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. 2024 Jul 5;19(7):e0305940. doi: 10.1371/journal.pone.0305940

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

Muhammad Imran Ramli 1,*, Nur Azah Hamzaid 1, Julia Patrick Engkasan 2, Juliana Usman 1, Marzelan Salleh 3, Wee Duen Hueh 1
Editor: Sahreen Anwar4
PMCID: PMC11226013  PMID: 38968230

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.

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.

Table 1. Participant demographics.

Demographic SCI participants (n = 13)
Age (year) 48.8 ± 8.6
Height (m) 1.6 ± 0.1
Weight (kg) 67.3 ± 11.6
BMI (kg/m3) 24.9 ± 4.0
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Note: BMI = body mass index

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.

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

Fig 1

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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).

Fig 2. The categories of song including examples.

Fig 2

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

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).

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

Muscle Song category Significant (p)
SCM SEL SEH 0.452
FHL 0.594
FHH 0.008
SEH FHL 0.827
FHH 0.058
FHL FHH 0.035
RA SEL SEH 0.206
FHL 0.013
FHH 0.767
SEH FHL <0.001
FHH 0.118
FHL FHH 0.029
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Fig 3. SCM and RA muscles performance while singing at different song categories.

Fig 3

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Note: * = P < 0.05.

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.

(TIF)

pone.0305940.s001.tif (581.7KB, tif)
S2 Appendix. Characterization of the songs according to their pitch.

(TIF)

pone.0305940.s002.tif (681.5KB, tif)
S3 Appendix. Characterization of the song into slow and fast tempo.

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pone.0305940.s003.tif (401.8KB, tif)
S4 Appendix. Song list.

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pone.0305940.s004.tif (649.7KB, tif)

Acknowledgments

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

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 Statement

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.

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Decision Letter 0

Sahreen Anwar

25 Jul 2023

PONE-D-23-07503Accessory Respiratory Muscles Performance During Singing at Different Song Characteristics Among People with Spinal Cord InjuryPLOS ONE

Dear Dr. Ramli

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Sep 08 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Sahreen Anwar, PhD PT

Academic Editor

PLOS ONE

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5. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: I Don't Know

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: I believe that this is the original work of the authors and presents a novel idea and appropriate methodology. the study is well planned and conducted accordingly. the selection of he songs and their characteristics is reasonable and the results may be utilized further in patients with SCI.

Reviewer #2: This is an interesting and well written article describing the results of an exploratory study of accessory respiratory muscle activation for people with spinal cord injury during singing songs with different characteristics.

Overall, the paper is clearly laid out and all sections are articulated well. There are only a few minor things for consideration that I have outlined below.

Would muscle ‘activation’ be a better word choice than ‘performance’ in the title? Also, I’m not sure about the grammar of “singing at different song characteristics”. Maybe “songs with different musical parameters”?

Avoid use of pathologizing language such as “suffer from” (first line of abstract). More neutral or strengths-based language is preferred, such as “experience” or “live with”

I’m also not sure about phrase “rhythmic syllable” as one of the musical parameters of songs referred to throughout the paper. I think what you mean is “rhythmic complexity” or “syllable rhythmic complexity” if you want to keep the reference to syllables in there.

In the abstract it would be helpful to state the level of SCI. Eg. participants with SCI (C4 -T11 ASIA A or B).

Last line of abstract, suggest replacing “outcome” with “knowledge” – “Clinicians could benefit from this knowledge…”

Please state the exact number of songs that were characterized into the four categories.

Introduction is clear and succinct and supported by appropriate current references.

A clear summary of current published knowledge in the area and justification for the study.

Line 51-52 – suggest joining these 2 sentences for better flow: “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.”

Revise lines 65-66 based on comments above about the grammar of “singing at different song characteristics”. Maybe “songs with different musical parameters”? Also “rhythmic complexity” rather than “rhythmic syllable”

Revise lines 69-70 for clarity of expression. Perhaps “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.”

