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Open Access

Peer-reviewed

Research Article

Accessory respiratory muscles performance among people with spinal cord injury while singing songs with different musical parameters

  • Muhammad Imran Ramli ,

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Software, Writing – original draft, Writing – review & editing

    imranramli@um.edu.my

    Affiliation Department of Biomedical Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯
  • Nur Azah Hamzaid,

    Roles Conceptualization, Methodology, Supervision, Validation, Writing – review & editing

    Affiliation Department of Biomedical Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯
  • Julia Patrick Engkasan,

    Roles Conceptualization, Methodology, Supervision, Writing – review & editing

    Affiliation Department of Rehabilitation Medicine, Faculty of Medicine, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯
  • Juliana Usman,

    Roles Supervision, Writing – review & editing

    Affiliation Department of Biomedical Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯
  • Marzelan Salleh,

    Roles Methodology, Supervision, Writing – review & editing

    Affiliation Department of Music, Faculty of Creative Arts, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯
  • Wee Duen Hueh

    Roles Formal analysis, Methodology, Writing – original draft, Writing – review & editing

    Affiliation Department of Biomedical Engineering, Faculty of Engineering, Universiti Malaya, Kuala Lumpur, Malaysia

    ⨯

Abstract

People with spinal cord injury (SCI) experience respiratory dysfunctions which include hypersecretions, bronchospasm, and respiratory muscles weakness. Singing therapy has been implemented as part of respiratory muscle training (RMT) to improve their muscle strength. Singing different types and genres of songs may elicit specific recruitment of respiratory muscles, attributed to the variation of the songs’ characteristics including tempo, pitch, and rhythmic complexity. This study aims to determine the effect of singing songs with different characteristics on the accessory respiratory muscle performance among people with SCI. Thirteen male SCI participants of ASIA A and B (C4 –T11) were recruited. Respiratory muscle signals were retrieved by placing two mechanomyography (MMG) sensors on the sternocleidomastoid (SCM) and rectus abdominis (RA) muscles. Eight music experts categorized several songs into four categories based on their pitch, tempo, and rhythmic complexity. Each participant sang one song from each category. Findings showed statistically significant difference in RA and SCM responses among all categories (P < 0.01). The SCM muscle is most active while singing high pitch songs. While the RA is most active during slow tempo and easy rhythmic complexity. This shows that different accessory respiratory muscle is activated by people with SCI while singing songs with different characteristics. Clinicians could benefit from this knowledge while prescribing singing therapy or exercise among people with SCI in the future.

Citation: Ramli MI, Hamzaid NA, Engkasan JP, Usman J, Salleh M, Hueh WD (2024) Accessory respiratory muscles performance among people with spinal cord injury while singing songs with different musical parameters. PLoS ONE 19(7): e0305940. https://doi.org/10.1371/journal.pone.0305940

Editor: Sahreen Anwar, Lahore University of Biological and Applied Sciences, PAKISTAN

Received: March 28, 2023; Accepted: June 8, 2024; Published: July 5, 2024

Copyright: © 2024 Ramli et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The data has been uploaded in the repository Dryad, where the data is in open access. Anyone with the link can access the data. Below is the DOI number. DOI: 10.5061/dryad.41ns1rnnk.

Funding: The first author, Muhammad Imran Ramli, received scholarship from Skim Latihan Akademik Bumiputera under Ministry of Higher Education Malaysia. The funder played a role as a scholarship for the first author in his Ph.D. study.

Competing interests: The authors have declared that no competing interests exist.

Introduction

During quiet breathing, the inspiratory muscles (diaphragm and external intercostals) expand the thoracic cavity causing air to fill the lungs. This is followed by passive recoil of the chest wall during expiration. However, during heightened physical activities, accessory respiratory muscles are activated to keep up with the higher oxygen demand. These muscles include sternocleidomastoid, the scalenus, latissimus dorsi, and the abdominal muscles.

People with spinal cord injury (SCI) often have symptoms of respiratory insufficiency, particularly those with injury involving the cervical and thoracic region [1, 2]. The higher the level of lesion, the more respiratory muscles are impaired causing significant respiratory impairments. After SCI, the motor pathways that innervate the muscles of respiratory are disrupted, leading to muscle weakness, spasticity, and paralysis [3]. People with SCI also suffer from impairment of respiratory motor control [4], limiting the recovery [5, 6] and quality of life [7].

