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ARTICLE IN PRESS

The Impact of Respiratory Exercises on Voice Outcomes:


A Systematic Review of the Literature
*Maude Desjardins, and *,†Heather Shaw Bonilha, *yCharleston, South Carolina

Summary: Introduction. The role of respiratory exercises in voice therapy remains unclear as many patients
do not need extensive breath support to meet their voice demands. However, since these exercises are commonly
used in clinical practice and ubiquitous in voice therapy textbooks, there is a need to determine the evidence for
using respiratory exercises to improve vocal function.
Objective. The goal of the present review is to determine the state of the evidence regarding the effectiveness of
respiratory interventions to improve respiratory and voice outcomes.
Methods. A review of the literature was conducted using three electronic databases: Pubmed, Scopus, and
CINAHL. A search strategy was developed to highlight two main concepts: (1) voice and (2) respiratory exercises.
Results. Out of 650 articles identified through the search, 23 articles met the inclusion criteria, spanning nine
types of respiratory exercises: (1) expiratory muscle strength training; (2) inspiratory muscle strength training; (3)
incentive spirometry; (4) isocapnic hyperpnea; (5) respiratory effort treatment; (6) abdominal directives; (7) “easy
breathing”; (8) stimulation training; and (9) vocalization with abdominal breath support. Respiratory improve-
ments were reported in 12 articles. Nine of 12 articles also reported some voice improvements, although these
were limited to subsets of participants.
Conclusions. The results of this review suggest that the evidence to support using respiratory exercises to
improve vocal function is specific to a patient's respiratory and vocal needs. That is, current evidence does not
support using respiratory exercises for all patients with voice disorders. Emerging evidence also indicates the
importance of generalizing the outcomes of respiratory exercises to voice tasks. It is critical that the mechanism
of action through which respiratory exercises can impact voice outcomes be thoroughly understood, and it is
hoped that future research will help provide more information in this regard.
Key Words: Voice−Respiratory exercises−Respiratory training−Voice therapy−Intervention−Review−Breathing
exercises.

INTRODUCTION for building efficient respiratory support. Reasons for this


Respiratory support void in the literature may reside in the fact that (1) to date,
Since the advent of voice sciences, the relationship between no clear-cut definition exists to characterize the supported
the respiratory and the laryngeal systems has been a subject voice,2,9 and (2) ways of achieving support may vary across
of great interest. These systems work in coordination to individuals,1 making it challenging to study as a treatment
control the sound emitted by the larynx and produce the outcome. Nonetheless, suggested definitions incorporate the
desired pitch, loudness, and vocal quality. To better under- notions of active muscular action counteracting passive
stand the role of the respiratory system and its importance relaxation pressures and of balance between inspiratory and
for healthy voice production, researchers have attempted to expiratory pressures.2,7 While the expiratory forces are
demystify the 00 supported voice,00 a concept that is predomi- pressing the air out of the lungs, the thoracic muscles are
nant in the singing field.1−6 So far, research has focused on resisting the collapse of the lungs to control the expiratory
establishing the physiological correlates of the supported pressure.7 The tonicity of the abdominal wall also partici-
voice, with fewer publications addressing the methods used pates in maintaining ribcage expansion and in controlling
to achieve it. Some authors have published pedagogical the ascension of the diaphragm.9−11 Importantly, the role of
papers on the application of breathing techniques7,8 and support is not to provide more air, but rather to contribute
although these essays are noteworthy for voice scientists to airflow and subglottal pressure control during phonation.
and teachers, they do not provide evidence-based practices This state of balance is thought to mitigate excessive laryn-
geal muscle tension, allowing the vocal folds to provide ade-
quate glottal resistance to airflow and to further regulate
Accepted for publication January 24, 2019.
Portions of this study were presented at the ASHA Convention. Boston, Massachu- the subglottal pressure for voice production.2,12
setts, November 2018. An active involvement of the respiratory muscles is
From the *Department of Health Science and Research, Medical University of
South Carolina, Charleston, South Carolina; and the yDepartment of Otolaryngology thought to improve and ease voice production. A study
− Head and Neck Surgery, Medical University of South Carolina, Charleston, South comparing singers’ performances with and without volun-
Carolina.
Address correspondence and reprint requests to Heather Shaw Bonilha, Department tarily engaging respiratory support revealed an increase
of Health Science and Research, Medical University of South Carolina, 77 President in acoustic power and a decrease in expiratory airflow in
St, Charleston, SC 29425. E-mail: bonilhah@musc.edu
Journal of Voice, Vol. &&, No. &&, pp. &&−&& the supported condition, indicating a more efficient pho-
0892-1997 nation mode.5 Singers describe their supported voice as
© 2019 Published by Elsevier Inc. on behalf of The Voice Foundation.
https://doi.org/10.1016/j.jvoice.2019.01.011 easier to manage, clearer, with improved resonance and
ARTICLE IN PRESS
2 Journal of Voice, Vol. &&, No. &&, 2019

TABLE 1. Respiratory support and voice disorders


List of Abbreviations While the normal physiology of respiration and phonation
and the relationship between the two have been extensively
Abbreviation Full Name described in the literature, data pertaining to the role of the
MTD Muscle tension dysphonia respiratory system in voice disorders is less abundant. This
SLP Speech and language pathologist is surprising considering that the subsystems of voice are
PRISMA Preferred Reporting Items for System- interdependent, and consequently there are multiple ways in
atic Reviews and Meta-Analyses which respiration and phonation can interact with each
MeSH Medical Subject Heading other and result in pathological states.
NHMRC National Health and Medical Research
Impaired respiratory function can cause or contribute to
Council
QIS Quality Index Score
poor voice outcomes, since the respiratory and laryngeal
RCT Randomized controlled-trial systems are coupled and impairment in one of them often
PD Parkinson disease leads to dysfunction of the other.13 Impaired respiratory
EMST Expiratory muscle strength training function can be induced by compromized pulmonary func-
IMST Inspiratory muscle strength training tion, such as in the case of asthma and chronic obstructive
RET Respiratory effort treatment pulmonary disease, and/or by weak respiratory muscles,
MEP Maximum expiratory pressure such as in the case of normal aging. If the respiratory system
MIP Maximum inspiratory pressure is not strong enough to generate sufficient air pressure and
MPT Maximum phonation time to control the natural respiratory pressures, one may have
FVC Forced vital capacity to rely on laryngeal adduction to increase loudness and to
FEV1 Forced expiratory volume in one
ensure airflow conservation. In fact, if the respiratory
second
PEF Peak expiratory flow
muscles are not strong enough to control the expiratory air-
SPL Sound pressure level flow during speech, the airflow conservation role relies
STSD Frequency variability in semitones solely on the vocal folds acting as a valve.13 If a laryngeal
F0 Fundamental frequency deficit is already present, the impact is even more notable:
LSVT Lee Silverman Voice Treatment Vaca et al14 found that elderly patients presenting with a
COPD Chronic obstructive pulmonary disease laryngeal deficit (glottal gap) in addition to respiratory defi-
LLN Lower limit of normal cits (either vital capacity or peak expiratory airflow below
FEF25−75% Forced expiratory flow at 25−75% of the 80% of the reference value) had shorter phonation times,
pulmonary volume increased jitter, worse auditory perceptual ratings, and
MMEF Maximum mid expiratory flow higher Voice Handicap Index scores than the patients with
deficits in only the laryngeal or respiratory system. The
impaired respiratory system could not compensate for
the poor laryngeal valving function, thereby explaining the
poorer voice outcomes in these patients.
Another pathway through which the respiratory system can
quality, and with increased range.1 To explain how they influence voice is through inadequate musculoskeletal pat-
do it, performers refer to proper adjustment of their respi- terns. A weakness or imbalance in the functioning of certain
ratory muscles (eg, compressing the diaphragm against muscles, such as the periabdominal muscles, can cause issues
the abdomen; expanding the chest; and increasing the sen- in the cervical spine, leading to detrimental compensatory
sation of muscular resistance).1 When comparing trained patterns in the neck and perilaryngeal region.11,15 This is
performers using support to untrained individuals, differ- thought to be a potential contributing factor in muscle tension
ences in breathing patterns have also been found. These dysphonia (MTD) (see Table 1 for a list of all abbrevia-
include a smaller change in ribcage volume and a greater tions).15 In addition, groups of researchers have started to
contribution of the abdomen volume during singing in examine the use of periabdominal muscles in dysphonic
experienced performers.9 patients and in vocally healthy speakers.3,11 Preliminary data
It is now widely accepted that engaging the respiratory suggest that patients with MTD tend to underutilize their
muscles is essential for production of a healthy projected voice transverse abdominal muscles and overactivate their internal
during singing and acting. While a large proportion of voice oblique muscles during voicing, in comparison to vocally
patients are professional voice users and rely on effective voice healthy subjects.3,11 However, the specific impact that this
projection, such as teachers and lawyers, other patients have may have on the laryngeal and perilaryngeal muscles remains
less exigent voice demands and do not rely on voice projection speculative and further studies are warranted.
to accomplish their daily work. For these patients, targeting It may also be helpful to improve respiratory support in
vocal function with voice exercises may be sufficient to induce patients with voice disorders who do not have co-occurring
functional improvements. Consequently, the importance of respiratory dysfunction, for two reasons. First, to help alle-
the widespread incorporation of breathing exercises and respi- viate the load on the vocal folds and laryngeal musculature,
ratory training in voice therapy remains unclear. which could lead to voice improvements. Second, voice
ARTICLE IN PRESS
Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 3

patients can develop unfavorable respiratory patterns when outcomes in patients with or without voice disorders can be
attempting to compensate for laryngeal dysfunction. In a validated. By reporting and discussing the results of respira-
recent paper on respiration and voice disorders, Lewandow- tory intervention studies, we hope to promote evidence-based
ski and Gillespie16 explain that ineffective breathing pat- practice by guiding clinicians and voice teachers in the deci-
terns have been identified not only as a cause but also as a sion to incorporate respiratory exercises in their voice inter-
result of some voice disorders, including MTD, paradoxical ventions, and if so which exercises. We also hope to identify
vocal fold movement disorder and benign vocal fold lesions. promising interventions as well as gaps in the literature to
For example, patients with bilateral vocal fold nodules need help focus future research in the field.
to recruit greater respiratory effort because of the increased The present study's aims are the following:
glottal airflow occasioned by incomplete glottal closure.16,17
If their respiratory support is inefficient, they will present 1) Review the literature on respiratory interventions
with increased risk of developing detrimental compensatory applied to the goal of improving voice outcomes.
mechanisms in the laryngeal or respiratory systems, which 2) Describe their impact on respiratory outcomes.
are likely to partake in the voice problem. 3) Describe their impact on voice outcomes.
Considering the role of respiratory physiology in voice dis- 4) Provide insights for clinical practice.
orders, Lewandowski and Gillespie emphasized the question 5) Assess the limitations and gaps in the literature and
as to whether respiratory exercises should be included as a spe- suggest direction for future research.
cific treatment component for voice patients.16 In fact, some
voice therapy techniques, such as flow phonation and vocal
function exercises, integrate aspects of respiratory-laryngeal
coordination and/or respiratory support. For some speech METHODS
and language pathologists (SLPs), these programs are thought Search procedures
to be sufficient to rebalance the respiratory system. Alterna- A review of the literature was conducted following the Pre-
tively, some SLPs choose to treat respiratory exercises as a dis- ferred Reporting Items for Systematic Reviews and Meta-
tinct component of treatment, allocating therapy time to work Analyses (PRIMSA) guidelines,20 using three electronic
explicitly on the respiratory system and then generalizing the databases: Pubmed, Scopus, and CINAHL. A search strat-
newly acquired motor patterns to voice tasks. Nevertheless, egy was developed to highlight two main concepts: (1) voice
respiratory exercises in themselves do not involve voicing and and (2) respiratory exercises. In Pubmed, the Medical Sub-
have been criticized for not fulfilling the specificity principle ject Heading (MeSH) terms: voice, voice quality, voice disor-
for motor learning. For this reason, it is essential that the evi- ders, hoarseness, aphonia, voice training, singing, speech,
dence for the relevance and impact of respiratory exercises on phonation, and speech disorders were combined with “OR”
voice outcomes be thoroughly examined. to: voice, dysphonia, aphonia, vocal, hoarseness, phonation,
singing, singer*, and speech, to depict the concept of voice.
Similarly, the MESH term breathing exercises was com-
Contribution to current knowledge bined with “OR” to: respirat* outcome*, respirat* treat-
In our recent literature review on voice therapy for dysphonic ment, breathing treatment, respirat* rehabilitation, breathing
patients,18 including fifteen randomized controlled trials rehabilitation, respirat* exercise*, breathing exercise*, respi-
(RCTs), all but one of the intervention programs incorporated rat* training, breathing training, respirat* therapy, breathing
aspects of respiratory support or coordination, based on Van therapy, respiratory muscle strength training, respiratory
Stan's taxonomy of voice therapies.19 The review revealed muscle training, respirat* intervention, breathing interven-
that efficacious voice therapy programs feature elements tion, respirat* technique*, “breathing technique*, breath-
related to vocal function, respiratory support and coordina- work”, respiratory support, and breath* support, to depict
tion, and somatosensory feedback.18 However, because none the concept of respiratory exercises. These two groups of
of the articles isolated the respiratory interventions as an inde- terms were then combined with “AND” to form the com-
pendent variable, no conclusion regarding their individual plete Pubmed search strategy.
effect on voice outcomes could be drawn. Considering the In CINAHL, the exploded headings voice, voice therapy,
results of our literature review on voice therapy, we decided to and voice disorders were used to represent the concept of
extend our search to include nonrandomized clinical trials voice, while the exploded heading breathing exercises was
and studies conducted on vocally healthy populations, since used for the concept of respiratory exercises. A search with
respiratory interventions that are successful in healthy sub- keywords was also conducted in CINAHL, using the same
jects, such as singers and actors, may also be relevant for voice keywords as for the Pubmed search. The same keywords
patients pending further studies. were also used to conduct the search in Scopus.
The goal of the present review is to determine the state of The search was conducted on February 6th, 2018. The
the evidence regarding the effectiveness of respiratory inter- reference lists of all relevant articles, those included in the
ventions to improve voice outcomes. This evidence will allow study, were screened by the first author to identify any
for an assessment of whether the premise that exercises focus- articles that were not retrieved from the database searches
ing on respiratory function are effective in improving voice detailed above.
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4 Journal of Voice, Vol. &&, No. &&, 2019

Screening procedures V. Study design:


