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International Journal of Speech-Language Pathology

ISSN: 1754-9507 (Print) 1754-9515 (Online) Journal homepage: http://www.tandfonline.com/loi/iasl20

Expiratory muscle strength training improves


swallowing and respiratory outcomes in people
with dysphagia: a systematic review

Marinda Brooks, Emma McLaughlin & Nora Shields

To cite this article: Marinda Brooks, Emma McLaughlin & Nora Shields (2017): Expiratory
muscle strength training improves swallowing and respiratory outcomes in people with
dysphagia: a systematic review, International Journal of Speech-Language Pathology, DOI:
10.1080/17549507.2017.1387285

To link to this article: https://doi.org/10.1080/17549507.2017.1387285

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Published online: 01 Nov 2017.

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International Journal of Speech-Language Pathology, 2017; Early Online: 1–12

Expiratory muscle strength training improves swallowing and


respiratory outcomes in people with dysphagia: a systematic review

MARINDA BROOKS1, EMMA MCLAUGHLIN2,3 & NORA SHIELDS1,2


1
Department of Allied Health, Northern Health, Epping, Australia, 2School of Allied Health, La Trobe University,
Melbourne, Australia, and 3Department of Allied Health, Castlemaine Health, Castlemaine, Australia

Abstract
Purpose: To investigate the effects of expiratory muscle strength training on communication and swallowing outcomes in
adults with acquired motor based communication and/or swallowing difficulties of any aetiology.
Method: A systematic review was conducted. Six databases (CINAHL, MEDLINE, EMBASE, SPEECHBYTE, AMED
and PUBMED) were searched from inception until end of May 2016. Randomised and non-randomised controlled studies
and pre-test/post-test studies published in English that investigated the effects of expiratory muscle strength training were
included. Study quality was assessed using the PEDro scale. Data were analysed descriptively and effect sizes and associated
95% confidence intervals were calculated.
Result: Seven articles reporting data from five studies were included. Preliminary data suggests expiratory muscle strength
training improved airway safety during swallowing in people with dysphagia and increased the strength of the expiratory
muscles in all patient groups. There was little evidence to suggest changes in communication outcomes after expiratory
muscle strength training.
Conclusion: Speech–language pathologists might consider using expiratory muscle strength training to improve airway safety
in adults with swallowing disorders.

Keywords: Expiratory muscle strength training; maximum expiratory pressure; dysphagia; voice impairment; speech–
language pathologist; intervention

Introduction Expiratory muscle weakness can be caused by


peripheral and central nervous system conditions
The expiratory muscles expel air from the lungs and
including stroke, multiple sclerosis and Parkinson’s
play a vital role in communication and swallowing.
disease. Reduced expiratory muscle strength may
Active expiration is coordinated by the internal
intercostal muscles, which lower the rib cage and negatively affect a person’s ability to generate
decrease thoracic volume; and the abdominal wall adequate expiratory pressure for voice production,
muscles (internal and external obliques, rectus and also result in an ineffective cough, placing
abdominis and transverse abdominis), which press individuals at risk of not being able to clear the
the abdominal organs upwards into the diaphragm, airway if aspiration occurs (Sapienza & Troche,
reducing the thoracic cavity (Sapienza & Troche, 2012). Strengthening the expiratory muscles may
2012). Coughing is a coordinated activity involving improve communication by requiring less force to
expiratory muscle contraction to build up high produce higher sound volumes. This might be
positive intra-pleural and intra-airways pressures particularly important for people with neuromuscu-
and develop peak expiratory flow rates that helps lar health conditions associated with insufficient
people clear mucous and aspirated material from the vocal loudness. There are fewer research studies
lungs. Expiratory muscle contraction also assists investigating the impact of expiratory muscle
communication by moving air through the airways, strength training on speech function in populations
and the glottis, which vibrates the vocal folds with other health conditions (Chiara et al., 2006).
resulting in phonation and in the case of forced However, available studies such as Wingate et al.
exhalation, such as in singing or yelling, by generat- (2007) suggest expiratory muscle strength training in
ing abdominal and thoracic pressure to push air out addition to voice therapy may have beneficial effects
of the lungs (Sapienza & Troche, 2012). for people with dysphonia or benign vocal lesions.