Line 73 has a reference date which is not required in this referencing style. NB. Tamplin et all have a 2011 study which is more aligned with the exploratory design of this study and should be referenced here and compared in the discussion also.

Tamplin, J., Brazzale, D., Pretto, J.J., Ruehland, W.R., Buttifant, M., Brown, D.J., Berlowitz, D.J. (2011). Assessment of breathing patterns and respiratory muscle recruitment during singing and speech in quadriplegia. Archives of Physical Medicine and Rehabilitation, 92(2), 250-256. doi: 10.1016/j.apmr.2010.10.032

Method and Results are clearly expressed. Appropriate use of tables and figures.

Line 82 – suggest removing the words “their respective respiratory muscles” and joining these two sentences.

Line 92 – suggest changing the word “chosen” to “eligible” and modifying this sentence:

“…volunteers with injury level below T11 were not eligible because there is minimal respiratory muscle impairment below this level of injury.”

Line 97 – typo – “vocal cord conditions”

Discussion and Implications are comprehensive and appropriate reflect on findings and study limitations in relation to previous research.

Possible typo on p12 line 359 “positive effects on other cognitive functions…”

Line 104 – remove the word “has”.

Lines 109-111

“Studies using alternative devices in measuring the mechanical activities of the respiratory muscles such as MMG are imperative to complement electromyography (EMG) assessments [33]. Some researchers have also suggested that a signal response that is inherently mechanical…”

Lines 114-115

“Two MMG sensors were attached to participants’ SCM and RA muscles to observe the accessory respiratory muscle activity while singing. These two muscles were chosen…”

Line 117

Plural error. Was there 1 or 2 MMG sensors place on SCM?

“MMG sensor on SCM was placed” or “MMG sensors on SCM were placed”

Line 127

“All participants were required to choose one song from each category.” Figure 2 shows only 1 song in each category though. Did they choose really?

Line 133

Suggest changing “follow the rhythm” to “follow the musical cues”

Line 138

What do you mean by: “Each song was recorded under three different trials”?

Line 144-145 What were the voice memo recordings used for?

Line 149 Suggest changing: “breathe-in and breathe-out activities were identified by referencing the voice recorded using Praat software” to “breathe-in and breathe-out activities were identified from the voice recordings using Praat software”

Line 152 “These timings were selected at the same section of the track for each participant.”

Didn’t each participant choose different songs though?

Results

Please add a results table and ensure to use exact p values in the results section (not just p0.05). Past tense also required. (eg. Line 173 “(LSD) test showed…”

It would be interesting to know if there were any differences in accessory respiratory muscle activation for people with different injury levels.

Discussion

Please use past tense and don’t present results/stats in discussion.

Line 180 – “MMG signal on the muscles while not singing is always lower compared to that of while singing (P 0.05).” Suggested revision: “MMG signals from the SCM and RA muscles were always higher when singing compared to when not singing.”

Line 192 – please clarify who you mean by “their”. Ie. “By activating accessory respiratory muscles like SCM, this may improve shortness of breath or dyspnoea for people with SCI.

Line 207 – please clarify what you mean by “follow through”.

Line 210 – the meaning of this sentence is unclear. Who are the “normal trained students”? Are these singing students? If so, this is a confusing comparison with classical singers.

“Among classical singers, abdominal muscles were also more active throughout singing session compared to those of normal, trained students.”

Are there any recommendations for which aspects of songs might be more beneficial for different levels of SCI? Ie. do higher level injured patients need to focus more on SCM or RA. Or are both equally beneficial? What about lower injury levels?

It would be good to have some clearer practice implications from this research if possible. Or if not, some clearer guidance for what further research is needed to provide clinical practice guidance.