Currently, clinicians and researchers have adopted several exercises to improve the respiratory muscles strength among people with SCI. This exercise is called respiratory muscle training (RMT) and includes exercises for inspiration, expiration or both of a certain duration and intensity to improve the strength and endurance of the muscles of respiration [8]. RMT includes resistive load training [9–12], pressure threshold loading training [13–16], normocapnic hyperpnea training [17–20], and singing training [21].

Utilizing singing as a training strategy to improve muscle strength among people with SCI is relatively new among researchers and clinicians compared to other conventional exercises. Singing has been shown to improve the respiratory strength, endurance and quality of life in many populations, such as degenerative speech/voice disorder [22–25], chronic obstructive pulmonary disease (COPD) [26], and cancer patients [27, 28]. Like any other RMT, singing requires repeated and extensive inhalation and exhalation, leading to improvement in respiratory function [8].

In classical and trained singers, studies have shown that different muscles of respiration were recruited at different musical parameters [29–32]. Other than pitch, tempo and rhythmic complexity also affect the breathing mechanism while singing. Pitch refers to the control of the fundamental frequency of voice. The higher the pitch, the higher the tone of voice. Tempo refers to the speed of song in beats per minute (BPM). The faster the tempo, the faster the speed of song. Meanwhile, rhythmic complexity refers to complexity of the rhythm of sung syllables. Rapid changes in the syllables of a song and complex or syncopated rhythm make it more difficult to sing.

Currently there are limited studies implementing singing training among people with SCI. Tamplin et al. (2013) have established trends of improvements in speech intensity, respiratory function, and muscle strength after singing a familiar song [21]. However, no study has investigated the effect of singing different characteristics of song among people with SCI. This knowledge is useful for clinical application with regards to the selection of appropriate songs for RMT. Therefore, the study aims to determine the effect of singing at different tempo, pitch and rhythmic complexity on the accessory respiratory muscle activity while singing among people with SCI.

Materials and methods

In this study, MMG (BIOPAC MP150 system with 2-channel vibromyography) data was monitored and measured from the sternocleidomastoid (SCM) and rectus abdominis (RA) muscles while singing.

Subjects

A total of 13 individuals with SCI (13 males) were recruited in this study (Table 1). All participants were recruited between 3rd June 2022 until 10th August 2022. The authors had access to information that could identify individual participants during or after data collection. The authors obtained written consent from each participant before the experiment began. The inclusion criteria include SCI level between C4 and T11; American Spinal Injury Association Impairment Scale (AIS) A or B; aged 18 years and above. People with SCI above C4 level were not included to ensure all included participants’ diaphragm innervation is still intact. Meanwhile, volunteers with injury level below T11 were not eligible because there is minimal respiratory muscle impairment below this level of injury. AIS A or B indicates the completeness of neurological deficits; A indicates complete motor and sensory injury whilst B indicates incomplete sensory. The exclusion criteria include any other disorders that could affect respiratory functions such as heart failure, coronavirus disease (COVID-19), and tuberculosis. Any volunteers who were unable to sing due to vocal cord conditions or sore throat were also excluded from this study.

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Table 1. Participant demographics.

https://doi.org/10.1371/journal.pone.0305940.t001

Study protocol

The data was collected with SCI participants in a lab in the Department of Biomedical Engineering, Universiti Malaya, Kuala Lumpur. In addition, some data were also monitored and recorded in a non-governmental organization (NGO) building named Beautiful Gate Foundation for the Disabled in Kepong, Kuala Lumpur. The University of Malaya Research Ethics Committee (Ref: UM.TNC2/UMREC– 638) approved the research ethics clearance before the protocol was conducted. Each participant provided informed consent prior to joining the experiment.

Researchers have collectively established MMG as a tool to demonstrate skeletal muscle performance through vibration in various clinical settings [33–35]. Studies using alternative devices in measuring the mechanical activities of the respiratory muscles such as MMG are imperative to complement electromyography (EMG) assessments [33]. According to some researchers, a signal response that is inherently mechanical would provide a more representative model of muscle contraction, as this contraction is fundamentally driven by the mechanical properties of the muscle fibre [36].