Correspondence: Marinda Brooks, Northern Health, 185 Cooper Street, Epping, Victoria 3076, Australia. Email: Marinda.brooks@nh.org.au
ISSN 1754-9507 print/ISSN 1754-9515 online ß 2017 The Speech Pathology Association of Australia Limited
Published by Informa UK Limited, trading as Taylor & Francis Group
DOI: 10.1080/17549507.2017.1387285
2 M. Brooks et al.

Respiratory muscle strength training is a motor may improve dysphagia secondary to neuromuscular
exercise technique where resistive load is increased impairments (Laciuga, Rosenbek, Davenport, &
during inspiration and/or expiration using a pressure Sapienza, 2014). Research has also investigated the
threshold device (Sapienza, Troche, Pitts, & impact of expiratory muscle strength training on
Davenport, 2011). The key principle in strength professional voice users. Wingate et al. (2007)
training is progressive overload. Extensive clinical employed a repeated measures design, and investi-
research has been completed in this field, and gated treatment outcomes of a combined interven-
expiratory muscle strength training is an emerging tion of expiratory muscle strength training and voice
intervention option for speech–language patholo- therapy compared to both voice therapy alone and
gists working with individuals presenting with expiratory muscle strength training alone in two
acquired motor based communication and/or swal- groups of participants presenting with dysphonia or
lowing impairments that may be related to expira- benign vocal lesions. Results from this study sug-
tory muscle weakness. The training aims to increase gested the combined treatment approach of expira-
active expiratory pressure by increasing the ability of tory muscle strength training and voice therapy was
the expiratory muscles to generate enough force for more effective than either treatment alone (Wingate
adequate ventilation and cough. Research has also et al., 2007). Research investigating the impact of
demonstrated that during expiratory muscle strength expiratory muscle strength training on speech func-
training there is increased and prolonged activation tion in neurological populations is less robust likely
of the suprahyoid muscle group (Wheeler, Chiara, & due to the nature of the speech disorders not solely
Sapienza, 2007; Wheeler-Hegland, Rosenbek, & being due to reduced expiratory muscle strength but
Sapienza, 2008). The suprahyoid muscle group also involving motor and other impairments (Chiara
(digastric, stylohyoid, geniohyoid and mylohyoid) is et al., 2006).
located above the hyoid bone in the neck. These To date, there has been no systematic evaluation
muscles assist in elevating the hyolaryngeal complex of the evidence regarding the effectiveness of expira-
and opening the upper oesophageal sphincter during tory muscle strength training for individuals pre-
swallowing. These movements are important for senting with acquired motor based communication
airway defence during swallowing and breathing and/or swallowing impairments of any aetiology.
(Wheeler et al., 2007). Expiratory muscle strength Such synthesised information would help inform
training has been shown to increase movement of the clinical practice among speech–language patholo-
hyolaryngeal complex during swallowing and gists working with these populations.
increased opening of the upper oesophageal sphinc- Therefore, the primary aim of this systematic
ter (Troche et al., 2010; Wheeler-Hegland et al., review was to investigate the effects of expiratory
2008). muscle strength training on acquired motor based
Expiratory muscle strength training uses short communication and swallowing outcomes in adults
duration, isometric contractions of the expiratory with communication and/or swallowing difficulties
muscles to generate the maximum pressure to open of any aetiology. The secondary aims were to
the pressure release valve in a handheld respiratory investigate the effects on respiratory and quality of
pressure threshold device (Sapienza et al., 2011). life outcomes, and to describe how expiratory
During the training the pressure threshold device is muscle strength training has been applied in previ-
adjusted incrementally, to progressively increase the ous studies. Communication and swallowing dis-
resistance (progressive overload). The resistance is orders can have a profound impact on an
determined initially by measuring an individuals’ individual’s quality of life, therefore understanding
maximum expiratory pressure (MEP) using a man- how any treatment affects their daily life, is import-
ometer, and setting the device to a percentage of ant to improving quality of care.
MEP for training (e.g. 75% of MEP). The ‘‘dose’’ of
expiratory muscle strength training is typically
defined in terms of the number of repetitions, sets Method
and training days per week. A typical example of a
This review was prepared and reported with refer-
training regime is five repetitions per set, with five
ence to the Preferred Reporting Items for Systematic
sets completed per day, 5 days per week, with the
Reviews and Meta-Analyses (PRISMA) guidelines
device resistance set at 75% of the participant’s
(Moher, Liberati, Tetzlaff, & Altman, 2009). This
MEP and progressed each week (Troche et al.,
systematic review was registered on the PROSPERO
2010).
database (CRD42015026722).
Expiratory muscle strength training has been
shown to improve MEP in patients with neurological
Search strategy
and respiratory conditions (Chiara, Martin,
Davenport, & Bolser, 2006; Kim, Davenport, & The following databases were searched from the
Sapienza, 2009; Pitts et al., 2009). A narrative earliest date available through to June 2016:
review exploring the benefits of expiratory muscle CINAHL, MEDLINE, EMBASE, SPEECHBYTE
strength training suggested that this intervention and AMED databases. PUBMED was also searched
Expiratory muscle strength training for dysphagia 3