Inclusion and exclusion criteria a. All studies assessing both pre- and post-treatment
voice outcomes were considered for inclusion.
I. Publication: b. Case studies and single-subject designs with less
a. English and French articles were included in the than five participants were excluded.
search because these are the languages mastered by
the authors of the review. No publication date After the initial search, duplicates were deleted and
restriction was applied. remaining articles were screened by the first author based
b. Only publications that were peer reviewed and on titles and abstracts. Twenty percent of these articles were
issued in an indexed journal were considered for the also screened by the last author to ensure reliability of the
review. Masters or doctorate theses as well as con- screening process. Studies that did not meet the inclusion
ference proceedings were excluded. criteria or that met any exclusion criterion were eliminated
II. Participant characteristics during that first screening phase. Those that met all the
a. No restrictions were applied pertaining to partici- inclusion criteria or that were ambiguous were kept for the
pant characteristics. For a study to be included in second screening phase, which consisted of a full-text
the review, subjects could either have a diagnosed review. Twenty percent of these articles were also screened
voice disorder, unspecified voice complaints, or be by the last author. Any disagreements were discussed to
vocally healthy. Studies conducted on voice profes- reach consensus. The results of the screening process are
sionals such as singers, actors, and teachers were presented in the Results section.
included. For dysphonic participants, voice disor-
ders of all origins (functional, organic, neurological,
and psychogenic) as well as dysphonia related to Data extraction
aging were considered for this review. Data elements of interest extracted from the reviewed stud-
b. Studies including participants of any age were con- ies are described below:
sidered.
c. Studies that were conducted on animals were
excluded. Study and participant characteristics
III. Therapy: The study design and corresponding level of evidence
a. Behavioral interventions specifically targeting were appraised for each study. Levels of evidence were
improvement of the respiratory function were determined following the National Health and Medical
included. Research Council (NHMRC) guidelines for evidence
b. Interventions that combined respiratory exercises hierarchy.24 The methodological quality of each study
with voice exercises (or any other type of voice was assessed using the Downs and Black's checklist.25
intervention, such as medical, surgical, or pharma- This checklist was developed to allow methodological
ceutical) were not included in the review, unless the quality assessment of both randomized and nonrandom-
study design allowed for the isolation of the respira- ized trials by evaluating the (1) quality of reporting; (2)
tory intervention as an independent variable. Respi- external validity; (3) internal validity bias; (4) internal
ratory interventions that included speech tasks for validity confounding; and (5) power. Its measure, the
generalization purposes solely, without attention Quality Index Score (QIS), was found to have a strong
given to vocal function, were included. internal consistency, a good test-retest and inter-rater reli-
c. Studies on cough and exercise-induced laryngeal ability, and a good criterion validity.25 The checklist was
obstruction were excluded. adapted for the purpose of this study (see Appendix 1).
d. Studies on glossopharyngeal breathing (or glosso- Item 19 was modified because very few studies reported
pharyngeal insufflation) were excluded because of compliance data. Therefore, it was changed from “was
their specificity to certain patient populations. compliance with the intervention(s) reliable?” to “was
Glossopharyngeal breathing is a technique in which compliance with the intervention(s) reported?”. Item 27
patients with respiratory muscle dysfunction use was modified because very few studies reported a sample
their lips, tongue, mouth, and pharyngeal muscles size justification. It was changed from “did the study have
to send the air from the oral cavity to the lungs and sufficient power to detect a clinically important effect
increase their vital capacity.21−23 where the probability value for a difference being due to
e. There were no restrictions regarding who adminis- chance is less than 5%?” to “did the study include a sam-
tered the respiratory exercises. ple size justification?”.
IV. Outcome measures: Studies reporting any subjective or A description of the participants’ main inclusion criteria
objective voice outcome measures were considered for (ie, diagnosis, voice disorder/symptoms, or occupation) was
inclusion. Outcomes that were reported post-treatment documented. Other participant characteristics extracted
only (ie, post-treatment questionnaire) were excluded consisted of: gender repartition, age mean and range, and
from the results. total sample size.
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Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 5

Records idenfied through


database search on February
6th 2018
(n=759)

Records aer duplicates Addional records idenfied


removed through other sources

(n=650) (n=9)

Records screened Records excluded

(n=659) (n=509)

Full-text arcles assessed for Full-text arcles excluded


eligibility (n=127)

(n=150) 4 failed criterion Ib


55 failed criterion IIIa
25 failed criterion IIIb
20 failed criterion IIIc
3 failed criterion IIId
11 failed criterion IV
Studies included in the 1 failed criterion Va
review 7 failed criterion Vb
1 arcle was not available
(n=23)

FIGURE 1. PRISMA flow diagram.20

Intervention characteristics more than one intervention, results of all interventions were
All interventions administered in the studies were reported, related for comparison purposes.
but only the respiratory interventions were described in
detail by relating tasks, instructions, and loads of training.
The total duration of treatment, frequency of treatment, RESULTS
and length of each session were reported for the respiratory Search results
interventions. Lastly, the main categories of physiological The screening process is depicted in an adaptation of the
targets were extracted. PRISMA flow chart20 in Figure 1. The chart shows the
number of articles that were found through the database
search and through the screening of reference lists. The
number of articles excluded at each step of the process is
Outcomes and results indicated and the reasons for exclusion are provided. Of
Voice and respiratory outcomes that were assessed before the 150 articles that underwent full-text screening, 127
and after the intervention were reported for each study, and were excluded. Four articles were masters or doctorate
the key results were described. When different studies theses or conference proceedings and were therefore
reported results from the same source of participants, only excluded because they were not peer reviewed. Fifty-five
results for different outcomes were reported to avoid repeti- articles did not include a behavioral intervention targeting
tion and bias. P values and effect sizes were reported when improvement of the respiratory function. Twenty-five stud-
available. If no statistical analyses were conducted, descrip- ies contained a respiratory intervention but did not isolate
tive key findings were summarized. When a study comprised it as the independent variable. Twenty articles were studies
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6 Journal of Voice, Vol. &&, No. &&, 2019

on cough or exercise-induced laryngeal obstruction, and studies included participants with some type of voice
three were studies on glossopharyngeal breathing. These impairment, either officially diagnosed or not. Respiratory
were excluded because they apply only to specific patient interventions were tested on: individuals with Parkinson dis-
populations. One paper did not assess both pre- and post- ease (PD)29−36; hypotonic children with low vocal intensity
intervention voice outcomes, and eleven papers did not levels37; individuals with multiple sclerosis38,39; children
report any voice outcomes. Seven studies were excluded with spastic cerebral palsy40; individuals with bilateral vocal
because they were case studies or single-subject designs nodules41,42; individuals with traumatic motor and sensory
with less than five participants. Finally, one article was complete tetraplegia43; professional voice users with or
not available. without reported vocal complaints44−46; individuals with
Twenty-three articles met all the criteria and are nonspecified dysphonia47; and individuals with MTD.48 Of
included in the review. Inter-rater reliability for the first the eight articles involving individuals with PD, seven were
screening phase (title and abstract) was 98.46%. Inter- based on the same initial sample of participants.29−35 The
rater reliability for the second screening phase (full text two articles on individuals with bilateral vocal nodules,41,42
review) was 96.67%. After discussion, consensus was as well as the two articles on professional classical sing-
reached between the raters and agreement was 100% for ers,26,27 were also based on common samples.
both screening phases.

Age and gender repartition


Study characteristics Age of the participants was strongly influenced by the diag-
Designs and levels of evidence noses. For example, although no experiment specifically tar-
Of the 23 included studies, 12 are RCTs, six are cross-over geted elderly participants, those studying individuals with
trials, two are repeated measures designs, two are single- PD had the highest participant age means.29−36 Only two
subject designs, and one is a nonrandomized trial. articles included individuals under 18 years old, with the
The design and associated level of evidence for each youngest participant being nine years old.37,40 The age
paper are presented in Table 2. range across the 23 reviewed studies was 9−83 years old,
and the average and median, from the 19 articles that
Quality index score reported age mean, were 47.4 and 45.8, respectively.
The QIS for each study are displayed in Figure 2. The Four studies did not report the gender repartition of the
studies are grouped in five categories because the Downs participants.30,34,37,45 Of the studies that did report gender
and Back's quality assessment checklist was adapted based repartition, seven had a majority of males and seven had a
on study design (see Appendix 1). Because the checklist is majority of females. Five articles included only female par-
primarily designed for RCTs, cohort studies, and case-con- ticipants.26−28,41,42
trol studies, some of its items do not apply for all of the
designs included in the review. In fact, questions based on
Total sample size
the assumption that there is more than one intervention
The sample sizes of the included articles varied from five
group in the study were removed for cross-over designs,
participants,26,27,39 which was the minimum for inclusion in
repeated measures designs, and single-subject designs.
this review, to 77 participants.45 The mean sample size of
Appendix 1 details which items were excluded for specific
the reviewed studies was 23 and the median was 20.
study designs, thus affecting the denominator of the results
below. Appendix 1 also details the scoring choices for each
item. Respiratory interventions
The mean total scores are 17.7/28 for RCTs (range: Types of intervention
14−21; median:18), 14/25 for cross-over designs (range: Four different interventions aimed at improving the
12−19; median:13.5); 11.5/23 for repeated measures designs strength of the respiratory muscles by using a device offer-
(range: 11−12; median:11.5), 14/23 for single-subject ing resistance during expiration or inhalation.
designs (range: 12−16; median:14), and 13/28 for the non- The interventions using a breathing device were: (1) expi-
randomized trial. ratory muscle strength training (EMST) or an adaptation
of, in eight studies28,36−39,44−46; (2) inspiratory muscle
strength training (IMST), in two studies28,43; (3) incentive
Participant characteristics
spirometry, in two studies40,43; and (4) isocapnic hyperpnea,
The participant characteristics summarized in this section
in one study.43 The details of the respiratory interventions
are detailed in Table 2.
are described in Table 3.
The remaining respiratory interventions included various
Main inclusion criteria exercises and aimed at achieving one or more of the follow-
Only three studies were conducted exclusively on vocally ing: increasing respiratory effort, coordinating respiration
healthy participants; these were professional classical sing- with phonation, improving breathing pattern, or facilitating
ers26,27 and classical singing students.28 The remaining effort-free breathing. These interventions were: (1)
Maude Desjardins and Heather Shaw Bonilha
TABLE 2.
Study and Participant Characteristics
Age
Reference Design (Level of Mean (Range
Number Author, year Evidence*) Participant Description Number and Gender Total N or SD)
29 Baumgartner RCT (II) Individuals with PD with at G1: 2 females, 5 males N = 20 G1: 64.8 (§9.6)
et al (2001) least moderate breathiness G2: 2 females, 11 males G2: 66.7 (§7.8)
and hoarseness (subset of
Ramig et al 1995)
37 Cerny et al Repeated meas- Children with expressive lan- 9 (gender NR) N=9 11 (9−14)
(1997) ures (III-3) guage impairment, soft voice
and short utterances
38 Chiara et al Non-randomized G1: Individuals with multiple G1: 14 females, 3 males N = 31 G1: 48.9 (§7.61)
(2007) trial (III-2) sclerosis G2: 12 females, 2 males G2: 44.1 (§7.64)
G2: Healthy controls

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40 Choi et al (2016) RCT (II) Children with spastic cerebral G1: 10 females, 15 males N = 48 G1: 11.4 (§2.3)
palsy G2: 12 females, 11 males G2: 11.7 (§2.5)
26 Collyer et al Cross-over trial Professional classical singers 5 females N=5 NR (31−44)
(2009) (III-2)

The Impact of Respiratory Exercises on Voice Outcomes


27 Collyer et al Cross-over trial Professional classical singers 5 females N=5 NR (31−44)
(2011) (III-2)
36 Darling-White Single-subject Individuals with PD 3 females N = 12 75 (66−82)
and Huber design (IV) 9 males
(2017)
42 Holmberg et al Cross-over trial Individuals with bilateral vocal 11 females N = 11 23.3 (19−35)
(2001) (III-2) nodules
41 Holmberg et al Cross-over trial Individuals with bilateral vocal 10 females N = 10 24.2 (19−35)
(2003) (III-2) nodules
39 Johansson et al Single-subject Individuals with multiple 2 females, 3 males N=5 54.6 (31−74)
(2012) design sclerosis
(IV)
43 Mueller et al RCT (II) Individuals with traumatic G1: 2 females, 6 males N = 24 G1: 35.2 (§12.7)
(2013) motor and sensory complete G2: 2 females, 6 males G2: 33.5 (§11.7)
tetraplegia G3: 2 females, 6 males G3: 41.6 (17.0)
44 Pereira et al RCT (II) Teachers with or without voice G1: 12 females, 5 males N = 31 G1: 43.6 (§11.4)
(2015) problems G2: 12 females, 2 males G2: 45.8 (§8.1)
31 Ramig et al RCT (II) Individuals with PD G1: 7 females, 12 males N = 45 G1 : 65.6 (8.9)
(1995) G2: 5 females, 21 males G2 : 63.5 (11.5)
32 Ramig and RCT (II) Individuals with PD G1: 1 female, 6 males N = 17 G1 : 63.7 (7.7)
Dromey (1996) (subset of Ramig et al 1995) G2: 1 female, 9 males G2 : 62.7 (10.5)
30 Ramig et al RCT (II) Individuals with PD G1: 13 (gender NR) N = 35 G1: 65.31 (§8.89)
(1996) (subset of Ramig et al 1995) G2: 22 (gender NR) G2: 63.23 (§11.87)
33 Ramig et al RCT (II) Individuals with PD G1: 5 females, 7 males N = 33 G1 : 63.3 (§7.1)
(2001) (subset of Ramig et al 1995) G2 : 4 females, 17 males G2: 61.3 (§11.4)
(Continued)

7
8
TABLE 2(Continued )
Age
Reference Design (Level of Mean (Range
Number Author, year Evidence*) Participant Description Number and Gender Total N or SD)
28 Ray et al (2018) Single-subject Classically trained singing 6 females N=6 28 (24−39)
cross-over students
design (IV)
45 Roy et al (2003) RCT (II) Full time teachers with past or G1: 24 (gender NR) N = 64 G1: 42.0 (§10.6)
present voice problems G2: 28 (gender NR) (N = 77 for the G2: 44.1 (§14.4)

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G3: 25 (gender NR) intention-to- G3: 44.2 (§9.5)
treat
analysis)
34 Sapir et al (2002) RCT (II) Individuals with PD G1: 13 (gender NR) N = 35 G1: 65.31 (§8.89)
(subset of Ramig et al 1996) G2: 22 (gender NR) G2: 63.23 (§11.87)
47 Schaeffer and Repeated Individuals with dysphonia (as 17 females, 3 males N = 20 Females: 36 (NR)
Sunyoung measures perceptually judged by the PI) Males: 40 (NR)
(2017) (III-3)
35 Smith et al RCT (II) Individuals with PD 5 females, 17 males N = 22 NR (49−76)
(1995) (subset of Ramig et al 1995)
46 Tsai et al (2016) RCT (II) Medical professionals (who G1: 14 females, 1 male N = 29 G1: NR (20−39)
use their voice for minimum G2: 12 females, 2 males G2: NR (20−44)
4 hours/day at work) with
self-reported voice problems
48 Van Lierde et al Cross-over trial Individuals with muscle ten- 4 females, 6 males N = 10 58 (18−65)
(2010) (III-2) sion dysphonia

Journal of Voice, Vol. &&, No. &&, 2019


* The level of evidence was determined following the National Health and Medical Research Council’s guidelines for evidence hierarchy.
G1, group 1; G2, group 2; G3, group 3; NR, not reported; PD, Parkinson disease; PI, principal investigator; RCT, randomized controlled trial; SD, standard deviation.
ARTICLE IN PRESS
Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 9

Quality Assessment Index


28

26

24

22

20

18

16

14

12

10

Randomized- Cross-over Repeated measures Single-subject Non-randomized


controlled trials designs designs designs trials

FIGURE 2. Quality Assessment Index.

respiratory effort treatment (RET), in seven studies29−35; (2) until their maximum respiratory pressure values reached a
abdominal directives, in two studies26,27; (3) 00 easy breath- plateau (differed by less than 5% across three sessions).
ing00 (respiration component of a broader voice therapy pro- The training regimens of the respiratory interventions,
gram), in two studies41,42; (4) stimulation training, in one with and without a respiratory device, are detailed below.
study47; and (5) vocalization with abdominal breath sup-
port, in one study.48 These interventions all contained Interventions with a respiratory device. The fre-
speech tasks for purposes of generalization of the respira- quency of the interventions using a resistance device varied
tory exercises (without any attention given specifically to between three and seven times a week, with a majority of
vocal function). The details of these interventions are the interventions having a frequency of five times a week.
described in Table 3. Sessions were supervised by a therapist once or twice a week
or not at all, with the exception of Mueller et al’s study43
involving participants with complete tetraplegia, and Cerny
Duration, frequency, and load of the interventions et al’s study37 on hypotonic children, for whom all sessions
The duration of the intervention programs varied from 1 were supervised.
week (one session) to 8 weeks; with most of the interventions EMST and IMST studies used threshold pressure devices
lasting between 4 and 8 weeks and averaging 4.14 weeks in which a spring-loaded valve blocks the airflow until a suf-
(median of 4 weeks). In one article, Ray et al28, the interven- ficient pressure is achieved by the participant, allowing the
tion did not have a set duration; instead, participants trained valve to open and the air to flow. The threshold pressure
10
TABLE 3.
Interventions
Duration of the
Reference Respiratory Respiratory Main Physiological
Number Study Interventions Description of the Respiratory Interventions Interventions Targets
29 Baumgartner Respiratory Participants were trained to increase their respiratory 4 weeks -Increase of respira-
et al (2001) effort effort. Tasks included: maximum inhalation and 4£/week (+daily tory effort
treatment exhalation, sustained /s/ and /f/, sustained intra-oral homework) -Coordination with
air pressure with the IOPI, visual feedback of ribcage 1 hour phonation
and abdomen excursions, and reminders to take
deep and frequent breaths during speaking tasks
and to maximize respiratory effort (00 think breathe00 ).
The first half of the session consisted of drills, and
the second half consisted of carryover to speech
tasks.