Two MMG sensors were attached to participants’ SCM and RA muscles to observe accessory respiratory muscle activity while singing. These two muscles were chosen because they are both superficial, which makes them palpable thus able to be located and captured by MMG. The MMG sensor on SCM was placed based on palpation of the muscle belly during manually resisted neck flexion contractions [37]. The sensor on RA was placed 2 cm lateral to the umbilicus, over the muscle mass [38].

Song categorization

In this study, 4 songs were chosen by the SCI participants from 4 different categories, in terms of their tempo, pitch and rhythmic complexity (Fig 1). The participants chose one song from each category from a total of 48 songs (S4 Appendix). Eight music experts from the Department of Music, Faculty of Creative Arts, Universiti Malaya were recruited to evaluate the characteristics of the songs (S1 and S4 Appendices). A phrase with consistent tempo, pitch and rhythmic complexity for each song were identified. Before singing, MMG signal during inspiration and expiration without singing was recorded.

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Fig 1. The process behind the categorization and characterization of the songs.

https://doi.org/10.1371/journal.pone.0305940.g001

All participants were required to choose one song from each category: (i) slow tempo easy low pitch (SEL), (ii) slow tempo easy high pitch (SEH), (iii) fast tempo hard low pitch (FHL) and (iv) fast tempo hard high pitch (FHH) (Fig 2). ‘Slow’ and ‘fast’ refer to the tempo of the song (S3 Appendix). ‘Easy’ and ‘hard’ refer to the rhythmic complexity. Meanwhile, ‘low’ and ‘high’ refer to the pitch of the song (S2 Appendix).

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Fig 2. The categories of song including examples.

Note: RS = rhythmic complexity; BPM = beats per minute.

https://doi.org/10.1371/journal.pone.0305940.g002

There were no specific instructions on how they were supposed to sing the song, except to follow the musical cues from the pre-recorded track. Every participant used headphones while listening to and singing to the lyrical songs. The volume or loudness of the track was also controlled by the participants themselves.

Data collection

Depending on the categories, each song comprised of either a chorus or a verse, with the duration of approximately between 40 to 80 seconds. Each song was recorded three times. A 5-minutes break in between attempts was allowed, before they repeated the same steps to complete the four categories. In total, each participant spent around 45–75 minutes to finish the experiment.

MMG data from SCM and RA muscles were recorded throughout the singing sessions. The SCM and RA muscles’ activity were collected using BIOPAC® AcqKnowledge® acquisition software from MMG. The participants’ voice while singing was also recorded simultaneously using the Voice Memo application from iPhone 12 Mini.

Data analysis

Muscle performance during quiet breathing and during singing (during inspiration and expiration) was monitored, recorded, and analyzed. In each round of singing, timing of breathe-in and breathe-out activities were identified from the voice recordings using Praat software (Praat, Paul Boersma and David Weenick, Phonetic Sciences Department, University of Amsterdam, The Netherlands).

The raw signal from BIOPAC® AcqKnowledge® acquisition software was sampled at 1 kHz frequency. The signal was then processed with a bandpass filter at lower and higher cut-off frequencies at 20 Hz and 200 Hz respectively. The bandpass filter was applied to reduce the additional noise that might have originated from motion artifacts. The amplitude of the signal was identified as voltages and retrieved as root mean square (RMS). All the processed data were exported for further analysis.

All data were analyzed using one-way analysis of variance (ANOVA) (SPSS Statistics, International Business Machines (IBM) Corporation, United States of America) to compare the accessory respiratory muscles activity while singing at different song categories. Least significant difference (LSD) test was conducted thereafter to determine any difference in accessory respiratory muscles activity while singing between specific categories. The significance level was fixed at 0.05.

Results

After ANOVA analysis, MMG signal of the SCM muscle during quiet breathing, i.e. without singing, showed significant difference between inspiration and expiration activities (P < 0.05). However, MMG signal of the RA during quiet breathing showed no significant difference between inspiration and expiration activities.

The performance of SCM and RA muscles while singing were compared between different song categories using one-way ANOVA. Overall, there was a statistically significant difference among all categories (P < 0.01).

In SCM, post-hoc least significant difference (LSD) test shows statistically significant difference between SEL and FHH (P = 0.008); and FHL and FHH categories (P = 0.035) (Table 2) (Fig 3). Meanwhile, in RA, LSD test showed statistically significant difference between FHL and FHH (P = 0.029) categories (Table 2) (Fig 3). There was also statistically significant difference between SEL and FHL (P = 0.013); and SEH and FHL (P < 0.001) categories in RA muscle (Table 2) (Fig 3).