Conclusion – please remove the unnecessary words “to conclude” in line 220

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Jeanette Tamplin

**********

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Attachment

Submitted filename: Paper 3_PLOS One.docx

pone.0305940.s005.docx (558.4KB, docx)
Attachment

Submitted filename: PONE-D-23-07503 (reviewer tracked).pdf

pone.0305940.s006.pdf (807.9KB, pdf)
Attachment

Submitted filename: PLOS One - reviewer comments.docx

pone.0305940.s007.docx (18.9KB, docx)
PLoS One. 2024 Jul 5;19(7):e0305940. doi: 10.1371/journal.pone.0305940.r002

Author response to Decision Letter 0

19 Mar 2024

A Point-by-Point Response to Reviewers’ Comments to the Author

No. Reviewer’s comment Response

1. Would muscle ‘activation’ be a better word choice than ‘performance’ in the title? Thank you for your suggestion. However, in our case ‘performance’ is better as we were using mechanomyography (MMG), not electromyography (EMG).

EMG measures the electrical activity of the muscle during contraction generated by the brain. Meanwhile, MMG measures the mechanical vibrations produced by the muscle contraction.

2. Also, I’m not sure about the grammar of “singing at different song characteristics”. Maybe “songs with different musical parameters”? I have rearranged the title of the manuscript according to your recommendation from “Accessory Respiratory Muscles Performance During Singing at Different Song Characteristics Among People with Spinal Cord Injury” into “Accessory Respiratory Muscles Performance Among People with Spinal Cord Injury While Singing Songs with Different Musical Parameters”.

3. Avoid use of pathologizing language such as “suffer from” (first line of abstract). More neutral or strengths-based language is preferred, such as “experience” or “live with”. The sentence is changed from “suffer from” into “experience”.

4. I’m also not sure about the phrase “rhythmic syllable” as one of the musical parameters of songs referred to throughout the paper. I think what you mean is “rhythmic complexity” or “syllable rhythmic complexity” if you want to keep the reference to syllables in there. Thank you for your input. The phrase “rhythmic syllable” is changed into “rhythmic complexity’” as pointed out by the reviewer, throughout the manuscript.

5. In the abstract it would be helpful to state the level of SCI. Eg. participants with SCI (C4 -T11 ASIA A or B). We have included the participants ASIA classification and injury level in the abstract. Thank you for the suggestion.

6. Last line of abstract, suggest replacing “outcome” with “knowledge” – “Clinicians could benefit from this knowledge…” The word “outcome” has been replaced with the word “knowledge” in the last line of abstract.

7. Please state the exact number of songs that were characterized into the four categories. The exact number of songs is added into the manuscript in line 122. Also, the whole paragraph has been rearranged to ensure less confusion from readers.

8. Line 51-52 – suggest joining these 2 sentences for better flow: “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.”

The 2 sentences in line 51-52 have been combined as mentioned by the reviewer.

9. Revise lines 65-66 based on comments above about the grammar of “singing at different song characteristics”. Maybe “songs with different musical parameters”? Also “rhythmic complexity” rather than “rhythmic syllable” Changes has been made accordingly in both cases.

10. Revise lines 69-70 for clarity of expression. Perhaps “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.” Thank you for the correction. The lines 69-70 has been revised as stated by the reviewer.

11. Line 73 has a reference date which is not required in this referencing style. I have double checked the reference with ScienceDirect, and it still stated the same year as the one in this manuscript, which is 2013.

12. Line 82 – suggest removing the words “their respective respiratory muscles” and joining these two sentences. Changes has been made accordingly.

13. Line 92 – suggest changing the word “chosen” to “eligible” and modifying this sentence:

“…volunteers with injury level below T11 were not eligible because there is minimal respiratory muscle impairment below this level of injury.” Line 92 has been revised as stated by the reviewer.