ARTICLE IN PRESS
37 Cerny et al Threshold EMST The children wore a face mask with a spring-loaded 6 weeks -Strengthening of the
(1997) valve during academic activities. Initial load: 2.5 5£/week respiratory muscles
cmH20. The load was increased based on bi-weekly 15 minutes
measures of MEP: if MEP had increased by more
than 10%, the threshold was increased by 2.5 cmH20,
until a maximum of 7.5 cmH20 was reached.
38 Chiara et al Threshold EMST Participants were instructed to breathe in and out 8 weeks -Strengthening of the
(2007) through the device and to maintain their exhalation 5£/week (once under respiratory muscles
for at least 5 seconds. supervision)
The load was set based on the participants’ MEP. 1st 4 sets of 6 breaths
week: 40% of MEP; 2nd week: 60% of MEP; 3rd − 8th
week: 80% of MEP.
40 Choi et al (2016) Flow-oriented Participants were instructed to inhale slowly in the 4 weeks -Strengthening of the
Incentive spirometer until the ball lifted, and to hold their 7£/week (twice under respiratory muscles
spirometer breath for as long as possible (or at least 5 seconds). supervision) -Stretching and open-
exercise The ball served as visual feedback. The flow rate was 10 training sessions of ing of airways to

Journal of Voice, Vol. &&, No. &&, 2019


increased in increments of 100 mL/sec when the par- 10−15 breaths/day improve pulmonary
ticipant could maintain the ball lifted for at least 5 function
seconds, until a maximum of 600 mL/sec was
reached.
26 Collyer et al Abdominal Abdomen-in: the singer was instructed to steadily pull 1 session of -Abdomen-in: Breath-
27 (2009) directives: the abdominal wall inward during each singing 1−1.5 hours ing pattern
Collyer et al habitual, phrase. -Abdomen-out:
(2011) abdomen-in, Abdomen-out: the singer was instructed to steadily Breathing pattern
abdomen-out expand the abdominal wall during each singing
phrase.
3 singers were given the abdomen-in condition first
and 2 singers were given the abdomen-out
condition first.
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 3(Continued )
Duration of the
Reference Respiratory Respiratory Main Physiological
Number Study Interventions Description of the Respiratory Interventions Interventions Targets
36 Darling-White Threshold EMST Participants were asked to inhale deeply and then 4 weeks -Strengthening of the
and Huber exhale forcefully in the threshold device. The load 5£/week (once under respiratory muscles
(2017) was set at 75% of the participants’ MEP or at the supervision)
highest level for successful completion of the task, 5 sets of 5 breaths
and was adjusted once a week during the 4-week
training period.
00
42 Holmberg et al Easy breathing00 Easy and relaxed breathing; timing between respira- 3 weeks (for the -Facilitation of effort-
41 (2001) tion and initiation of phonation; inhalation of a nor- breathing compo- free breathing
Holmberg et al mal amount of air prior to initiation of phonation; nent only) -Coordination with
(2003) inhalation at appropriate moments. There was a 1£/week (+2 £ 15 phonation
progression of tasks from rest breathing to conver- minutes of daily
sational speech. homework)

ARTICLE IN PRESS
39 Johansson et al Threshold EMST Participants were instructed to forcefully exhale into 6 weeks -Strengthening of the
(2012) the device for 5 breaths at a time. The load was (2 participants had an respiratory muscles
adjusted at each supervised session according to the additional training
participants’ MEP (no further details provided). The phase of 9−10

The Impact of Respiratory Exercises on Voice Outcomes


maximum load of the device was 20 cmH20 for the weeks)
first 6 weeks, and 150 cmH20 for the following 10 5£/week
weeks (only 2 participants received this second 5 sets of 5 breaths
treatment phase).
43 Mueller et al G1: Inspiratory IRT: Participants were instructed to inhale maximally 8 weeks -IRT: strengthening of
(2013) resistance in the device for 90 breaths. Visual feedback was 4£/week the respiratory
training (IRT) provided, and inhalations achieving less than 80% of 10 minutes muscles
(threshold the subject’s MIP had to be repeated. MIP was (all sessions were -IH: increase of respi-
IMST) assessed at the beginning of each session. supervised) ratory muscle endur-
G2: Respiratory IH: By breathing in the device, participants hyperventi- ance
muscle endur- lated for 10 minutes at 40−50% of their MVV. The -IS: used as placebo
ance training breathing frequency was increased by 1 breath/mi-
using iso- nute every second or third session. Visual and
capnic hyper- acoustic feedback of the breathing volume and fre-
pnea (IH) quency was provided.
G3: Incentive IS: Participants were instructed to inhale from residual
spirometry (IS) volume to total lung capacity 16 times in the spirom-
used as etry device, with 30−40 seconds of rest between
placebo breaths.
44 Pereira et al Breathing train- Participants in the breathing training group wore a 6 weeks -Strengthening of the
(2015) ing (EMST with nasal clip and were instructed to breathe deeply 5£/week (once a day respiratory muscles
mucus clear- through the mouth and then exhale trough a mucus before teaching their
ance device) clearance device. first class
13 minutes
5 sets of 5 breaths

11
(Continued)
12
TABLE 3(Continued )
Duration of the
Reference Respiratory Respiratory Main Physiological
Number Study Interventions Description of the Respiratory Interventions Interventions Targets
31 Ramig et al Respiratory Participants were trained to increase their respiratory 4 weeks -Increase of respira-
32 (1995) effort effort. Tasks included: maximum inhalation and 16 sessions (+daily tory effort
30 Ramig and treatment exhalation, sustained /s/ and /f/, sustained intra-oral homework) -Coordination with
33 Dromey (1996) air pressure with the IOPI, visual feedback of ribcage 50 minutes phonation
Ramig et al and abdomen excursions, and reminders to take
(1996) deep and frequent breaths during speaking tasks
Ramig et al and to maximize respiratory effort (00 think breathe00 ).
(2001) The first half of the session consisted of drills, and
the second half consisted of carryover to speech
tasks.
28 Ray et al (2018) Threshold IMST, IMST and EMST: Participants were instructed on how 7£/week -IMST: Strengthening
threshold to use the IMST and the EMST devices. The load was 5 sets of 5 breaths of the respiratory

ARTICLE IN PRESS
EMST, and adjusted to 80% of the subjects’ MIP (for IMST) and Supervised session muscles
combined MEP (for EMST) at each supervised session. Partici- were space 5 to -EMST: Strengthening
effects pants were assigned to start either with IMST or 10 days apart of the respiratory
EMST. When their MIP or MEP was stable for 3 con- muscles
secutive supervised session (§5%), the type of train-
ing was changed.
45 Roy et al (2003) Respiratory Participants were instructed to breathe in completely 6 weeks (1 supervised -Strengthening of the
muscle training and then exhale forcefully in the threshold pressure session at weeks respiratory muscles
(threshold device. The trainer was set at 80% of the partic- 1,2,4 and 6)
EMST) ipants’ baseline MEP and was adjusted during two 5£/week
supervised sessions, at week 2 and 5 sets of 5 breaths
week 4.
34 Sapir et al (2002) Respiratory Participants were trained to increase their respiratory 4 weeks -Increase of respira-
effort effort. Tasks included: maximum inhalation and 16 sessions (+daily tory effort
treatment exhalation, sustained /s/ and /f/, sustained intra-oral homework) -Coordination with

Journal of Voice, Vol. &&, No. &&, 2019


air pressure with the IOPI, visual feedback of ribcage 50 minutes phonation
and abdomen excursions, and reminders to take
deep and frequent breaths during speaking tasks
and to maximize respiratory effort (00 think breathe00 ).
The first half of the session consisted of drills, and
the second half consisted of carryover to speech
tasks.
47 Schaeffer and Stimulation The stimulation training consisted of four steps: coor- 1 session -Coordination with
Sunyoung training dinating respiration without phonation, coordinat- phonation
(2017) ing respiration and phonation through a hierarchy of -Breathing pattern
speaking tasks, pulling in the abdominal muscles
without phonation, pulling in the abdominal
muscles with phonation through a hierarchy of
tasks.
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 3(Continued )
Duration of the
Reference Respiratory Respiratory Main Physiological
Number Study Interventions Description of the Respiratory Interventions Interventions Targets
35 Smith et al Respiratory Participants were trained to increase their respiratory 4 weeks -Increase of respira-
(1995) effort effort. Tasks included: maximum inhalation and 16 sessions (+daily tory effort
exhalation, sustained /s/ and /f/, sustained intra-oral homework) -Coordination with
air pressure with the IOPI, visual feedback of ribcage 50 minutes phonation
and abdomen excursions, and reminders to take
deep and frequent breaths during speaking tasks
and to maximize respiratory effort (00 think breathe00 ).
The first half of the session consisted of drills, and
the second half consisted of carryover to speech
tasks.
46 Tsai et al (2016) EMST Participants were wearing a nose clip and were 5 weeks -Strengthening of the
instructed to inhale maximally before exhaling 3£/week respiratory muscles

ARTICLE IN PRESS
forcefully into the device. The load was set at 75% of 5 sets of 5 breaths
the participants’ MEP and was adjusted every week.
48 Van Lierde et al Vocalization To start, the breathing pattern of the participants was 1 session -Breathing pattern
(2010) with abdomi- identified. Then the participants practiced abdomi- 45 minutes -Coordination with

The Impact of Respiratory Exercises on Voice Outcomes


nal breath nal/diaphragmatic breathing while sitting and using phonation
support tactile and visual feedback of the abdomen. The
breathing pattern was then practiced with phona-
tion, using a hierarchy of tasks (sounds /z/ and /v/,
syllables, short and long words, and counting).
EMST, expiratory muscle strength training; IMST, inspiratory muscle strength training; IOPI, Iowa Oral Performance Instrument; LSVT, Lee Silverman Voice Treatment; MIP, maximum inspiratory pressure;
MEP, maximum expiratory pressure; MVV, maximal voluntary ventilation.

13
ARTICLE IN PRESS
14 Journal of Voice, Vol. &&, No. &&, 2019

was based on the participants' maximum expiratory pres- Outcomes


sure (MEP) in the case of EMST, and maximum inspiratory Respiratory outcomes
pressure (MIP) in the case of IMST. The load was set at Respiratory outcomes were reported in 15 out of 23 papers.
75% of the participants’ MEP in two studies,36,46 at 80% of From these papers, three reported respiratory data from the
the participants’ MIP or MEP in three studies,28,43,45 and at same source of participants.30−32 Therefore, the respiratory
10% of the participants’ MEP (up to a maximum of 7.5 results of 13 articles will be discussed.
cmH2O) in one study37. In Chiara et al’s experiment,38 the Three main categories of respiratory outcomes were
threshold was set at 40% of the children's MEP for the first extracted from the reviewed articles:
week, at 60% of their MEP for the second week, and at 80%
of their MEP for weeks 3−8. The device was adjusted 1) Spirometry measures were reported in five studies.
according to the participants’ MEP in Johansson et al’s 2) Maximum respiratory pressure measures were
study,39 but no further details were provided. Lastly, in the reported in eight articles. Indexes such as MIP and
study by Pereira et al44 using a mucus clearance device, no MEP indirectly measure respiratory muscle strength
load adjustment was mentioned. The most common instruc- by appraising the pressures at the mouth, by using
tion to the participants was to complete five sets of five a hand-held pressure meter or a manometer.49 To
breaths with a pause between each set.28,36,39,44−46 Chiara et directly measure the number and the size of the
al’s instructions were slightly different and involved four respiratory muscle fibers before and after an inter-
sets of six breaths per practice session. In Mueller et al’s vention would be invasive and would not provide
study,43 participants were asked to perform 90 breaths per clinically meaningful information, which is why
day (or 10 minutes of training). In Cerny et al’s study,37 maximum respiratory pressure measures are com-
children wore a face mask and performed their exercises for monly used in the respiratory literature.
15 minutes during their daily activities. 3) Kinematic measures were reported in three articles.
The two studies involving spirometer exercises had a dif-
ferent training regimen. In Choi et al’s study,40 children In addition, auditory-perceptual judgments of breath
were instructed to perform 10 training sessions of 10−15 management were reported in one article, self-assessments
breaths in the spirometer, daily. The flow rate was increased of subjective breathing parameters were reported in one
by 100 mL/s (up to a maximum of 600 mL/s) when the child article, and respiratory waveforms were reported in one
could sustain the ball for at least 5 sec. In Mueller et al’s article.
study,43 in which spirometer exercises represented the pla- MEP was the most frequent respiratory measure,
cebo intervention, participants with tetraplegia were asked reported in eight articles, followed by vital capacity (VC) or
to inhale from residual volume to total lung capacity forced vital capacity (FVC), reported in five articles. The
16 times per training session. No details were provided details of the respiratory outcomes are depicted in Table 4.
regarding adjustment of the flow rate. In the same study,
some participants were assigned to isocapnic hyperpnea,
and were instructed to hyperventilate in the device during Voice outcomes
10 minutes at 40−50% of their maximum voluntary ventila- Outcome measures pertaining to voice were grouped in five
tion, at each session. The breathing frequency was increased categories: (1) acoustic measures, reported in 14 articles; (2)
by one breath/minute every second or third session. aerodynamic and duration measures, reported in 12 articles;
(3) auditory-perceptual judgments, reported in six articles;
(4) self-assessments, reported in five articles; and (5) visual
Interventions without a respiratory device. The examination, reported in one article. In addition, one article
RET program for patients with Parkinson disease was reported glottographic measures and one article reported
administered four times a week in sessions of 50 minutes, the dysphonia severity index. Overall, the most commonly
and participants were given homework to practice on their reported voice outcomes were measures of voice intensity,
own on a daily basis.29−35 In Holmberg et al’s studies,41,42 reported in 13 studies, and maximum phonation time
participants with vocal nodules saw the therapist once a (MPT), reported in seven studies.
week, and a total of three sessions were allocated to the res-
piration component of the therapy program. Participants
were given homework to practice daily in two sessions of 15 Efficacy of the interventions
minutes. Results are reported in Table 4 and include P values and
Four articles reported a respiratory intervention occur- effect sizes when available. Only voice and respiratory out-
ring during a single session.26,27,47,48 The duration of the comes that were assessed before and after the intervention
unique session was of 45 minutes in Van Lierde et al’s arti- are reported. When a study comprised more than one inter-
cle48 and of 1 hour to one hour and a half in both of Collyer vention, results of all interventions are reported for compar-
et al’s studies.26,27 The duration of the stimulation ison purposes. When the same outcome measure was used
training session in Schaeffer and Sunyoung's paper was not in multiple studies for the same source of participants, it is
specified.47 only reported once. The most frequently used outcome
Maude Desjardins and Heather Shaw Bonilha
TABLE 4.
Outcome Measures and Results
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
29 Baumgartner G1: Respiratory Auditory-perceptual judgment N/A
et al (2001) effort treat- Breathiness: no significant improvement was
ment (RET) found in the RET group, whereas the LSVT group
G2: LSVT improved significantly (breathiness decreased)
(P = 0.025).
Hoarseness: no significant improvement was
found in the RET group, whereas the LSVT group
improved significantly (hoarseness decreased)
(P = 0.005).
37 Cerny et al Threshold Acoustic Spirometry
(1997) EMST SPL: a sig. pre-post improvement (increase) was FVC: NS
found in the comfortable condition (P < 0.0001); it