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Fig 3. SCM and RA muscles performance while singing at different song categories.

Note: * = P < 0.05.

https://doi.org/10.1371/journal.pone.0305940.g003

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Table 2. Post-hoc least significant difference (LSD) test results between song categories.

https://doi.org/10.1371/journal.pone.0305940.t002

Discussion

MMG signals from the SCM and RA muscles were always higher when singing compared to when not singing (P <0.05). This is in line with the role of accessory respiratory muscles like SCM and RA during deep breathing and heightened breathing demand activity such as singing. SCM performance during quiet breathing i.e., without singing reflects the nature of the accessory respiratory muscle during deep breathing [39, 40]. Meanwhile, RA was less active compared to SCM during quiet breathing. This is in parallel with the role of RA as accessory muscles during forceful expiration [41].

Music experts often labelled activation of the muscles of neck, shoulders, upper back, and chest as clavicular breathing [42]. This technique is often regarded as inefficient way of breathing for trained singers because it requires fatiguing way of elevating the rib cage while breathing in [42]. However, this could be beneficial in SCI, where main muscles of respiration might be affected after injury, including the diaphragm [43]. By activating accessory respiratory muscles like SCM, this may improve shortness of breath or dyspnoea in people with SCI [44, 45].

From Fig 3, it can be observed that the SCM muscle is most active when singing songs in high pitch. The SCI participants involuntarily activated their SCM muscle more during heightened breathing demands while singing. This outcome is consistent with many trained and classical singers, whereby their SCM muscles are most active at highest pitch [29–32]. This is important for people with SCI who have impaired diaphragm and intercostal muscles, especially those with cervical spinal cord injury.

In contrast to clavicular breathing, experts viewed abdominal breathing as the viable breathing mechanism for trained singers [46]. Abdominal breathing, or often referred as ‘belly breathing’ is when singers allow the full descent of the diaphragm by activating their abdominal muscles [46, 47]. By expanding the rib cage during inhalation, the intercostals allow the abdominal muscles to be active during expiratory [46, 47].

Fig 3 shows that the RA muscle is most active while singing songs with slow tempo and easy rhythmic complexity. Songs with easy rhythmic complexity have minimal note changes throughout the song, making it much easier for the participants to follow through. Combined with slow tempo, this creates more space and room for the SCI participants to inhale and exhale while singing, involuntarily utilising the ‘belly breathing’ technique.

Among classical singers, abdominal muscles were also more active throughout singing session compared to those of normal people [31]. Classical singers utilize ‘belly breathing’ that allows them to have more control on the speed which the chest collapses after inhalation. This technique is particularly useful for people with SCI level of T1-T11 to improve their trunk; whereby their diaphragm, intercostal, abdominal muscles are still intact.

In short, findings from this study have potential clinical application to clinical populations requiring breathing exercises or RMT for training and improving the strength of accessory muscles during singing therapy. Future research is needed to help clinicians in planning adequate singing therapy to strengthen the respiratory muscles in SCI, including investigation based on their levels of injury.

Conclusion

This study has shown that different song characteristics (such as pitch, tempo, and rhythmic complexity) influenced the accessory respiratory muscles (such as SCM and RA) differently while singing. In high pitch songs, SCM muscle is more active compared to RA muscle. Meanwhile, RA muscle is more active while singing songs with easy tempo and rhythmic complexity. This could be beneficial for clinicians in prescribing singing therapy to improve the respiratory muscles impairment among people with SCI in the future. Further study is recommended to help clinicians estimate the intensity and duration of singing therapy needed to strengthen the respiratory muscles among people with SCI, including investigation based on their levels of injury.

Supporting information

S1 Appendix. Google Form filled by eight music experts in developing the song categories.

https://doi.org/10.1371/journal.pone.0305940.s001

(TIF)

S2 Appendix. Characterization of the songs according to their pitch.

https://doi.org/10.1371/journal.pone.0305940.s002

(TIF)

S3 Appendix. Characterization of the song into slow and fast tempo.

https://doi.org/10.1371/journal.pone.0305940.s003

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S4 Appendix. Song list.

https://doi.org/10.1371/journal.pone.0305940.s004

(TIF)

Acknowledgments

The authors thank all the study participants for their time volunteering.

