk of bias from study design ( Tamplin et al., 2013 ; Wiens et al., 1999 ). Notwithstanding the above, all were judged to have low risks of bias from data collection, as they used standard equipment for measurement of respiratory function. All but one study ( Di Benedetto et al., 2009 ; Rosa et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ) described an adequate follow-up rate of at least 80%. All but one ( Brim, 1951 ; Di Benedetto et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ) included physical therapy, a potential co-intervention. Finally, all were potentially biased, as they were likely underpowered (lowered probability that the study will correctly test its hypothesis) due to a small sample size, and/or had inadequate reporting of information provided in the publication, making it difficult to eliminate the possibility of bias.

Outcome Measures

The primary outcomes used in this review were increments, and thereby improvements in MEP, MIP, and VC. MEP and MIP were measured in three studies ( Di Benedetto et al., 2009 ; Tamplin et al., 2013 ; Wiens et al., 1999 ), and the third study ( Tamplin et al., 2013 ) also measured VC. In the other two studies ( Brim, 1951 ; Rosa et al., 2009 ), the primary outcome was improvement in VC. The results of the primary outcomes are summarized in Tables 3a (randomized controlled trials) and 3b (pretest/posttest quasi-experimental studies).

Primary outcomes of the Randomized Controlled Trials

CG: control group; IG: intervention group; MEP: maximum expiratory pressure; MIP: maximum inspiratory pressure; SD: standard deviation; VC: vital capacity. Data are expressed as mean (SD). Units for MEP and MIP are in centimeter of water (cm H2O), and units for VC are in liters (l).

Primary outcomes of the pretest/posttest quasi-experimental studies

Data are expressed as mean (SD). MEP: maximum expiratory pressure; MIP: maximum inspiratory pressure; SD: standard deviation; VC: vital capacity. Units for MEP and MIP are in centimeter of water (cm H2O), and units for VC are in liters (l).

Effectiveness

Voice and Choral Singing Treatment (VCST) delivered as group therapy to patients with Parkinson’s disease ( Di Benedetto et al., 2009 ) resulted in a statistically significant increase in their mean MEP and MIP, by 20.5 cm H20 and 7.4 cm H2O, respectively. Improvements in mean MEP and MIP were not statistically significant in both controlled trials in other populations ( Tamplin et al., 2013 ; Wiens et al., 1999 ), when compared with controls. Although the patients with Parkinson’s disease were older than participants in the other studies ( Table 1 ), they had higher baseline mean MEP and MIP (128.5 cm H20 and 73.4 cm H20). The respective increments were 13.3 cm H20 and 5.4 cm H20 (mean baseline 73.3 cm H20, 83.5 cm H20) in the patients with quadriplegia ( Tamplin et al., 2013 ), and 2.9 cm H20 and 4.2 cm H20 (mean baseline 29.8 cm H20, 36.8 cm H20) in the patients with Multiple Sclerosis ( Wiens et al., 1999 ). The patients with quadriplegia were prescribed 36 hours for the intervention, while the patients with Multiple Sclerosis had up to 18 hours, as opposed to the VCST group, with the longest total of 46 hours. Mean FEV1 % predicted was higher at 106.5% in the VCST group, indicating a less severe respiratory impairment, than in the patients with quadriplegia ( Tamplin et al., 2013 ) (63%).

The other two studies ( Brim, 1951 ; Rosa et al., 2009 ) measured VC, which increased with intervention. The two adults with Parkinson’s disease who played the recorder ( Rosa et al., 2009 ) had a mean increase of 0.40 liters (l). VC was also measured in the RCT involving patients with quadriplegia ( Tamplin et al., 2013 ), but the increment of 0.17l in the intervention group was not statistically significant.

This systematic review identified five studies, consisting of 109 participants, generally reporting a trend of improvement in respiratory function for people with LTNCs who took part in singing or wind instrument interventions. No adverse effects were reported.

Only one quasi-experimental pretest/posttest study on group Voice and Choral Singing Treatment on 20 patients with Parkinson’s disease ( Di Benedetto et al., 2009 ) observed statistically significant improvements in mean MEP and MIP. Had the authors used a criterion for clinical significance (such as of 10 cm H20 improvement in MEP and MIP, as in the randomized trial in people with Multiple Sclerosis ( Wiens et al., 1999 ), these results might not be considered clinically significant (i.e., of practical significance to patients). The clinically significant difference of other outcome measures such as VC is unknown too, as is the timing of measurement post intervention. Further, it is not known if such improvements result in functional outcomes, such as reduction of aspiration and pneumonia.