ARTICLE IN PRESS
FEV1: NS
remained significant at 3 weeks follow-up Maximum respiratory pressure
(P < 0.03). A sig. pre-post improvement was also MEP: there was a significant increase from
found in the loud condition (P < 0.0001); it pre- to post- (P = 0.0003) and MEP

The Impact of Respiratory Exercises on Voice Outcomes


remained significant at 3 weeks follow-up remained elevated at 3 weeks follow-up
(P < 0.004). (P < 0.02).
Aerodynamic and duration Expiratory muscle endurance: NS
Psub: a sig. pre-post improvement (increase) was
found in the comfortable (P < 0.005) and loud
(P < 0.01) conditions.
Syllables/breath: NS
38 Chiara et al G1 and G2: Aerodynamic and duration Maximum respiratory pressure
(2007) Threshold MPT (comfortable and loud conditions): there was MEP: the improvement in MEP (increase)
EMST no improvement in MPT at post-treatment in par- was significant from pre- to post-treat-
ticipants with multiple sclerosis. ment (P = 0.0001) and from pre-treatment
Words/minute (comfortable and loud conditions): to 4-week follow-up (P = 0.0001). No
EMST resulted in an improvement (increase) in group x assessment interaction was
words per minute at post-treatment (P = 0.0006). found between the subjects with multi-
The significant increase was maintained at 4- ple sclerosis and the healthy controls.
week follow-up (P = 0.0001).
Self-Assessment
V-RQOL: EMST did not improve V-RQOL in patients
with multiple sclerosis.
40 Choi et al G1: Flow-ori- Aerodynamic and duration Spirometry
(2016) ented Incen- MPT: there was a significant improvement FVC: there was a significant improvement
tive spirome- (increase) from pre- to post-treatment (P = 0.001). (increase) from pre- to post-treatment in
ter exercise The increase was sig. greater in the experimental liters (P = 0.000) and in % predicted
(ISE) (ISE) vs the control group (P = 0.008). (P = 0.001). The increase was sig. greater
in the experimental vs the control group
(Continued)

15
16
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
G2: control in liters (P = 0.005) and in % predicted
group (P = 0.031).
FEV1: there was a significant improve-
ment (increase) from pre- to post-treat-
ment in liters (P = 0.005) and in %
predicted (P = 0.009). The increase was
sig. greater in the experimental vs the
control group in liters (P = 0.017) and in
% predicted (P = 0.036).
FEV1/FVC: NS
PEF: there was a significant improvement
(increase) from pre- to post-treatment
(P = 0.003).

ARTICLE IN PRESS
26 Collyer et al Abdominal Acoustic Kinematics
(2009) directives: Normalized Leq: NS. Breathing directives did not Abdominal dimensions (at initiation, at
Habitual impact the loudness of the songs. termination, excursion): breathing direc-
Abdomen-in tives had a sig. effect on abdomen
Abdomen-out dimension at initiation (P < 0.001) and on
abdomen excursion (P = 0.001), but not
on abdomen at termination of the
phrase. Singers began phrases with a
larger than usual abdomen dimension in
the abdomen-in condition and with a
smaller than usual abdomen dimension
in the abdomen-out condition.
Ribcage dimensions (at initiation, at ter-
mination, excursion): breathing direc-
tives had a sig. effect on ribcage

Journal of Voice, Vol. &&, No. &&, 2019


dimension at initiation (P < 0.001) and on
ribcage excursion (P < 0.001), but not on
ribcage at termination of the phrase.
Pairwise comparisons showed that the
habitual and abdomen-in conditions
were not different, but that they both dif-
fered from the abdomen-out condition.
Ribcage changes counterbalanced abdo-
men changes.
Lung volumes (at initiation, at termina-
tion, excursion): NS. Breathing directives
had no effect on lung volume at initia-
tion, lung volume at termination, and
lung volume excursion.
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
27 Collyer et al Abdominal Auditory-perceptual judgment Auditory-perceptual judgment
00
(2011) directives: Standard of singing00 : there was a significant main 00
Standard of breath management00 : There
Habitual effect for breathing directive (P = 0.019) and for was a significant main effect for singer (P
Abdomen-in singer (P < 0.001). The interaction effect of < 0.001). The main effect for breathing
Abdomen-out breathing directive x singer was significant directive was not significant. There was
(P < 0.001); indicating that the effect of the breath- an interaction effect of breathing direc-
ing directive was significant only for some partici- tive x singer (P < 0.001); indicating that
pants (as shown by either an increase or a the effect of the breathing directive was
decrease in ratings). significant only for some participants (as
shown by either an increase or a
decrease in ratings).
36 Darling-White Threshold *Effect sizes greater than §1.00 were considered *Effect sizes greater than §1.00 were con-
and Huber EMST significant* sidered significant*

ARTICLE IN PRESS
(2017) Acoustic Maximum respiratory pressure
SPL: 2/9 participants had significant improvement MEP: a significant improvement (increase)
(increase) following treatment, while 2 partici- was found for 9 participants (ES ranging
pants had a significant decrease (ES ranging from from d = 4.14 to d = 19.20). 3 participants

The Impact of Respiratory Exercises on Voice Outcomes


d = ¡1.95 to d = 4.85. had a significant decrease in MEP and
Aerodynamic and duration were excluded from the other analyses
Utterance length: 3/9 participants had significant (ES ranging from d = ¡3.98 to d = ¡1.74).
increase for utterance length, while 1 participant Kinematics
had a significant decrease (ES ranging from Lung volumes (at initiation, at termina-
d = ¡10.88 to d = 19.50). tion, excursion): 7/8 participants had
significant effect sizes for lung volume
at initiation (ES ranging from
d = ¡37.44 to d = 1.74), but the direction
of the change was inconsistent. 4/8
participants had significant effect sizes
for lung volume at termination (in the
same direction as lung at initiation
changes) (ES ranging from d = ¡18.37
to d = 1.59). 4/8 participants had signifi-
cant effect sizes for lung excursion (2
positive and 2 negative) (ES ranging
from d = -21.28 to d = 7.38).
00
42 Holmberg Easy breath- Auditory-perceptual judgement N/A
et al (2001) ing00 press/hyperfunction, breathiness, aphonic instan-
Vocal hygiene ces, lack of sonority, instability, gratings, rough-
Direct facilita- ness, vocal fry/creaks, scrape, overall dysphonia:
tion A sig. improvement (decrease) following the res-
Relaxation piration component was found for the following
Carryover parameters: press (P = 0.012), and vocal fry
phase (P = 0.013).

17
(Continued)
18
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
A sig. improvement (decrease) of the following
parameters was found following the “direct facili-
tation” component of the therapy: press
(p = 0.009) and gratings (p = 0.037). After the car-
ryover phase, the following parameters had
improved significantly: press (p = 0.004), gratings
(p = 0.045), roughness (p = 0.008), and vocal fry
(p = 0.010).
00
41 Holmberg Easy breath- Acoustic N/A
et al (2003) ing00 SPL: NS
Vocal hygiene F0: NS
Direct facilita- Relative amplitude differences between selected
tion peaks (h1-h2; h1-f1; hi-f3; f1-f3): NS

ARTICLE IN PRESS
Relaxation Aerodynamic and duration
Carryover Transglottal air pressure: NS
phase AC flow: NS
Closed quotient: NS
Speed quotient (time opening/time closing): NS
MFDR: NS
39 Johansson Threshold Acoustic Maximum respiratory pressure
et al (2012) EMST SPL sustained phonation: 4/5 subjects increased MEP: 5/5 subjects increased their MEP,
(only the their intensity during sustained phonation, with with ES ranging from d = 0.4 to d = 2.1
results from ES ranging from d = 0.5 to d = 3.6 (mean increase (mean increase of 6.9 cmH2O).
the 6-week of 4.6 dB).
treatment SPL reading: 3/5 subjects increased their intensity
phase, under- during reading, with ES ranging from d = 0.4 to
gone by all 5 d = 1.3 (mean increase of 0.6 dB).
subjects, are Coefficient of variation of F0: 3/5 subjects

Journal of Voice, Vol. &&, No. &&, 2019


reported decreased their CVF0, with ES ranging from
here) d = -0.7 to d = ¡1.2 (mean difference of ¡12.3%).
Aerodynamic and duration
MPT: 3/5 subjects increased their MPT, with ES
ranging from d = 0.2 to d = 3.6 (mean increase of
5.1 seconds).
43 Mueller et al G1: Inspiratory *Effect sizes greater than 0.8 were considered clini- *Effect sizes greater than 0.8 were consid-
(2013) resistance cally relevant* ered clinically relevant*
training (IRT) Acoustic Spirometry
(threshold Loudness: There was no sig. difference in mean TLC, RV, ERV, VC, FEV1, PEF, MVV: There
IMST) pre-post change between the 3 groups. was no sig. difference in mean pre-post
G2: Respiratory Aerodynamic and duration change between the 3 groups. However,
muscle MPT: There was no sig. difference in mean pre-post a high effect size was found for PEF for
endurance change between the 3 groups. the IRT group when compared to the IH
training using **Although baseline values and mean changes group (d = 0.80)
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
isocapnic were reported, the significance of pre-post Maximum respiratory pressure
hyperpnea changes was not assessed in the study, for all MIP: There was a significant difference in
(IH) variables. mean pre-post change for the IRT group
G3: Incentive when compared to the IH (P < 0.05;
spirometry d = 1.29) and IS (P < 0.05; d = 1.13) groups.
(IS) used as MEP: There was no sig. difference in mean
placebo pre-post change between the 3 groups.
Kinematics
Thorax mobility (T4 and T9 anterior-poste-
rior diameters, T4 and T9 intra-thoracic
areas): There was no sig. difference in
mean pre-post change between the 3
groups. However, high negative ES were

ARTICLE IN PRESS
found for T4 intra-thoracic area when
comparing IRT to IS (d = -0.85) and IRT to
IH (d = -0.87), meaning that IH and IS led to
greater increases of the intra-thoracic area

The Impact of Respiratory Exercises on Voice Outcomes


at the T4 level than IRT.
Self-assessment
Subjective breathing parameters: cough-
ing, secretion clearance, ability to blow
one’s nose, breathlessness during exer-
cises: There was no sig. difference in
mean pre-post change between the 3
groups. However, high ES were found
between the IRT and the IS group for "the
ability to blow one’s nose" (d = 0.97) and
between the IH and the IS group for
"breathlessness during exercise" (0.81).
44 Pereira et al G1: Breathing Acoustic N/A
(2015) training F0: After treatment, no significant difference was
(EMST with found in the breathing training group, whereas a
mucus clear- significant improvement (decrease) was found in
ance device) the vocal warm-up group (P = 0.049).
G2: Vocal Jitter: NS in both groups.
warm-up Shimmer: No significant improvement was found
in either group following treatment. Rather, there
was a significant pre- to post-treatment increase
in shimmer in the breathing training group
(P = 0.022).
GNE: NS in both groups.
Noise: NS in both groups.

19
(Continued)
20
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
Self-assessment
VHI-10: a significant pre- to post-treatment
improvement (decrease) was found for the
breathing training group (P < 0.001) and for the
vocal warm-up group (P = 0.007).
For all parameters, the average pre-post change
was not significantly different between the 2
groups.
31 Ramig et al G1: Respiratory Auditory-perceptual judgement Spirometry
(1995) effort treat- Loudness, monotonicity, hoarseness: The family FVC: No significant improvement was
ment (RET) ratings revealed only a significant improvement found in either group.
G2: LSVT (increase) in loudness, for both groups
(P = 0.029), but not in monotonicity and hoarse-

ARTICLE IN PRESS
ness.
Acoustic
SPL: Subjects in both groups significantly
improved (increased) their SPL during conversa-
tion (P = 0.001). Females and males in the LSVT
group increased SPL during reading, but only
females improved in the RET group. SPL during
sustained vowel was significantly increased in
the LSVT group only.
F0: Subjects from both groups significantly
increased their F0 during reading from pre- to
post-treatment (P = 0.001), but not during conver-
sation.
STSD: Subjects from both groups significantly
improved (increased) STSD during reading from

Journal of Voice, Vol. &&, No. &&, 2019


pre- to post-treatment (P = 0.001). Only subjects in
the LSVT group increased their STSD during con-
versation.
Aerodynamic and duration
MPT: Subjects from both groups significantly
improved (increased) their MPT from pre- to post-
treatment (P = 0.004).
Utterance duration: Subjects from both groups
significantly decreased their utterance duration
during reading (P = 0.001), but not during conver-
sation.
Pause duration: Only subjects in the RET group sig-
nificantly increased their pause duration during
reading. No significant improvement was found
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
for the conversation condition in either group.
Self-assessment
Loudness, monotonicity, hoarseness: A significant
improvement (reduction in severity) was found in
both groups for self-ratings of monotonicity and
hoarseness (P = 0.001). Only males in the LSVT
group and females in the RET group improved
(increased) their self-rated loudness.
32 Ramig and G1: Respiratory Acoustic [FVC: FVC values for the same patients
Dromey effort treat- SPL: SPL values for syllable repetition improved were reported in Ramig et al (1995).]
(1996) ment (RET) (increased) in the LSVT group and decreased in
G2: LSVT the RET group (sig. pre-post by treatment group
interaction; P = 0.042).