References

  1. 1. Baydur A., Adkins R. H., & Milic-Emili J. (2001). Lung mechanics in individuals with spinal cord injury: effects of injury level and posture. Journal of Applied Physiology (Bethesda, Md.: 1985), 90(2), 405–411. pmid:11160035
  2. 2. van Houtte S., Vanlandewijck Y., & Gosselink R. (2006). Respiratory muscle training in persons with spinal cord injury: a systematic review. Respiratory Medicine, 100(11), 1886–1895. pmid:16626951
  3. 3. de Paleville D. G. L. T., McKay W. B., Folz R. J., & Ovechkin A. v. (2011). Respiratory Motor Control Disrupted by Spinal Cord Injury: Mechanisms, Evaluation, and Restoration. Translational Stroke Research, 2(4), 463–473. pmid:22408690
  4. 4. Schilero G. J., Spungen A. M., Bauman W. A., Radulovic M., & Lesser M. (2009). Pulmonary function and spinal cord injury. Respiratory Physiology & Neurobiology, 166(3), 129–141. pmid:19442929
  5. 5. Laffont I., Durand M.-C., Rech C., de La Sotta A. P., Hart N., Dizien O., et al. (2003). Breathlessness associated with abdominal spastic contraction in a patient with C4 tetraplegia: a case report. Archives of Physical Medicine and Rehabilitation, 84(6), 906–908. pmid:12808547
  6. 6. Linn W. S., Adkins R. H., Gong H., & Waters R. L. (2000). Pulmonary function in chronic spinal cord injury: a cross-sectional survey of 222 southern California adult outpatients. Archives of Physical Medicine and Rehabilitation, 81(6), 757–763. pmid:10857520
  7. 7. Walter J. S., Sacks J., Othman R., Rankin A. Z., Nemchausky B., Chintam R., et al. (2002). A database of self-reported secondary medical problems among VA spinal cord injury patients: its role in clinical care and management. Journal of Rehabilitation Research and Development, 39(1), 53–61. pmid:11926327
  8. 8. Berlowitz D. and Tamplin J. (2010) ‘Respiratory muscle training for cervical spinal cord injury’, Cochrane Database of Systematic Reviews, 23(7). pmid:23881660
  9. 9. Liaw M. Y., Lin M. C., Cheng P. T., Wong M. K. A., & Tang F. T. (2000). Resistive inspiratory muscle training: Its effectiveness in patients with acute complete cervical cord injury. Archives of Physical Medicine and Rehabilitation, 81(6), 752–756. pmid:10857519
  10. 10. Litchke L., Lloyd L., Schmidt E., Russian C., & Reardon R. (2010). Comparison of Two Concurrent Respiratory Resistance Devices on Pulmonary Function and Time Trial Performance of Wheel Chair Athletes. Therapeutic Recreation Journal, 44(1), 51–62.
  11. 11. Litchke L. G., Russian C. J., Lloyd L. K., Schmidt E. A., Price L., & Walker J. L. (2008). Effects of respiratory resistance training with a concurrent flow device on wheelchair athletes. Journal of Spinal Cord Medicine, 31(1), 65–71. pmid:18533414
  12. 12. Roth E. J., Stenson K. W., Powley S., Oken J., Primack S., Nussbaum S. B., et al. (2010). Expiratory Muscle Training in Spinal Cord Injury: A Randomized Controlled Trial. Archives of Physical Medicine and Rehabilitation, 91(6), 857–861. pmid:20510974
  13. 13. Boswell-Ruys C. L., Lewis C. R. H., Wijeysuriya N. S., McBaAin R. A., Lee B. B., McKenzie D. K., et al (2020). Impact of respiratory muscle training on respiratory muscle strength, respiratory function and quality of life in individuals with tetraplegia: A randomised clinical trial. Thorax, 75(3), 279–288. pmid:31937553
  14. 14. Postma K., Haisma J. A., Hopman M. T. E., Bergen M. P., Stam H. J., & Bussmann J. B. (2014). Resistive inspiratory muscle training in people with spinal cord injury during inpatient rehabilitation: A randomized controlled trial. Physical Therapy, 94(12), 1709–1719. pmid:25082923