Although studies were of low quality, this is underlined by the complexity of the intervention, in which there are separate elements each essential for optimal functioning ( Campbell et al., 2000 ), with each essential element known as an “active ingredient.” A complex intervention also makes it difficult, if not impossible, for participants to be blinded, although their outcome assessors could be blinded to group allocation. Larger numbers would be required for an adequately powered RCT, but the difficulty in recruitment is underscored by high participant refusal rates. High refusal rates and the recording of refusal rates are important, especially in the context of pilot studies and clinical trials, to enable improvement of study design to achieve better participation rates in future studies. The varied “active ingredients” and intervention dosages and duration studied also highlight further gaps in knowledge on what the optimal intervention should include: active ingredients such as singing or wind instrument playing, one-to-one or in a group, personalized or not, type of music, patient music preference, types of vocal or blowing exercises, and aside from active ingredients, their dose, frequency, and duration. Questions also remain as to which patients benefit the most, the stage of disease to introduce the intervention (timing of intervention), and timing of data collection such that meaningful differences can be detected. The variety in disease subgroups compounded by their different extents of within-subgroup neurological and respiratory impairment further limits the generalizability of the findings. Finally, the varied follow-up period and level of reporting, especially regarding assessing and maintaining intervention fidelity and adherence ( Robb, Burns, & Carpenter, 2011 ), raise questions on whether there could be more significant improvements in respiratory function.

With regard to the effects of singing or playing a wind instrument on respiratory function in conditions other than LTNCs, singing interventions were also found to maintain or improve respiratory muscle function in people with chronic obstructive pulmonary disease ( Bonilha, Onofre, Vieira, Prado, & Martinez, 2009 ), emphysema ( Engen, 2005 ), and asthma ( Wade, 2002 ). There is, however, a paucity of reviews on singing interventions, and no other studies could be found on playing of the recorder. A Cochrane review on singing interventions in bronchiectasis did not find any eligible trial ( Irons et al., 2010 ), whereas its review on patients with cystic fibrosis ( Irons et al., 2014 ) only found one RCT. This RCT also found a positive trend in respiratory function, with post-intervention MEP higher in the singing group, though no significant difference for any of the other respiratory function parameters was found ( Irons, Kenny, McElrea, & Chang, 2012 ).

The positive trend in respiratory function is promising, and no harm was reported. The psychological effects of music are well known, although they were not addressed in the studies included in this systematic review. Music reduces anxiety and may contribute to social health through the management of self-identity and interpersonal relationships ( Bradt & Dileo, 2014 ; Stacy et al., 2002 ). Not only can singing improve mood, it can also alter the perception of pain ( Kenny & Faunce, 2004 ). Music in the form of distractive auditory stimuli was an effective attention-diverting strategy reducing breathlessness during exercise, such that participants could perform exercise at higher intensities, and for longer periods of time ( De Peuter et al., 2004 ). Music also motivated participants with asthma to be compliant to breathing exercises that incorporated singing or music ( Fukuda, 2000 ). Music therapy interventions, if held in groups, can be a social activity that connects individuals with disabilities ( Tamplin, Baker, Grocke, & Berlowitz, 2014 ). Group singing in a choir not only provides peer support, but could increase confidence, enhance mood, and increase motivation ( Tamplin, Baker, Jones, Way, & Lee, 2013 ).

Potential Biases in the Review Process

There is a possibility of missing studies with negative data, as positive studies are more likely to have been published. Authors of included studies were asked to check the list of included studies to identify any known missing or unpublished studies, but this strategy did not yield any additional studies.

Data extraction was carried out alone, and cross-checking for inclusion criteria of studies or inter-rater reliability for trial selection was not possible. Subjective decisions and differences during data extraction and analysis could not be discussed. Hand-searching was not done, and therefore very recent publications that have not yet been included and indexed, articles from journals that are not indexed, or inaccurate indexing by electronic databases might have been missed ( Centre for Reviews and Dissemination University of York, 2009 ).

Implications for Practice

The initial evidence as measured by MEP, MIP, and VC, in patients with LTNCs via singing or wind instrument interventions, shows a trend of improvement in respiratory function, which is promising. However, the evidence on the whole to support or refute this proposition conclusively is insufficient.

Implications for Research

There are gaps in knowledge on what an optimal intervention should include: singing or wind instrument playing; one-to-one or in a group; personalized or not; type of music; patient music preference; types of vocal or blowing exercises; and their dose, frequency, and duration. Questions also remain as to which patients benefit the most, the stage of disease to introduce the intervention (timing of intervention), and timing of data collection such that meaningful differences can be detected. These gaps in knowledge would inform variables to be controlled/standardized and comparison criteria for the control group.

Ultimately, methodologically robust research in this area is missing and needs to be undertaken. Although trial participants could not be blinded to their group allocation, outcome assessors should be blinded where feasible. Larger numbers of patients than used in studies to date would be required for an adequately powered trial, and these data can inform future sample size calculations. Expected advances in technology should reduce information bias further. The level of reporting ought to increase with greater awareness of reporting guidelines for music-based interventions ( Robb et al., 2011 ), and inform design and implementation, including assessment and maintenance of fidelity and adherence specific to singing or wind instrument therapies.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflicts of interest: None declared.

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LTNC: long-term neurological condition

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