ARTICLE IN PRESS
[SPL values for conversation, reading, and sus-
tained phonation were reported in Ramig et al
(1995).]
Aerodynamic and duration

The Impact of Respiratory Exercises on Voice Outcomes


Psub: Psub values improved (increased) in the
LSVT group and decreased in the RET group (sig.
pre-post by treatment group interaction;
P = 0.003).
MFDR: MFDR values improved (increased) in the
LSVT group and decreased in the RET group (sig.
pre-post treatment group interaction; P = 0.001).
Glottographic Measures
OQ: NS for both groups.
EGGW-25: EGGW-25 values improved (increased)
in the LSVT group and decreased in the RET
group (sig. pre-post by treatment group interac-
tion; P = 0.003).
30 Ramig et al G1: Respiratory * Only long-term results (6 and 12 months follow- [FVC: FVC values for the same patients
(1996) effort treat- up) are reported here. Results for immediate pre- were reported in Ramig et al (1995).]
ment (RET) post changes are described in Ramig et al
G2: LSVT (1995). *
Acoustic
SPL: The LSVT group maintained their improve-
ment (increase) for sustained phonation at 6 and
12 months after treatment (P < 0.0001). Only sub-
jects in the LSVT group maintained a sig. increase
of SPL during reading at 6 and 12 months follow-
up (P = 0.002; P = 0.009). For both groups, no sig.
increase of SPL during conversation was

21
(Continued)
22
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
observed at follow-up.
STSD: Subjects in the LSVT group improved
(increased) STSD from pre- to 6 months
(P = 0.018) and from pre- to 12 months (P = 0.020)
for the conversation condition. No long-term
improvement was found for the RET group for the
conversation condition. A significant main effect
for time was found in the reading condition
(P < 0.0001) (no further details provided).
F0: A significant main effect for time was found in
the reading condition for men (P < 0.0001) and
women (P = 0.015). A significant main effect for
time was found in the conversation condition for

ARTICLE IN PRESS
men only (P = 0.013) (no further details provided).
33 Ramig et al G1: Respiratory *Only the results for 24 months follow-up are N/A
(2001) effort treat- reported here*
ment (RET) Acoustic
G2: LSVT SPL: Improvements (increases) in SPL between
pre- and 24-month follow-up were significant in
the LSVT group for the sustained vowel condition
(P = 0.000), the reading condition (P = 0.001) and
the conversation monologue condition
(P = 0.009). Changes were NS for the RET group.
STSD: Improvements (increases) in STSD from
pre- and 24-month follow-up were significant in
the LSVT group for the reading condition
(P = 0.000) and the conversational monologue
condition (P = 0.044). Changes were NS in the RET

Journal of Voice, Vol. &&, No. &&, 2019


group.
28 Ray et al Threshold Acoustic Maximum respiratory pressure
(2018) IMST, F0 range: In total, 3/6 subjects improved MIP: In participants who received IMST
Threshold (increased) their pitch range during the treatment first, MIP improved (increased) by 37%,
EMST, and period. For the 3 subjects, the increase occurred 101%, and 118% during the IMST phase.
combined in their lower range and during the EMST phase. In participants who received EMST first,
effects SPL range: The combined effect of IMST and EMST MIP increased by 16%, 33%, and 34%
on intensity range was minimal (mean change during the EMST phase.
from 17.4 dB to 16.7 dB). Combined effects of IMST and EMST: The
participants’ mean MIP value increased
significantly from baseline to the end of
the treatment (P = 0.002; d = 1.30).
MEP: In participants who received IMST
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
first, MEP improved (increased) by 23%,
45%, and 130% during the IMST phase.
In participants who received EMST first,
MEP increased by 70%, 28% and 137%
during the EMST phase.
Combined effects of IMST and EMST: The
participants’ mean MEP increased signif-
icantly from baseline to the end of the
treatment (P = 0.008; d = 1.80).
45 Roy et al G1: Respiratory Self-Assessment Maximum respiratory pressure
(2003) muscle train- VHI: The VA and RT groups experienced a signifi- MEP: MEP results were only reported for
ing (RMT) cant improvement (decrease) of VHI scores from the RMT group. Subjects in this group
(threshold pre- to post-treatment (P = 0.002; P = 0.007 respec- experienced a significant pre- to post-

ARTICLE IN PRESS
EMST) tively). There was no significant improvement in treatment improvement (increase) in
G2: Resonance the RMT group. MEP (P = 0.003).
therapy (RT) Voice severity rating: The subjects’ self-ratings of
G3: Voice severity improved (decreased) significantly from

The Impact of Respiratory Exercises on Voice Outcomes


amplification pre- to post-treatment in the VA group (P = 0.008)
(VA) and the RT group (P = 0.019). No significant
improvement was found in the RMT group.
34 Sapir et al G1: Respiratory Auditory-perceptual judgement N/A
(2002) effort treat- Loudness: In the LSVT group, significantly more
ment (RET) subjects were judged to be louder during reading
G2: LSVT at 12-month follow-up, versus at pre-treatment.
The difference was significant (P < 0.0001). The
difference was not significant for the RET group.
Quality: In the LSVT group, significantly more sub-
jects were judged to have a better quality during
reading at 12-month follow-up, versus at pre-
treatment. The difference was significant
(P < 0.0001). The difference was not significant for
the RET group.
47 Schaeffer and Stimulation Auditory-perceptual judgement Respiratory waveforms
Sunyoung training Quality: All subjects improved their voice quality, The graphs showed a pre- to post-treat-
(2017) as observed by judges (PI and research assis- ment improvement (greater consistency)
tants). in the respiratory waveforms for SPL, F0,
Acoustic Psub and airflow.
SPL: 11/20 subjects improved (increased) their
mean SPL level to within the normal range.
F0: 10/20 subjects improved (increased) their F0
level toward normal values.
Aerodynamic and duration

23
(Continued)
24
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
Psub:17/20 subjects improved their Psub level
toward the normal range.
Airflow: results not reported.
35 Smith et al G1: Respiratory Visual examination N/A
(1995) (R) Glottal configuration: There was an improvement
G2: Voice and (more participants had a normal glottal configu-
respiratory ration) from pre- to post-treatment in the VR
(VR) group at normal pitch and loudness. The effect of
treatment type was significant in both flexible
(P < 0.01) and rigid (P < 0.05) endoscope views.
Results in the loud condition were non-significant
for both groups.
Degree of glottal incompetence: There was a sig-

ARTICLE IN PRESS
nificant difference in the pre-post improvement
(decrease of the magnitude of glottal incompe-
tence) at normal pitch and loudness between the
2 treatment types, in favor of the VR group, for
both the flexible (P < 0.010) and rigid (P < 0.010)
endoscope views. No significant difference was
found in the loud condition.
Laryngeal hyperfunction − false-fold compression:
There was no significant pre- to post-treatment
change in either group.
Laryngeal hyperfunction − anterior-posterior com-
pression: There was no significant pre- to post-
treatment change in either group.
46 Tsai et al G1: EMST Aerodynamic and duration Spirometry
(2016) G2: No MPT: There were no significant change for either FVC: NS for both groups.

Journal of Voice, Vol. &&, No. &&, 2019


intervention group. FEV1: NS for both groups.
s/z ratio: There were no significant change in s/z FEV1/FVC: NS for both groups.
ratio for either group, but the percentage of Maximum respiratory pressure
change (increase) in the durations of the /s/ and /z/ MEP: There was a significant pre- to post-
sounds were significantly greater in the EMST treatment improvement (increase) in
group when compared to the control group MEP in the EMST group (P = 0.001), but
(P = 0.018; P = 0.026, respectively). not for the control group.
Self-assessment
Vocal symptoms questionnaire: The EMST group
showed significant improvements in items of 2
sections of the questionnaire (self-awareness of
voice problems and self-awareness of vocal
health), whereas the control group did not show
any significant improvement.
(Continued)
Maude Desjardins and Heather Shaw Bonilha
TABLE 4(Continued )
Reference Interventions
Number Study Voice Outcomes and Results Respiratory Outcomes and Results
48 Van Lierde et Vocalization Acoustic N/A
al (2010) with abdomi- Lowest and highest intensity: No significant
nal breath change was found after the breath support condi-
support and tion. A significant improvement (lowering) of the
MCT lowest intensity was found following the MCT
condition (P = 0.007).
Lowest and highest frequency: No significant
change was found after the breath support condi-
tion, but a significant improvement (increase) of
the highest frequency was found after the MCT
condition (P = 0.05).
Jitter: No significant change was found after the
breath support condition, but a significant

ARTICLE IN PRESS
improvement (reduction) was found after the
MCT condition (P = 0.05).
Shimmer: No significant change was found after
the breath support condition, but a significant

The Impact of Respiratory Exercises on Voice Outcomes


improvement (reduction) was found after the
MCT condition (P = 0.05).
Aerodynamic and duration
MPT: No significant change was found following
the breath support condition, but there was a sig-
nificant improvement (increase) following MCT
(P = 0.05).
Other
DSI: No significant change was found following the
breath support condition, but a significant
improvement (toward normal) was found follow-
ing the MCT condition (P < 0.001).
CVF0, coefficient of variation of fundamental frequency; dB: decibels; d, standardized mean difference; DSI, dysphonia severity index; EGGW-25, relative width of the electroglottographic waveform at 25%
of its height; ES, effect size; ERV, expiratory reserve volume; f1-f3, first and third formant regions; F0, fundamental frequency; FEV1, forced expiratory volume in one second; FEF, forced expiratory flow;
FRC, functional residual capacity; FVC, forced vital capacity; GNE, glottal-to-noise excitation ratio; h1−h2, first and second harmonics; IC, inspiratory capacity; LSVT, Lee Silverman Voice Treatment; Leq,
equivalent sound level; MCT, manual circumlaryngeal therapy; MEP, maximum expiratory pressure; MFDR, maximum flow declination rate; MVV, maximal voluntary ventilation; MPT, maximum phonation
time; N/A, not assessed; NS, not statistically significant; OQ, open quotient; PEF, peak expiratory flow; PI, principal investigator; Psub, subglottal pressure; Raw, resistance of airway; RV, residual volume;
SPL, sound pressure level; STSD, frequency variability in semitones; TLC, total lung capacity; VC, vital capacity; V-RQOL, Voice-Related Quality of Life; Vtg, volume thoracic gas; VHI, Voice Handicap Index.

25
ARTICLE IN PRESS
26 Journal of Voice, Vol. &&, No. &&, 2019

measures are compared across studies. Main results for and singer, meaning that the breathing directive (abdomen-
immediate treatment effects are discussed below. in or abdomen-out) was found to impact the perceived
breath management only in some singers. In Mueller et al's
study,43 participants with tetraplegia were asked to evaluate
Results for respiratory outcomes
the impact of the respiratory exercises on various respira-
Maximum respiratory pressure
tory parameters, such as the ability to blow one's nose or
MEP was reported only for respiratory muscle strength
breathlessness during exercise. No difference was found
training studies. An improvement of MEP was found in all
between the experimental groups (IMST and isocapnic
EMST studies where MEP was assessed.28,36−39,45,46 In the
hyperpnea) and the placebo group (incentive spirometry).
study by Johansson et al39, significance was not assessed but
In Schaeffer and Sunyoung's study47 on participants with
all five subjects with multiple sclerosis improved their MEP
dysphonia of various etiologies, respiratory waveforms
following EMST training, with effect sizes ranging from d =
graphs were reported and were described as improved fol-
0.4 to d = 2.1. In Ray et al’s study,28 both IMST and EMST
lowing a single session of stimulation training focused on
were found to have an effect on the signing students’ MEP,
coordinating respiration with phonation and developing an
with increases ranging from 28% to 137% following EMST
abdominal breathing pattern. No further details were pro-
and from 23% to 130% following IMST. In the same study,
vided regarding this outcome.
IMST and EMST also induced changes in MIP, increasing
from 16% to 34% following EMST and from 37% to 118%
following IMST. One study tested the effect of IMST and Results for voice outcomes
isocapnic hyperpnea on MEP and found no significant dif- EMST studies
ference in mean change when compared to the placebo Four of the five EMST studies that reported acoustic meas-
group (incentive spirometry).43 On the other hand, that ures found some positive effect of EMST on acoustic out-
same study found a significant pre-post improvement of comes. However, these four studies are single-subject
MIP in the IMST group, and the mean change was signifi- designs that showed improvement in only a subset of the
cantly greater than those recorded in the isocapnic hyper- participants. Specifically, sound pressure level (SPL) and/or
pnea and incentive spirometry groups. frequency variability in semitones (STSD) were improved in
some participants with Parkinson disease (2/9 participants
improved) and multiple sclerosis (4/5 and 3/5 participants
Spirometry:
improved), and in hypotonic children.36,37,39 On the other
Of the five studies that assessed measures of vital capacity,
hand, EMST was shown to have a minimal effect on SPL
only one found a significant improvement in FVC, follow-
range in classical singing students in Ray et al’s study.28 In
ing incentive spirometry in children with spastic cerebral
that same study, three out of six participants extended their
palsy.40 That same study also found a significant improve-
lower range during the EMST phase of the experiment. Sev-
ment in forced expiratory volume in one second (FEV1)
eral other acoustic measures were assessed in another
and in peak expiratory flow (PEF), but not in the FEV1/
EMST study, including jitter, shimmer, noise, glottal-to-
FVC ratio. FEV1 was measured in three other studies, but
noise excitation ratio, and fundamental frequency (F0), but
did not improve significantly in any of them.37,43,46
no change was found in those outcomes in professional
voice users.44 Four of the five studies that reported aerody-
Kinematics namic and duration measures found some improvement in
Breathing directives yielded significant effects on singers’ subglottal pressure, MPT, and/or utterance length in various
abdominal and ribcage excursions and dimensions at initia- subject populations (healthy controls, individuals with PD
tion of phonation, but not on lung volume.26 On the other and with multiple sclerosis, and hypotonic children).36−39
hand, lung volume at initiation of speech changed signifi- The improvement in individuals with PD and with multiple
cantly (either increased or decreased) in most participants sclerosis was limited to subsets of participants: three out
with PD (seven out of eight) after EMST in Darling-White of nine participants with PD improved utterance length with
and Huber's experiment.36 In the same study, lung volume an effect size superior to d = 1.00,36 and three out of five
at termination of speech, as well as lung volume excursion, participants with multiple sclerosis improved MPT, with
were significantly modified in half of the participants. effect sizes ranging from d = 0.2 to d = 3.6.39 On the other
Lastly, Mueller et al found no significant difference in tho- hand, Chiara et al38 found no increase in MPT in subjects
rax mobility between the experimental groups (IMST and with multiple sclerosis after EMST. Other outcomes such as
isocapnic hyperpnea) and the placebo group (incentive spi- s/z ratio and number of syllables per breath did not show any
rometry) in subjects with tetraplegia.43 improvement in professional voice users and in hypotonic
children following EMST.37,46 One out of two studies found
a change in Voice Handicap Index score after the interven-
Other parameters
tion, in professional voice users.44 Other patient perception
In Collyer et al's study,27 listeners were asked to judge voice
and quality of life scales did not reveal any change in individ-
samples with regards to perceived breath management. An
uals with multiple sclerosis and in professional voice users,
interaction effect was found between breathing condition
ARTICLE IN PRESS
Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 27