  15. 15. Soumyashree S., & Kaur J. (2020). Effect of inspiratory muscle training (IMT) on aerobic capacity, respiratory muscle strength and rate of perceived exertion in paraplegics. Journal of Spinal Cord Medicine, 43(1), 53–59. pmid:29667507
  16. 16. West C. R., Taylor B. J., Campbell I. G., & Romer L. M. (2014). Effects of inspiratory muscle training on exercise responses in Paralympic athletes with cervical spinal cord injury. Scandinavian Journal of Medicine and Science in Sports, 24(5), 764–772. pmid:23530708
  17. 17. Fischer G., Tarperi C., George K., & Ardigò L. P. (2014). An exploratory study of respiratory muscle endurance training in high lesion level paraplegic handbike athletes. Clinical Journal of Sport Medicine, 24(1), 69–75. pmid:24326928
  18. 18. Mueller G., Perret C., & Hopman M. T. E. (2008). Effects of respiratory muscle endurance training on wheelchair racing performance in athletes with paraplegia: A pilot study. Clinical Journal of Sport Medicine, 18(1), 85–88. pmid:18185045
  19. 19. van Houtte S., Vanlandewijck Y., Kiekens C., Spengler C. M., & Gosselink R. (2008). Patients with acute spinal cord injury benefit from normocapnic hyperpnoea training. Journal of Rehabilitation Medicine, 40(2), 119–125. pmid:18509576
  20. 20. Xi J., Jiang H., Wang J., Zhang B., Cao H., Yang B., et al (2019). Respiratory muscle endurance training with normocapnic hyperpnoea for patients with chronic spinal cord injury: A pilot short-term randomized controlled trial. Journal of Rehabilitation Medicine, 51(8), 616–620. pmid:31198974
  21. 21. Tamplin J., Baker F. A., Grocke D., Brazzale D. J., Pretto J. J., Ruehland W. R., et al. (2013). Effect of singing on respiratory function, voice, and mood after quadriplegia: A randomized controlled trial. Archives of Physical Medicine and Rehabilitation, 94(3), 426–434. pmid:23103430
  22. 22. Azekawa M., & Lagasse A. B. (2018). Singing Exercises for Speech and Vocal Abilities in Individuals with Hypokinetic Dysarthria: A Feasibility Study. Music Therapy Perspectives, 36(1), 40–49.
  23. 23. di Benedetto P., Cavazzon M., Mondolo F., Rugiu G., Peratoner A., & Biasutti E. (2009). Voice and choral singing treatment: a new approach for speech and voice disorders in Parkinson’s disease. European Journal of Physical and Rehabilitation Medicine, 45(1), 13–19. pmid:18987565
  24. 24. Shih L. C., Piel J., Warren A., Kraics L., Silver A., Vanderhorst V., et al. (2012). Singing in groups for Parkinson’s disease (SING-PD): A pilot study of group singing therapy for PD-related voice/speech disorders. Parkinsonism and Related Disorders, 18(5), 548–552. pmid:22436653
  25. 25. Stegemöller E. L., Hibbing P., Radig H., & Wingate J. (2017). Therapeutic singing as an early intervention for swallowing in persons with Parkinson’s disease. Complementary Therapies in Medicine, 31, 127–133. pmid:28434465
  26. 26. Mcnamara R. J., Epsley C., Coren E., & Mckeough Z. J. (2017). Singing for adults with chronic obstructive pulmonary disease (COPD). In Cochrane Database of Systematic Reviews. pmid:29253921
  27. 27. Clements-Cortés A. (2017). Singing and Vocal Interventions in Palliative and Cancer Care: Music Therapists’ Perceptions of Usage. Journal of Music Therapy, 54(3), 336–361. pmid:28992349
  28. 28. Fancourt D., Williamon A., Carvalho L. A., Steptoe A., Dow R., & Lewis I. (2016). Singing modulates mood, stress, cortisol, cytokine and neuropeptide activity in cancer patients and carers. Ecancermedicalscience, 10, 1–13. pmid:27170831
  29. 29. Pettersen V. (2005). Muscular patterns and activation levels of auxiliary breathing muscles and thorax movement in classical singing. In Folia Phoniatrica et Logopaedica (Vol. 57, Issues 5–6, pp. 255–277). pmid:16280629
