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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.
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
(n=650) (n=9)
(n=659) (n=509)
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.
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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)
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
26
24
22
20
18
16
14
12
10
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.
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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
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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
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
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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
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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
13
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14 Journal of Voice, Vol. &&, No. &&, 2019
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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
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).
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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
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(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
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
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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
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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
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-
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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
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[SPL values for conversation, reading, and sus-
tained phonation were reported in Ramig et al
(1995).]
Aerodynamic and duration
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
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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
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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
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-
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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.
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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
25
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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
ARTICLE IN PRESS
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
ARTICLE IN PRESS
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
ARTICLE IN PRESS
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.
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
ARTICLE IN PRESS
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
ARTICLE IN PRESS
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
(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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