with the exception of some items in a vocal symptoms ques- assessed.47 In that same study, perceptual judgements of
tionnaire in Tsai et al’s study.38,45,46 voice quality by nonblinded judges revealed an improve-
ment in all subjects from pre- to post-therapy. Participants
in this study had dysphonia of various etiologies. They did
IMST, isocapnic hyperpnea, and incentive spirometry not undergo visual examination of the larynx and therefore
One study compared the outcomes of IMST, isocapnic no further information was provided on their conditions.
hyperpnea and incentive spirometry on participants with
complete tetraplegia, using incentive spirometry as a pla-
cebo intervention. The results showed no significant differ- Other respiratory exercises:
ence in mean change between the three groups for the two Two studies examined the effect of the respiration component
00
voice outcomes measured: MPT and SPL.43 Although an easy breathing00 within a voice therapy protocol including
increase in MPT was noted in the three groups, the signifi- five phases: vocal hygiene, direct facilitation, respiration,
cance of those improvements was not assessed in the study. relaxation, and carryover.41,42 Three therapy sessions were
As for SPL, an increase was found in the incentive spirome- allocated for each phase of the protocol, and the order of the
try and isocapnic hyperpnea groups, but a decrease was phases varied to counterbalance order effects (except for vocal
found in the IMST group. The significance of these pre-post hygiene and carryover which were always first and last,
changes was not assessed. Another study, testing incentive respectively). The results of this program are reported sepa-
spirometry with gradually increasing flow rate in children rately because no focus was directed toward promoting a cer-
with spastic cerebral palsy, found a significant improvement tain type of breathing pattern or respiratory strengthening.
in MPT after the intervention period.40 In Ray et al’s study Exercises aimed at developing a relaxed and effort-free
on singing students, two out of three participants increased breathing and coordinating respiration with phonation
their SPL range during the IMST part of the intervention, through a hierarchy of tasks. Several acoustic and aerody-
but none increased their F0 range. namic outcomes were assessed, but they all failed to show a
significant improvement after the respiration component of
the voice therapy program.41 Of the 10 auditory-perceptual
Respiratory effort treatment parameters that were assessed, only press/hyperfunction and
Seven articles described the outcomes of RET on partici- vocal fry were statistically significantly reduced.42
pants with Parkinson disease. SPL, F0, and STSD all
improved significantly in the reading condition for at least
one gender group.31 SPL was also increased in conversation, Duration of treatment effects
while improvements in F0 and in STSD were not general- Five papers addressed long-term effects of treat-
ized to the conversation condition.31 The respiratory inter- ment.30,33,34,37,38 While the Lee Silverman Voice Treatment
vention yielded changes in MPT and in utterance and pause (LSVT) induced long-term changes in SPL and in auditory-
duration during reading, but not in subglottal pressure and perceptual ratings of loudness and quality in participants
maximum flow declination rate.31,32 Only loudness was with PD, no long-term improvements were found in the
judged by external listeners to be improved following treat- RET group.30,33,34 STSD was also found to be increased at
ment, but participants also reported improvements in 24 months follow-up in the LSVT group, but not in the
hoarseness and monotonicity.31 None of the glottographic RET group.33 On the other hand, Cerny et al37 found a last-
or videostroboscopic outcomes were improved following ing effect of threshold EMST on SPL in a group of hypo-
RET.32,35 tonic children. However, the follow-up period was only 3
weeks. Chiara et al38 also found long-term (4 weeks)
improvements following threshold EMST, on three out-
Focus on abdominal breathing pattern come measures: MPT, words per minute, and MEP. Inter-
There were three interventions (described in four articles) estingly, MPT was found to be improved at follow-up
that focused on the control of the abdominal muscles during despite no significant change immediately after the interven-
phonation (vocalization with abdominal breath support, tion period in individuals with multiple sclerosis.
stimulation training, and abdominal directives). Interest-
ingly, those three interventions took place during a single
treatment session. For two of the interventions, intensity DISCUSSION
and frequency range, jitter, shimmer, dysphonia severity The goal of this review was to appraise the state of the evi-
index, and MPT remained the same after the session, in pro- dence regarding the effectiveness of respiratory interven-
fessional classical singers and in participants with tions to improve voice outcomes. More specifically, the
MTD.26,48 In another study, after one session of stimulation review's aims were to (1) describe the respiratory exercises
training focusing on coordinating respiration with phona- that have been studied in relation to voice; (2) assess their
tion and acquiring an abdominal breathing pattern, most impact on respiratory outcomes; (3) assess their impact on
participants improved their subglottal pressure (17 out of voice outcomes; (4) provide insights for clinical practice;
20) and many improved F0 (10 out of 20) and SPL (11 out and (5) assess the limitations and gaps in the literature to
of 20). However, the significance of these results was not suggest direction for future research.
ARTICLE IN PRESS
28 Journal of Voice, Vol. &&, No. &&, 2019

Effect on respiratory outcomes equation for MEP.59 Although young and otherwise
Respiratory outcomes of 13 articles were discussed in this healthy despite their voice disorders, participants had a
review. EMST, IMST, incentive spirometry, abdominal mean MEP below the LLN at baseline and a mean MEP
directives, and stimulation training focusing on abdominal within normal limits after the EMST intervention. The pos-
support all had a positive effect on at least one respiratory sibility that a compromised respiratory muscle strength may
outcome. RET did not result in a significant improvement have contributed to the development or maintenance of a
on the assessed respiratory measure. No respiratory out- voice disorder in this population sample was not discussed
comes were reported in the studies on vocalization with in the study but is worth considering. Also of note, is that
abdominal support and “easy breathing.” the low baseline MEPs could have been a factor favoring
the positive effect of the EMST intervention on respiratory
outcomes. This could also have been the case in Ray et al’s
EMST improves MEP study, in which most participants (students in a Vocal Music
EMST interventions improved MEP in all seven studies in graduate program) surprisingly had a baseline MEP close to
which it was assessed.28,36−39,45,46 These results are consis- the LLN for their age and sex, based on Evans’ reference
tent with the broad literature on EMST. This type of respi- equations.59 It is also possible that the baseline measures,
ratory training has generated a lot of interest in various although taken multiple times, did not reflect the true maxi-
areas of research and clinical care, including geriatrics, dys- mal strength of the participants. Further analysis of the
phagia, chronic obstructive pulmonary disease (COPD), influence of baseline MEP on treatment outcomes is
PD, multiple sclerosis, and amyotrophic lateral sclerosis needed.
(for a summary of the effects of EMST on various popula-
tions and outcomes, refer to Laciuga et al50). The literature
EMST can improve MIP through cross-training effects
at large confirms the positive effect of EMST on MEP on
Only one of the included studies measured the effect of
these various patient populations with compromised respi-
EMST on MIP, possibly because an improvement in inspi-
ratory muscle strength.51−58
ratory muscle strength is not necessarily expected when
In four out of the seven reviewed EMST studies, partici-
training the expiratory muscles. Nonetheless, the cross-over
pants also had a condition that may have impacted their
study, by Ray et al, did find an increase in MIP following
baseline MEP measures: hypotonic characteristics,37 multi-
an EMST phase.28 In the respiratory muscle strength train-
ple sclerosis,38,39 and PD.36 In Cerny et al's study on hypo-
ing literature, studies that measured the impact of EMST
tonic children, the participants’ baseline MEPs were
on MIP have yielded inconsistent results. Experiments on
confirmed to be below normal values. In Chiara et al's
participants with COPD and multiple sclerosis showed that
study, participants with multiple sclerosis who presented
although EMST significantly improved MEP, it did not
with a moderate disability level on the Expanded Disability
have a significant effect on MIP.58,60,61 However, another
Status Scale were found to have a greater MEP increase
study involving patients with severe multiple sclerosis found
than those with a mild disability level, possibly indicating
possible cross-training effects leading to significant increases
an effect of baseline status on treatment outcomes. A similar
in MIP following EMST, while no improvements were
pattern was found in Johansson et al's study, also on indi-
found in MEP.62 The authors characterized this finding as
viduals with multiple sclerosis: after 6 weeks of EMST, par-
surprising and suggested that the very low expiratory mus-
ticipants with lower baseline MEPs (below the lower limit
cle strength at baseline (18% of predicted value) may have
of normal (LLN) based on Evans’ reference equations59)
forced the participants to use a greater lung volume to
improved with larger effect sizes (ranging from d = 0.5 to
increase recoil pressure, thereby inducing a possible training
2.1) when compared to participants with a less severe condi-
effect in the inspiratory muscles.62
tion and higher baseline MEPs (effect sizes ranging from
d = 0.4 to 0.5). In Darling-White and Huber's study, base-
line MEPs were not reported, but participants were all diag- EMST may have limited effect on spirometry
nosed with PD and were therefore susceptible for decreased outcomes
respiratory muscle strength. The only two EMST studies in which spirometry outcomes
Three EMST studies found significant improvements of were measured did not find any improvement in FVC,
MEP in healthy participants with voice complaints, more FEV1 or FEV1/FVC.37,46 These results reflect the larger
specifically in professional voice users (teachers, medical EMST literature in which spirometry outcomes are infre-
professionals who use their voice for at least 4 hours a day quently considered and maximum respiratory pressure out-
while working, and classical music students).28,45,46 In Roy's comes are mainly used to measure treatment effect. When
study on teachers, baseline MEP values were not provided spirometry outcomes are assessed, they often yield conflict-
so it remains unknown whether or not participants had ing results. For example, a study by Mehani60 conducted on
lower than expected respiratory muscle strength prior to patients with moderate COPD revealed significant changes
treatment. In Tsai's study, most participants were females in pulmonary function (FEV1, FVC, FEV1/FVC) after two
between 25 and 35 years old; therefore we calculated LLN months of training. These results were not confirmed by
for a female of 30 years old, following Evans’ reference Weiner et al and Mota et al’s studies,57,63 in which EMST
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Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 29

performed by participants with severe COPD failed to meta-analyses confirm the efficacy of IMST for improving
improve spirometry outcomes including FVC and FEV1, MIP in patients with COPD and asthma.68−70 An increased
after 3 months or 5 weeks of training. Of note, participants MIP following IMST was also found in other patient popu-
in those two studies had severe airflow obstruction (FEV1 lations including (but not limited to) critically ill patients,71
below 50% of predicted value), while severely affected children with cerebral palsy,72 sedentary hemodialysis
patients were excluded from Mehani's study. Therefore, it patients,73 and individuals with upper airway diseases such
may be that severely impaired pulmonary function can limit as congenital juvenile laryngeal papilloma (scarring and
improvements from EMST, just as much as an intact pul- laryngeal web from surgical excisions),74 exercise-induced
monary function may prevent improvement due to a ceiling vocal fold dysfunction,75 and congenital and acquired bilat-
effect.51 The authors also explain that flow does not inten- eral abductor vocal fold paralysis.76,77 Contrarily to other
sify with increased driving pressure above a certain trans- patient populations, those with upper airway obstruction
pulmonary pressure, which could explain why spirometry are usually healthy despite their breathing condition.
outcomes do not necessarily improve despite changes in Although their inspiratory muscle strength is likely to be
respiratory muscle strength (64; cited in51). within normal limits at baseline, these patients need above
average inspiratory strength in order to increase the size of
their laryngeal inlet, which is made possible by the relation-
EMST improves kinematic measures in one study
ship between the diaphragm and the posterior cricoaryte-
One study, by Darling-White and Huber,36 investigated the
noid muscle.78,79 This could explain why functional results
impact of EMST on kinematics, more precisely on lung
(for example, a reduced sensation of dyspnea) were found in
volume at initiation and termination of speech, and lung
these populations following IMST and an increase in
volume excursion. The authors found significant changes in
MIP.75,80 This supports the concept that individuals with a
lung volumes following 4 weeks of EMST training in partic-
baseline MIP within normal limits can further increase MIP
ipants with PD. All but one of the participants had a signifi-
following respiratory training, potentially leading to func-
cant change in lung volume at initiation: after treatment,
tional improvements depending on the nature of their voice
some individuals initiated phonation at a higher lung vol-
problem.
ume, while some initiated phonation at a lower lung vol-
ume. The authors explain that the EMST intervention
normalized the breathing pattern of individuals towards IMST can improve MEP through cross-training effects
what would be expected from normal aging adults.36 It is To the same extent that the effect of EMST on MIP is
worth noting that, in this study, participants with no uncertain, there is ambiguity surrounding the effect of
improvement in MEP were excluded from the kinematic IMST on MEP because of conflicting results in the litera-
analyses. Since changes in lung volumes at initiation can ture. While some authors have found no difference in MEP
impact the expiratory pressure, it is possible that by exclud- between the IMST and control groups after an interven-
ing subjects with no improvement in MEP, the investigators tion,72 other investigators did find an improved MEP fol-
may also have excluded participants without a change in lowing IMST.28,81 One of these studies, by Ray et al,28 was
kinematics. included in the present review and showed that singers
undergoing a phase of IMST could increase their MEP up
to 130%. Moreover, in Vorona et al’s review and meta-anal-
IMST improves MIP
ysis, four randomized trials showed improvements in MEP
Only two of the reviewed studies evaluated MIP outcomes.
following an IMST intervention in critically ill adults, with
One of them, by Mueller et al,43 compared two experimen-
a mean increase of 9 cmH2O.71 Thus, there is some evidence
tal interventions (IMST and isocapnic hyperpnea) with a
for cross training for both IMST improving MEP and for
placebo group (incentive spirometry). The IMST group had
EMST improving MIP.
the largest change in MIP when compared to the isocapnic
hyperpnea and incentive spirometry groups. This result is
not surprising since the main physiological target of IMST Incentive spirometry improves pulmonary function in
is to increase inspiratory muscle strength, while isocapnic one study
hyperpnea is known to improve respiratory muscle endur- Of the 23 reviewed studies, only one found significant pre-
ance and measures of exercise performance but not inspira- post improvements in spirometry outcomes (FVC, FEV1,
tory or expiratory pressures.65−67 The other study, by Ray and PEF), and this was in Choi et al's study on incentive spi-
et al.,28 measured changes in MIP following either IMST or rometry exercises for children with spastic cerebral palsy.40
EMST in a cross-over design. The results revealed improve- Interestingly, in Mueller et al's study,43 incentive spirometry
ments in MIP after both interventions, although the changes was used as the control condition against which IMST and
were more substantial following IMST. isocapnic hyperpnea outcomes were compared. While the arti-
Inspiratory muscle training with a pressure threshold or cle states that no significant difference in pulmonary function
resistive device has been studied in various patient popula- was found between the three groups of participants with tetra-
tions, including patients with airway obstruction disorders plegia, it is unknown whether or not the interventions yielded
such as COPD68,69 and asthma.70 Literature reviews and significant pre- to post-treatment improvements within the
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30 Journal of Voice, Vol. &&, No. &&, 2019