  30. 30. Pettersen V., Bjørkøy K., Torp H., & Westgaard R. H. (2005). Neck and shoulder muscle activity and thorax movement in singing and speaking tasks with variation in vocal loudness and pitch. Journal of Voice, 19(4), 623–634. pmid:16301107
  31. 31. Pettersen V., & Westgaard R. H. (2004). Muscle activity in professional classical singing: A study on muscles in the shoulder, neck and trunk. Logopedics Phoniatrics Vocology, 29(2), 56–65. pmid:15260181
  32. 32. Pettersen V., & Westgaard R. H. (2005). The activity patterns of neck muscles in professional classical singing. Journal of Voice, 19(2), 238–251. pmid:15907438
  33. 33. Ibitoye M. O., Hamzaid N. A., Zuniga J. M., Hasnan N., & Wahab A. K. A. (2014). Mechanomyographic parameter extraction methods: An appraisal for clinical applications. Sensors (Switzerland), 14(12), 22940–22970. pmid:25479326
  34. 34. Islam A., Sundaraj K., Ahmad R. B., & Ahamed N. U. (2013). Mechanomyogram for Muscle Function Assessment: A Review. PloS ONE, 8(3). pmid:23536834
  35. 35. Ramli M. I., Hamzaid N. A., & Engkasan J. P. (2019). Monitoring Breathing Muscle Performance During Singing Noninvasively Using Mechanomyography and Electromyography. Journal of Voice. pmid:31300185
  36. 36. Gerdle B., Karlsson S., Day S., & Djupsjöbacka M. (1999). Acquisition, Processing and Analysis of the Surface Electromyogram. In Modern Techniques in Neuroscience Research.
  37. 37. Falla D., Dall’Alba P., Rainoldi A., Merletti R., & Jull G. (2002). Repeatability of surface EMG variables in the sternocleidomastoid and anterior scalene muscles. European Journal of Applied Physiology, 87(6), 542–549. pmid:12355194
  38. 38. Marshall P., & Murphy B. (2003). The validity and reliability of surface EMG to assess the neuromuscular response of the abdominal muscles to rapid limb movement. Journal of Electromyography and Kinesiology, 13(5), 477–489. pmid:12932422
  39. 39. Short D. J., Silver J. R., & Lehr R. P. (1991). Electromyographic study of sternocleidomastoid and scalene muscles in tetraplegic subjects during respiration. Disability and Rehabilitation, 13(2), 46–49. pmid:1757404
  40. 40. Vitti M. et al. (1973) ‘The integrated roles of Longus Colli and Sternocleidomastoid Muscles: An electromyographic study’, The Anatomical Record, 177(4), pp. 471–484. pmid:4762725
  41. 41. Ito K., Nonaka K., Ogaya S., Ogi A., Matsunaka C., & Horie J. (2016). Surface electromyography activity of the rectus abdominis, internal oblique, and external oblique muscles during forced expiration in healthy adults. Journal of Electromyography and Kinesiology, 28, 76–81. pmid:27077819
  42. 42. Rootberg R. (2003). Clavicular Breathing, Held Shoulders and Related Issues: A Round Table Discussion. Voice and Speech Review, 3(1), 278–295.
  43. 43. Warren P. M., Askew G. N., Kissane R. W. P., Egginton S., & Kwok J. C. F. (2020). Oxygen transport kinetics underpin rapid and robust diaphragm recovery following chronic spinal cord injury. Journal of Physiology-London, 0, 1–26. pmid:33146892
  44. 44. Cardozo C. P. (2007). Respiratory Complications of Spinal Cord Injury. The Journal of Spinal Cord Medicine, 30(4), 307–308. pmid:17853651
  45. 45. Gee C. M., Williams A. M., West C. R., Sheel A. W., & Eves N. D. (2019). Respiratory muscle training in athletes with cervical spinal cord injury: effects on cardiopulmonary function and exercise capacity. Journal of Physiology, 597(14), 3673–3685. pmid:31115056
  46. 46. Salomoni S., van den Hoorn W., & Hodges P. (2016). Breathing and singing: Objective characterization of breathing patterns in classical singers. PLoS ONE, 11(5). pmid:27159498
  47. 47. Watson P. J., Hoit J. D., Lansing R. W., & Hixon T. J. (1989). Abdominal Muscle Activity During Classical Singing. Journal of Voice, 3(1), 24–31.