14. Line 97 – typo – “vocal cord conditions” Noted. The word “cords” has been changed into “cord”.

15. Line 104 – remove the word “has”. The word “has” has been removed.

16. Lines 109-111

“Studies using alternative devices in measuring the mechanical activities of the respiratory muscles such as MMG are imperative to complement electromyography (EMG) assessments [33]. Some researchers have also suggested that a signal response that is inherently mechanical…” Thank you for pointing out the grammar mistakes. Changes has been made accordingly.

17. Lines 114-115

“Two MMG sensors were attached to participants’ SCM and RA muscles to observe the accessory respiratory muscle activity while singing. These two muscles were chosen…” Changes has been made accordingly.

18. Line 117

Plural error. Was there 1 or 2 MMG sensors place on SCM?

“MMG sensor on SCM was placed” or “MMG sensors on SCM were placed” There was only one sensor placed on SCM. Therefore, the correct sentence would be “MMG sensor on SCM was placed”. Changes has been made on line 117.

19. Line 127

“All participants were required to choose one song from each category.” Figure 2 shows only 1 song in each category though. Did they choose really? Participants were given a list of songs for each category, as shown in Appendix D. There are 48 songs on the list (as addressed in point no. 7).

From that list, the participants will choose only one song for each category.

Figure 2 only showed the four quadrants (or categories); (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).

20. Line 133

Suggest changing “follow the rhythm” to “follow the musical cues” Changes has been made as suggested.

21. Line 138

What do you mean by: “Each song was recorded under three different trials”? Each song was recorded for three attempts. The sentence has been changed to make sure less confusion from the readers.

22. Line 144-145 What were the voice memo recordings used for?

The voice memo recordings were used together with Praat software to identify the exact moments of inspiration and expiration for data analysis.

23. Line 149 Suggest changing: “breathe-in and breathe-out activities were identified by referencing the voice recorded using Praat software” to “breathe-in and breathe-out activities were identified from the voice recordings using Praat software” Thank you for the suggestion. Changes has been made as stated by the reviewer.

24. Line 152 “These timings were selected at the same section of the track for each participant.”

Didn’t each participant choose different songs though? Yes, you are right. This is a mistake from my end. The sentence has been removed from the manuscript.

25. Please add a results table and ensure to use exact p values in the results section (not just p0.05). Past tense also required. (eg. Line 173 “(LSD) test showed…” A new table (Table 2) has been added on the manuscript. The exact p values were also stated in the result section. The grammar error on Line 173 has also been corrected.

26. It would be interesting to know if there were any differences in accessory respiratory muscle activation for people with different injury levels. We did not perform any specific analysis to compare the accessory respiratory muscle activation between participants of different injury levels, thus are unable to provide a conclusive statement addressing this point.

However, based on our crude observation, we do not see any difference in muscle performance between the different injury levels.

We have added this in the discussion (line 217, page 10)

“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.”

27. Please use past tense and don’t present results/stats in discussion.

Line 180 – “MMG signal on the muscles while not singing is always lower compared to that of while singing (P 0.05).” Suggested revision: “MMG signals from the SCM and RA muscles were always higher when singing compared to when not singing.” Changes has been made accordingly.

28. Line 192 – please clarify who you mean by “their”. Ie. “By activating accessory respiratory muscles like SCM, this may improve shortness of breath or dyspnoea for people with SCI. Thank you for the suggestion. The sentence has been rearranged in the manuscript.

29. Line 207 – please clarify what you mean by “follow through”. From our experience during data collection, some participants found it harder to sing all the lyrics in songs categorized as hard rhythmic complexity. Some participants could not keep up with the lyrics due to the fast nature of the songs.

30. Line 210 – the meaning of this sentence is unclear. Who are the “normal trained students”? Are these singing students? If so, this is a confusing comparison with classical singers.

“Among classical singers, abdominal muscles were also more active throughout singing session compared to those of normal, trained students.” Thank you for notifying us with the mistake. Correction has been made accordingly.

31. please remove the unnecessary words “to conclude” in line 220 The word “to conclude” has been removed.