groups, because significance of the changes was not assessed. assessed following vocalization with abdominal breath sup-
The question is even more relevant considering that some port48 and “easy breathing.”41,42
studies in the respiratory literature found significant improve- In the literature, respiratory interventions that do not use
ments in measures of pulmonary function after incentive spi- a device are often gathered under the umbrella of “breath-
rometry whereas others did not.82−84 This is also the case ing exercises” or are studied as part of a broader interven-
regarding IMST, for which various studies have reported tion program. This makes it challenging to identify the
improvements in spirometry outcomes although others did specific effects of different exercises on respiratory outcomes
not.60,73,85−87 The heterogeneity of the patient populations and to compare treatment outcomes across studies. For
and baseline deficits, combined with differences in training example, a Cochrane review conducted in 2016 on breath-
protocols, are key factors that could explain why spirometry ing exercises in children with asthma could not draw any
outcomes are inconsistent across experiments. reliable conclusion on their effectiveness because no study
isolated the breathing intervention as an independent vari-
able.89 The exercises, which consisted of lateral costal
Incentive spirometry and isocapnic hyperpnea show
breathing, diaphragmatic breathing, inspiratory patterns,
some impact on kinematic measures
and pursed lips breathing, were all part of a more complex
In Mueller et al's study,43 although no significant difference
program including other components such as relaxation
was found in thorax mobility between the three intervention
exercises and rhythmic mobilization exercises.89 Another
groups, high effect sizes were found for incentive spirometry
review included 13 studies on breathing exercises for adults
and isocapnic hyperpnea when compared to the IMST group.
with asthma, and in seven of them the intervention consisted
The authors explain this result by the high breathing volumes
of yoga training with a main focus on breathing exercises
induced by the two former methods, which are likely to
(pranayama).90 Other interventions consisted of deep dia-
involve respiratory accessory muscles in the neck. By promot-
phragmatic breathing, nasal breathing techniques, breath-
ing ribcage elevation, these muscles are also likely to increase
ing retraining, and the Buteyko method involving periods
thorax mobility and intrathoracic areas at certain levels of the
of breath holding and of shallow breathing.90,91 This review
spine.43 However, the involvement of respiratory accessory
revealed conflicting results regarding spirometry outcomes
muscles was also reported during IMST. In fact, Ramsook et
(PEF, FVC, FEV1, FEV1/FVC, and FEF25−75%): five stud-
al found that the sternocleidomastoid and scalene muscles
ies found no significant effect of breathing exercises when
were engaged during IMST in healthy men.88 Just like the dia-
compared to inactive control or asthma education, while six
phragm, these muscles were recruited at 50−60% of their
studies found an effect in favor of breathing exercises.90
maximal electromyogram activity during the respiratory
Despite these results, the eight studies that measured quality
training.88 These results suggest that, for some populations,
of life reported benefits in the breathing exercises group.90
IMST has the potential to impact respiratory kinematics in
A Cochrane review assessed the evidence supporting breath-
addition to increasing respiratory muscle strength.
ing exercises for patients with COPD.92 The following
breathing techniques were assessed in 16 included trials:
The impact of respiratory exercises without device pursed lips breathing, diaphragmatic breathing, yoga
remains unclear breathing (timed breathing and emphasis on the exhalation
FVC was the only respiratory outcome assessed in the stud- phase), respiratory biofeedback, breathing exercises per-
ies on RET for participants with PD, and no significant formed during physical exercises, deep breathing exercises,
improvement was found.30−32 This respiratory treatment and balloon inflation. Once again, breathing exercises were
was specifically designed as a control condition against sometimes combined with other intervention components,
which LSVT could be compared and thus the treatment out- but studies were included only if at least 50% of the inter-
comes cannot be supported or disproved by other studies in vention consisted of breath work. Four studies reported
the broad literature. Although some of its components improvements in exercise tolerance, which were not neces-
(such as maximum inhalation and exhalation, sustained /s/ sarily translated into improved quality of life or dyspnea
and /f/, and attention to abdomen and ribcage excursions) rating. Secondary outcomes including physiological meas-
are commonly used by SLPs who work with voice patients, ures (eg, gas exchange, ventilation, and breathing patterns)
their effect on respiratory outcomes remains uncertain. This were infrequently used and heterogeneous, making it chal-
is also true for exercises focusing on developing an abdomi- lenging to draw conclusions.92
nal breathing pattern or coordinating phonation with respi- Some studies did examine the effects of specific respira-
ration, for which the reviewed articles provided little tory exercises on respiratory outcomes. For example, Woo
information to clarify their effect on respiratory function. et al found that deep breathing exercises focusing either on
Abdominal directives were found to improve perceived inspiration or on expiration and conducted five times
breath management as judged by external listeners and to weekly for 1 month improved spirometry outcomes (FVC,
have an impact on abdominal and ribcage dimensions, in FEV1, and PEF) and chest expansion in healthy males.93
some singers.26,27 Stimulation training was found to Song and Park's study94 on stroke patients examined the
improve regularity of breathing as shown by respiratory effect of chest expansion resistance exercises, in which the
waveforms graphs.47 No respiratory outcomes were therapist applies hand pressure on the patient's ribcage and
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Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 31

diaphragm during respiration, and chest expansion exer- order to meet their above average vocal demands. Second,
cises, in which the therapist passively moves the patient's even if maximum respiratory pressure is brought up to an
shoulders, pelvic area, and trunk during respiration to opti- optimal value, generalization to voice tasks is likely to be
mize expansion of the ribcage. After 8 weeks of therapy five needed for functional improvements to occur. In fact,
times a week, participants in both intervention groups had EMST, and other respiratory exercises, do not meet the
improved their FVC and FEV1, while their FEV1/FVC specificity criteria of motor learning theory. In order for the
ratios remained unchanged. As another example, a study benefits to be maximized, the exercise has to induce a func-
by Kim and Lee95 measured the effect of deep abdominal tional reorganization in the cortex (increased neuronal
muscle strengthening exercises on healthy subjects. While excitability and synaptic response), a phenomenon that has
lying on the floor with their knees bent and feet on the been associated with specific skilled tasks.96 Although respi-
floor, participants were instructed to inhale deeply and ratory strength training such as EMST does not involve
hold their breath for 10 seconds at the end of the inhala- phonation, Sapienza has argued that since it requires the
tion. The exercise was repeated for five sets of 10 breaths, integration and coordination of many muscle groups, it is
three times a week for 4 weeks, after which significant thought to be complex and specific enough to lead to neuro-
improvements in FVC, FEV1, and transverse abdominal plasticity and threshold changes affecting respiratory func-
muscle contractility were observed. These examples dem- tion.96 Nonetheless, the carryover of the effects of
onstrate that the respiratory and physical therapy litera- respiratory training to specific voicing tasks, as well as voice
tures can be of great relevance to the voice field. They exercises directly targeting vocal function, remain a crucial
provide valuable information on exercises and their impact aspect of the therapy to reach the best possible voice and
on respiratory outcomes. Exercises that are found to be functional outcomes. In addition, it is possible that for
efficacious for improving respiratory function may prove some patients, depending on the voice disorder, a change in
helpful in improving voice outcomes in specific patient respiratory outcomes may not be relevant for improving
populations and for this reason may be worth studying on voice outcomes. This highlights the importance of studying
voice patients. However, an improved respiratory function the effects of respiratory exercises in different populations
does not necessarily translate into better voice outcomes, of voice patients.
as discussed in the following section.

The pertinence of increasing MIP to improve voice


Effect on voice outcomes
outcomes remains theoretical
Once the effect of respiratory exercises on respiratory out-
The same principles apply to the relationship between MIP
comes has been considered, two questions arise: (1) Do
and voice outcomes. In the present review, only two studies
changes in respiratory outcomes translate into improved
measured MIP, which was found to be improved following
voice outcomes? (2) Can voice outcomes improve following
IMST. One of the studies, by Mueller et al.,43 found no sig-
respiratory exercises even when there is no change in respi-
nificant difference in mean SPL and MPT change between
ratory measures (and if so, via what mechanism)? The fol-
IMST and the other intervention groups (isocapnic hyper-
lowing section addresses these questions.
pnea and incentive spirometry).43 However, the article does
not mention if significant improvements were found within
Changes in MEP translate into voice improvements in each group following treatment and consequently the extent
some patients to which these three respiratory interventions can impact
EMST interventions, which improved the participants’ voice remains uncertain. The other study, a single-subject
MEP in all studies in which it was assessed, also yielded design by Ray et al,28 found no difference in F0 range fol-
improvements in some voice outcomes. SPL, STSD, F0, lowing IMST, and found only a minimal change in SPL, in
Psub, MPT, and utterance length were found to be some participants. These results provide limited information
improved in at least some participants, but several other on the impact of improving MIP on voice outcomes. Per-
acoustic, aerodynamic, and duration measures were left taining to voice, IMST has been investigated significantly
unchanged. Furthermore, changes did not always translate less than EMST. Studies on IMST have focused on improv-
into functional improvements, as indicated by various self- ing ventilatory functions to reduce the sensation of dyspnea
assessment measures. A variety of reasons could explain in patients with upper airway obstruction disorders.97 Even
these results. First, the person's vocal demands have to be so, improving MIP through IMST could be relevant to
taken into account. If one's MEP is already sufficient to voice production because intensifying the passive recoil
meet their vocal demands, respiratory exercises may gener- pressures by increasing the inspiratory lung volume is one
ate only limited changes in voice outcomes, despite an of the main strategies for augmenting loudness of the voice.
increase in MEP. On the other hand, in some participants In addition, activation of strong inspiratory muscles during
who display normal maximum respiratory pressure values, the expiration phase of phonation results in a better control
there could be a gap between actual MEP and optimal of the airflow, which should allow for longer and louder
MEP for the participants’ vocal demands. For example, speech without activating expiratory muscles and using the
professional voice users could necessitate a higher MEP in expiratory reserve volume. Some voice patients need even
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32 Journal of Voice, Vol. &&, No. &&, 2019

more strengthening of their inspiratory muscles to compen- to when healthy speakers are talking below their resting
sate for an impaired laryngeal valving caused by glottic expiratory volume. With time, this increased effort induces
insufficiency. These positive effects of an increase in MIP tension in the larynx, as revealed by the observed medializa-
remain theoretical and cannot be confirmed with tion of the ventricular folds on videostroboscopy in about
the few studies that assessed the impact of IMST on voice half of the subjects with COPD.98 Moreover, a lack of pul-
outcomes in this review.43 Thus, more research is needed to monary drive hinders the attainment of a regular mucosal
better understand the relationship between MIP and voice wave, hence the visual-perceptual judgement of irregularity
outcomes. present in more than 50% of the subjects despite an absence
of organic lesions. The correlations between voice parame-
ters and pulmonary function in patients with COPD was
Improving spirometry outcomes may impact voice in also confirmed in another study, which found significant
specific patient populations negative correlations between jitter, shimmer, grade of dys-
While changes in respiratory muscle pressure seem to corre- phonia, and FVC, FEV1, and MMEF percentages of pre-
late, to a certain extent, with changes in voice outcomes, the dicted values.99 Moreover, a significant positive correlation
same cannot be stated regarding spirometry measures. was found between F0 and the same spirometry parameters.99
Despite a lack of improvement in FVC, FEV1, and FEV1/ Patients with COPD represent a specific population because
FVC, studies reported that EMST and RET were associated of their airflow limitations; in patients with normal baseline
with at least some changes in voice measures. It is possible spirometry outcomes, a change in measures such as FVC may
that a different variable, such as an increase in other respira- not be necessary to improve voice outcomes. In fact, normal
tory measures, for example MEP or MIP, may have con- speakers don't use their full vital capacity when speaking,
tributed to these improvements even in the absence of a even when initiating speech at high lung volumes.100 Further
change in pulmonary function. Nonetheless, an increase in research is needed to understand the relevance of improving
MEP or MIP is likely to be associated with an increase in spirometry outcomes in specific voice patient populations.
spirometry values considering the relationship between
maximum respiratory pressures and pulmonary function. In
fact, measures of vital capacity, such as FVC, do not only Changes in respiratory kinematics can impact voice
reflect the integrity of the lungs but are also influenced by positively or negatively
the strength of the respiratory muscles. Weak inspiratory Only three studies in the present review assessed the effects
muscles can impede the ability of the lungs to expand to full of respiratory exercises on kinematic measures. In Collyer
capacity, whereas weak expiratory muscles can impede lung et al’s experiment,26,27 changes were observed in abdominal
compression to a normal residual volume.59 It is possible and ribcage dimensions, but not in lung volumes, after the
that spirometry outcomes are more difficult to change and participants received abdominal directives (abdomen-in or
that an improvement in maximum respiratory pressure, abdomen-out while singing). The directives did not affect
while sufficient to impact phonation, may not be enough to the participants’ SPL, but did impact, for some of them,
change spirometry measures. how the singing was perceived by external judges.26,27 In
Only one study showed a possible link between improve- Darling-White and Huber's study,36 EMST induced
ments in FVC, FEV1, and PEF and improvements in MPT, changes in lung volumes for most of the participants, but
following incentive spirometry exercises. No correlation changes in voice outcomes (utterance length and vocal
tests were conducted by the investigators to confirm whether intensity) were reported only for a few participants.
or not the change in MPT could be attributed to improved Based on these studies’ results, a change in respiratory
pulmonary parameters, but a recent study did confirm a cor- kinematics seems to have an effect on voice in some individ-
relation between low pulmonary function and the preva- uals, although this effect was not necessarily positive. In
lence of dysphonia in a sample of patients with COPD.98 Collyer et al's experiment, in which the respiratory behavior
The study showed that FVC, FEV1, PEF, and maximum was explicitly manipulated in singers, the authors noted a
mid expiratory flow (MMEF) percentages of predicted val- strong effect of habitual behavior on the outcomes. They
ues were significantly lower in the group with dysphonia noticed that, while singers were able to modify the position
than in the group without dysphonia, as determined by of their abdomen in concordance with the task (abdomen-in
auditory-perceptual judgements of voice quality. The study or abdomen-out), they compensated with their ribcage to
also revealed that MPT, SPL, and phonatory efficiency maintain their habitual lung volumes.26 Furthermore, when
were positively correlated with at least one of the following the directive deviated from the singer's habitual behavior,
parameters: FEV1, FVC, and/or MMEF percentages of the quality of the singing was more negatively perceived by
predicted values. Moreover, correlation tests showed that experienced listeners.27 Similar observations were found by
jitter, pitch perturbation quotient, and phonatory resistance Thomasson, who noted that singers had difficulty compen-
were negatively correlated with those same pulmonary func- sating for a high lung volume when using a nonhabitual
tion parameters. The authors explained that, because of inhalatory behavior.101 This resulted in higher subglottal
their reduced vital capacity, patients with COPD tend to pressures at high lung volumes, an effect that was not found
compensate by increasing their expiratory effort, similarly in the habitual breathing conditions in which singers used
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Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 33