Attachment

Submitted filename: Response to Reviewers Imran PlosOne.docx

pone.0305940.s008.docx (21.1KB, docx)

Decision Letter 1

Sahreen Anwar

9 Apr 2024

PONE-D-23-07503R1Accessory Respiratory Muscles Performance Among People with Spinal Cord Injury While Singing Songs with Different Musical ParametersPLOS ONE

Dear Dr. Ramli,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

ACADEMIC EDITOR: Please carefully consider the comments made by the reviewers. Make sure to get your manuscript formatted by a language expert.Overall, there is merit in the article but after incorporating these changes it will be more refined and presentable.==============================

Please submit your revised manuscript by May 24 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-emailutm_source=authorlettersutm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Sahreen Anwar, PhD Physical Therapy

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments 

Thank you for submitting your work to PLOS ONE. There are some areas that need attention. Please get your article reviewed from a language expert, moreover, the technical language related to musicology must be simple and concise to enhance its readability.

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Jul 5;19(7):e0305940. doi: 10.1371/journal.pone.0305940.r004

Author response to Decision Letter 1

14 May 2024

Point-by-point responses to the editor comments:

1. Please get your article reviewed from a language expert.

The manuscript has been proofread by a proofreader. A certificate from the proofreader is attached in the appendix below.

2. Please get your article reviewed from the technical language related to musicology must be simple and concise to enhance its readability.

The manuscript has been proofread by two experts from music background: (1) Dr Marzelan Salleh, one of the co-authors of the manuscript from Music Department in Faculty of Creative Arts in Universiti Malaya, and (2) Dr Camellia Siti Maya Mohamed Razali from Music Department in Faculty of Human Ecology in Universiti Putra Malaysia.

3. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text or remove these references and replace them with relevant current references.

The reference list has been reviewed and several changes has been made in the DOI link. The changes were made because some of the DOI links were not working. This includes the link to references number 8, 9, 40, 41, 44, and 47. None of the references were retracted after reviewing the list.

4. While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements.

All figures from the manuscript have been uploaded in PACE website. The updated and corrected version of the figures have been uploaded during submission.

Attachment

Submitted filename: Point by point responses.docx

pone.0305940.s009.docx (103.3KB, docx)

Decision Letter 2

Sahreen Anwar

10 Jun 2024

Accessory Respiratory Muscles Performance Among People with Spinal Cord Injury While Singing Songs with Different Musical Parameters

PONE-D-23-07503R2

Dear Dr. Ramli,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Acceptance letter

Sahreen Anwar

24 Jun 2024

PONE-D-23-07503R2

PLOS ONE

Dear Dr. Ramli,

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

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

    (TIF)

    pone.0305940.s001.tif (581.7KB, tif)
    S2 Appendix. Characterization of the songs according to their pitch.

    (TIF)

    pone.0305940.s002.tif (681.5KB, tif)
    S3 Appendix. Characterization of the song into slow and fast tempo.

    (TIF)

    pone.0305940.s003.tif (401.8KB, tif)
    S4 Appendix. Song list.

    (TIF)

    pone.0305940.s004.tif (649.7KB, tif)
    Attachment

    Submitted filename: Paper 3_PLOS One.docx

    pone.0305940.s005.docx (558.4KB, docx)
    Attachment

    Submitted filename: PONE-D-23-07503 (reviewer tracked).pdf

    pone.0305940.s006.pdf (807.9KB, pdf)
    Attachment

    Submitted filename: PLOS One - reviewer comments.docx

    pone.0305940.s007.docx (18.9KB, docx)
    Attachment

    Submitted filename: Response to Reviewers Imran PlosOne.docx

    pone.0305940.s008.docx (21.1KB, docx)
    Attachment

    Submitted filename: Point by point responses.docx

    pone.0305940.s009.docx (103.3KB, docx)

    Data Availability Statement

    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.

    Articles from PLOS ONE are provided here courtesy of PLOS

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