muscular action to counterbalance elastic recoil forces.101 In in both self-assessment measures used, while no improve-
Darling-White and Huber's study on participants with PD, ment was found in the EMST group.45 Pereira et al’s study
the EMST intervention seemed to have normalized the constitutes an exception: no significant difference was found
respiratory pattern instead of disrupting it. In this case, the in voice change between the vocal warm-up group and the
lack of improvement in voice outcomes despite a normal- EMST (with a mucus clearance device) group.44 Nonethe-
ized respiratory behavior was thought by the authors to be less, significantly more teachers in the vocal warm-up group
caused by the absence of generalization exercises. In fact, reported a voice improvement and a greater ease of speech
participants with PD, who already have an impaired self- in the post-treatment questionnaire.
monitoring function, may have had difficulty transferring The included studies compared a respiratory intervention
the new respiratory pattern to speech without explicit to either: voice therapy, no intervention, or an alternative
instructions.36 respiratory intervention. Interestingly, no study compared
the effect of voice therapy only versus voice therapy com-
bined with a respiratory intervention. There is a need to
Clinical practice understand if the synergetic effect of combining both treat-
Exercises that aim to improve respiratory support are fre- ment modalities would lead to improved voice outcomes, or
quently used by SLPs during voice therapy. The most com- if the time spent with a voice therapist should be entirely
mon techniques, and those described in voice therapy allocated to direct work on vocal function. Some interven-
textbooks, include: diaphragmatic breathing, increasing tions programs, such as LSVT, vocal function exercises,
extent of thoracic expansion, increasing period of rib eleva- and flow phonation, include aspects of coordination
tion, and increasing period of expiratory airflow on pho- between phonation and respiration, and this may be suffi-
nemes /s, z, a, ñ, i/. Emphasis is placed on feeling the cient for some patients depending on their deficits. How-
abdomen and ribcage expand and retract with the hands ever, if the patient has significant respiratory impairments,
and on maintaining a straight posture.102 A survey con- or if their vocal demands are too high for what their respira-
ducted by Burg et al with responses from 434 voice thera- tory system can provide, specific work on respiration may
pists in three different countries confirmed that work on be relevant if vocal function is also addressed. Importantly,
respiration is among the three most commonly used strate- the type of respiratory exercise chosen needs to be tailored
gies when treating voice patients.103 In fact, 87.1% of the to the patient's respiratory and voice deficits in order to
respondents affirmed using relaxation of the diaphragm as induce the desired effects. Table 5 summarizes the condi-
well as coordination of articulation, phonation, and breath- tions in which respiratory exercises may or may not be
ing to improve voice.103 The concern with these exercises is appropriate for improving voice outcomes, based on the evi-
that evidence supporting their positive effect on both respi- dence that was provided in this review.
ratory and voice outcomes remains limited, as shown in this
review. Depending on the etiology of the voice disorder,
simply modifying the breathing pattern by encouraging LIMITATIONS
abdominal breathing may not result in functional improve- Limitations of the reviewed studies
ments for the patient. Reporting
Some of the articles included in the present literature In general, the reported data were of good quality. Authors
review indicated that respiratory exercises alone are less clearly reported and described the objectives of the studies,
effective than interventions involving direct work on vocal the main outcome measures, the characteristics of the par-
function. For example, in the studies comparing RET to ticipants, the interventions, and the results. However, only
LSVT, improvements were significantly greater and main- 15 studies out of 23 reported respiratory outcomes in addi-
tained over longer periods of time in the latter group than in tion to voice outcomes. If respiratory outcomes are not
the former. The authors specified that, for patients with PD, reported, the mechanism of action through which voice
who present with glottal insufficiency, augmenting the respi- measures are or are not improved remains ambiguous and
ratory effort only did not help increase vocal fold adduc- can only be based on assumptions. When reported, respira-
tion. On the other hand, consistent increases in SPL as well tory outcomes were limited and inconsistent across studies.
as enhanced vocal fold adduction were found in the LSVT No statistical analyses were conducted to assess the causal
groups.32,35 The authors go further by suggesting that, in relationship between changes in respiratory function and
certain patients with glottal insufficiency, increasing the voice outcomes, further limiting the conclusions that could
respiratory drive without achieving sufficient glottal closure be drawn pertaining to the effects of respiratory exercises.
may even be counterproductive because it would enhance Some respiratory interventions may be similar or identical
glottal flow due to insufficient laryngeal resistance.32,104,105 to exercises targeting laryngeal or oral muscles, and there-
A greater flow rate, in addition to creating turbulence fore an intervention could have directly affected structures
affecting voice quality, would lead to a faster decline in lung involved in voice production. For instance, the Iowa Oral
volume and consequently reduce utterance duration.104,105 Performance Instrument, which was a component of the
In Roy et al’s study, teachers in the voice amplification and RET, is also commonly used to improve lingual strength.106
the resonance therapy groups underwent significant changes Moreover, as explained in a previous section, interventions
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34 Journal of Voice, Vol. &&, No. &&, 2019

TABLE 5.
Indications from the Literature Regarding Using Respiratory Exercises for Improving Voice Outcomes
Not Appropriate Potentially Appropriate
@ If respiratory function is already optimal for @ If respiratory function is impaired.
meeting vocal demands. @ If respiratory function is not meeting vocal demands.
@ If the respiratory exercises do not target the @ If the respiratory exercises target the respiratory parameters that
respiratory parameters that need improvement. need to be improved.
@ If the respiratory exercises are not accompanied @ If the changes in respiratory function are successfully generalized
by generalization exercises to voice tasks. to voice tasks.
@ If the respiratory exercises are not intense @ If the respiratory exercises yield respiratory changes that are suffi-
enough to induce respiratory changes sufficient cient to overcome laryngeal deficits.
to overcome laryngeal deficits.

that require high breathing volumes such as incentive spi- Limitations of the literature and future research
rometry, isocapnic hyperpnea, and IMST are likely to Despite the widespread use of respiratory exercises with voice
involve accessory respiratory muscles present in the neck,43 patients, the literature evaluating their effect on voice out-
such as the sternocleidomastoid and scalene muscles. comes is limited. Many studies were not included in
Although more research is needed, it is possible that a this review because they did not isolate the respiratory inter-
change in neck muscles could impact voice outcomes posi- vention as an independent variable. When studies did isolate
tively by further stabilizing the larynx during phonation, or the respiratory treatment, it often encompassed a combination
negatively by generating excessive muscle tension. of various exercises. Consequently, the specific effect
of some commonly used breathing exercises, such as sustained
exhalation on /s/ and /z/, is still unknown. A similar limitation
has been noted previously regarding research on voice exer-
cises,107 but the field at-large has since then progressed toward
Internal validity
a more specific assessment of voice therapy techniques.18
Less than half of the reviewed studies were RCTs. Within
Many studies were conducted on special patient popula-
the cross-over trials, only two out of six studies randomized
tions with impaired respiratory baseline measures, such as
the order of the intervention, and one used alternate assign-
patients with multiple sclerosis and PD. These patients’
ment. Because of the lack of strong designs, the evidence
physiology and response to respiratory exercises is likely to
provided by the studies, although informative, remains lim-
differ from the general patient population encountered in
ited. Furthermore, in most studies, important information
voice clinics, mostly constituted of healthy individuals,
was lacking to allow the reader to independently interpret
apart from their voice disorder. This makes it difficult to
the results and their validity. For example, some authors
generalize conclusions on the impact of respiratory exercises
omitted to provide raw data on individual treatments and
on respiratory and voice function to voice patients at large.
instead provided data in terms of change or in comparison
More studies should be conducted on patients whose main
with a different treatment. Many studies lacked information
complaints are their voice problems, and who do not pres-
on the participants’ compliance with the intervention. Only
ent with a significantly impaired respiratory function. More-
one study provided sample size justification, and the distri-
over, the specific effect of respiratory exercises on different
bution of the data was rarely described. Due to the small
types of voice disorders should be further studied.
sample sizes, nonparametric statistical tests should have
Lastly, as previously mentioned, no study compared the
been employed most of the time; however, parametric tests
effect of voice therapy only versus voice therapy combined
were often used instead.
with a respiratory intervention. Future studies should
address this question as its impact on clinical practice would
be significant.

External validity
The external validity of the studies was generally limited. CONCLUSIONS
The lack of information pertaining to the setting in which EMST, IMST, incentive spirometry, isocapnic hyperpnea,
the interventions were conducted decreased the generaliz- RET, exercises with a focus on abdominal breathing pat-
ability of the results. In addition, random or consecutive terns, as well as “easy breathing” as part of larger voice
samplings were rarely used while convenience sampling was therapy program, were studied in relation to voice out-
predominant, giving no evidence that the sample was repre- comes. Respiratory outcomes were assessed in approxi-
sentative of the source population and that, therefore, the mately two thirds of the studies, and seemed to be
results can be generalized. influenced by the intensity and duration of training and by
ARTICLE IN PRESS
Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 35

the participants’ baseline impairment profile. Changes in relationship between respiratory and voice improvements;
respiratory function did not always translate into voice (4) comparing “voice therapy only” to “voice therapy com-
improvements, which could have been caused by the bined with respiratory exercises”; and (5) examining the
patients’ characteristics (voice disorder and vocal demands); effects of respiratory interventions on various voice disor-
by a lack of generalization to speech tasks; or by methodo- ders.
logical reasons such as small sample sizes, study designs, or Respiratory exercises are commonly used by SLPs in
choice of outcome measures. Alternatively, some studies voice therapy. This review highlighted the importance of
reported improved voice outcomes even in the absence of choosing the right respiratory exercises (if any) depend-
enhanced respiratory function. In these cases, a change in ing on specific patient needs instead of a “one size fits
other variables, such as respiratory outcomes that were not all” approach. To ensure that respiratory exercises are
assessed in the study, or strengthening of other muscles rele- used only when appropriate and targeted for the patient's
vant to phonation, may have impacted voice outcomes. specific deficits, it is critical that their mechanism of
However, the exact mechanism of action through which action and resulting effect on voice outcomes be under-
respiratory exercises can improve voice remains unclear stood by the clinician before integrating them in a treat-
because of various limitations in the literature, including the ment plan. It is hoped that future research will
lack of studies (1) isolating specific respiratory exercises as help address the limitations highlighted in this review
independent variables; (2) reporting a complete array of to further improve clinical care of patients with voice
respiratory and voice outcomes; (3) assessing the causal disorders.

APPENDIX 1. ADAPTATION OF THE DOWNS AND BLACK CHECKLIST FOR MEASURING STUDY QUALITY

Reporting Scoring
1. Is the hypothesis/aim/objective of the study clearly described? Yes = 1
No = 0
2. Are the main outcomes to be measured clearly described in the Introduction or Methods Yes = 1
section? If the main outcomes are first mentioned in the Results section, the question No = 0
should be answered no.
3. Are the characteristics of the patients included in the study clearly described? In cohort Yes = 1
studies and trials, inclusion and/or exclusion criteria should be given. In case-control No = 0
studies, a case-definition and the source for controls should be given.
4. Are the interventions of interest clearly described? Treatments and placebo (where rele- Yes = 1
vant) that are to be compared should be clearly described. No = 0
5. Are the distributions of principal confounders in each group of subjects to be compared Yes = 2
clearly described? A list of principal confounders is provided. Partially = 1
No = 0
6. Are the main findings of the study clearly described? Simple outcome data (including Yes = 1
denominators and numerators) should be reported for all major findings so that the No = 0
reader can check the major analyses and conclusions. (This question does not cover sta-
tistical tests which are considered below).
7. Does the study provide estimates of the random variability in the data for the main out- Yes = 1
comes? In non-normally distributed data the inter-quartile range of results should be No = 0
reported. In normally distributed data the standard error, standard deviation or confi-
dence intervals should be reported. If the distribution of the data is not described, it must
be assumed that the estimates used were appropriate and the question should be
answered yes.
8. Have all important adverse events that may be a consequence of the intervention been Yes = 1
reported? This should be answered yes if the study demonstrates that there was a com- No = 0
prehensive attempt to measure adverse events. (A list of possible adverse events is
provided).
9. Have the characteristics of patients lost to follow-up been described? This should be Yes = 1
answered yes where there were no losses to follow-up or where losses to follow-up were No = 0
so small that findings would be unaffected by their inclusion. This should be answered
nowhere a study does not report the number of patients lost to follow-up.
10. Have actual probability values been reported (eg, 0.035 rather than <0.05) for the main Yes = 1
outcomes except where the probability value is less than 0.001? No = 0
(Continued)
ARTICLE IN PRESS
36 Journal of Voice, Vol. &&, No. &&, 2019

(Continued )
Reporting Scoring
External validity
11. Were the subjects asked to participate in the study representative of the entire popula- Yes = 1
tion from which they were recruited? The study must identify the source population for No = 0
patients and describe how the patients were selected. Patients would be representative Unable to
if they comprised the entire source population, an unselected sample of consecutive determine = 0
patients, or a random sample. Random sampling is only feasible where a list of all
members of the relevant population exists. Where a study does not report the propor-
tion of the source population from which the patients are derived, the question should
be answered as unable to determine.
12. Were those subjects who were prepared to participate representative of the entire pop- Yes = 1
ulation from which they were recruited? The proportion of those asked who agreed No = 0
should be stated. Validation that the sample was representative would include demon- Unable to
strating that the distribution of the main confounding factors was the same in the study determine = 0
sample and the source population.
13. Were the staff, places, and facilities where the patients were treated representative of Yes = 1
the treatment the majority of patients receive? For the question to be answered yes, the No = 0
study should demonstrate that the intervention was representative of that in use in the Unable to deter-
source population. The question should be answered no if, for example, the interven- mine = 0
tion was undertaken in a specialist center unrepresentative of the hospitals most of the
source population attend.

Internal validity-bias
14. Was an attempt made to blind study subjects to the intervention they have received? Yes = 1
For studies where the patients would have no way of knowing which intervention they No = 0
received, this should be answered yes. Unable to
determine = 0
15. Was an attempt made to blind those measuring the main outcomes of the intervention? Yes = 1
No = 0
Unable to
determine = 0
16. If any of the results of the study were based on “data dredging”, was this made clear? Yes = 1
Any analyses that had not been planned at the outset of the study should be clearly No = 0
indicated. If no retrospective unplanned subgroup analyses were reported, then answer Unable to
yes. determine = 0
17. In trials and cohort studies, do the analyses adjust for different lengths of follow-up of Yes = 1
patients, or in case-control studies, is the time period between the intervention and out- No = 0
come the same for cases and controls? Where follow-up was the same for all study Unable to
patients the answer should be yes. If different lengths of follow-up were adjusted for by, determine = 0
for example, survival analysis, the answer should be yes. Studies where differences in
follow-up are ignored should be answered no.
18. Were the statistical tests used to assess the main outcomes appropriate? The statistical Yes = 1
techniques used must be appropriate for the data. For example, nonparametric meth- No = 0
ods should be used for small sample sizes. Where little statistical analysis has been Unable to
undertaken but where there is no evidence of bias, the question should be answered determine = 0
yes. If the distribution of the data (normal or not) is not described it must be assumed
that the estimates used were appropriate and the question should be answered yes.
19. Was compliance with the intervention reported?* Yes = 1
No = 0
20. Were the main outcome measures used accurate (valid and reliable)? For studies where Yes = 1
the outcome measures were clearly described, the question was answered yes. For No = 0
studies which refer to other work or that demonstrates the outcome measures are accu- Unable to deter-
rate, the question should be answered as yes. mine = 0

Internal validity-confounding (selection bias)


21. Were the patients in different intervention groups (trials and cohort studies) or were the Yes = 1
cases and controls (case-control studies) recruited from the same population? For No = 0
example, patients for all comparison groups should be selected from the same hospital.
(Continued)
ARTICLE IN PRESS
Maude Desjardins and Heather Shaw Bonilha The Impact of Respiratory Exercises on Voice Outcomes 37

(Continued )
Reporting Scoring
The question should be answered unable to determine for cohort and case-control stud- Unable to
ies where there is no information concerning the source of patients included in the determine = 0
study.
22. Were the study subjects in different intervention groups (trials and cohort studies) or Yes = 1
were the cases and controls (case-control studies) reported over the same period of No = 0
time? For a study which does not specify the time period over which patients were Unable to
recruited, the question should be answered as unable to determine. determine = 0
23. Were the subjects randomized to intervention groups? Studies which state that subjects Yes = 1
were randomized should be answered yes except where method of randomization No = 0
would not ensure random allocation. For example, alternate allocation would score no Unable to
because it is predictable. determine = 0
24. Was the randomized intervention assignment concealed from both patients and health Yes = 1
care staff until recruitment was complete and irrevocable? All nonrandomized studies No = 0
should be answered no. If assignment was concealed from patients but not from staff, it Unable to
should be answered no. determine = 0
25. Was there adequate adjustment for confounding in the analyses from which the main Yes = 1
findings were drawn? This question should be answered no for trials if: the main con- No = 0
clusions of the study were based on analyses of treatment rather than intention to treat; Unable to
the distribution of known confounders in the different treatment groups was not determine = 0
described; or the distribution of known confounders differed between the between the
treatment groups but was not taken into account in the analyses. In nonrandomized
studies if the effect of the main confounders was not investigated or confounding was
demonstrated but no adjustment was made in the final analyses the question should be
answered as no.
26. Were losses of patients to follow-up taken into account? If the numbers of patients lost Yes = 1
to follow-up are not reported, the question should be answered as unable to determine. No = 0
If the proportion of lost to follow-up was too small to affect the main findings, the ques- Unable to deter-
tion should be answered yes. mine = 0

Power
27. Was there a sample size justification?* Yes = 1
No = 0
* Indicates when an item was slightly modified from its original version. Items excluded for: Randomized clinical trials: none. Cross-over trials: 14, 21, 22.
Repeated measures designs: 14, 21, 22, 23, 24. Single-subject studies: 14, 21, 22, 23, 24. Nonrandomized trial: none.

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