from 2010 for more recent publications. Two con- duration, frequency of intervention, resistance and
cepts related to the research questions were used to programme delivery), details about any control
construct the search strategy: (1) terms related to group (e.g. type, duration, frequency of intervention
communication and swallowing disorders treated by and who delivered the programme), intervention
speech–language pathologists and (2) expiratory setting (e.g. in-patient, out-patient and home pro-
muscle strength training (Supplementary gramme), outcome measures (quantitative and
Appendix 1). Synonyms for these concepts were qualitative) relating to communication and swallow-
used in developing the search strategy. In addition to ing dysfunction and results. Data extraction was
database searches, citation tracking of the included completed by one reviewer and reviewed for accur-
articles was performed using Google Scholar and acy by a second reviewer. These are the minimum
manual searches of the reference lists of these requirements recommended by the Cochrane
articles were also completed. Handbook for Systematic Reviews (Higgins &
The yields from the database searches were Green, 2011) for the data extraction process.
imported into bibliographic software (EndNote, Disagreements were resolved by consensus.
version X7, Thompson Reuters, Philadelphia, PA).
Duplicate articles were removed. Using predeter- Assessment of risk of bias
mined inclusion and exclusion criteria, two
Two researchers independently applied the PEDro
reviewers independently screened each item for
scale to rate the methodological quality of the
relevance by title and abstract. In cases where a
included studies (Maher, Sherrington, Herbert,
decision could not be made as to whether the
Moseley, & Elkins, 2003). The PEDro scale is a
eligibility criteria were met based on the title and
validated quality assessment tool for randomised
abstract, the full text of the article was obtained and
controlled trials. Eleven items are rated as either
the criteria re-applied by the two reviewers inde-
meeting or not meeting the criteria; a maximum
pendently. Only the items which met the eligibility
score of 10 is possible as the first item (eligibility
criteria at this stage were included in the review.
criteria) is not scored. The 11 items are: eligibility
Disagreements were resolved by consensus.
criteria, random allocation, concealed allocation,
baseline comparability, blinding of assessors, ade-
Eligibility criteria
quate follow-up, intention-to-treat analysis,
Studies were eligible for inclusion if they met the between group comparisons and point estimates
following criteria: (1) participants were aged 18 and variability. A study with a PEDro score of 6
years or older and had a diagnosed or self-reported is considered to be high quality (Moseley,
communication disorder (voice and/or motor Herbert, Sherrington, & Maher, 2002).
speech) and/or swallowing dysfunction; (2) the Disagreement between the reviewers was resolved
intervention was expiratory muscle strength train- through discussion until a consensus was reached
ing of at least 4-weeks duration with no concurrent (Supplementary Appendix 2).
interventions; (3) at least one outcome measure
was related to swallowing, communication, respira- Data syntheses
tory function or quality of life; (4) the article was
Descriptive analysis was completed to identify and
published in English; and (5) the study design was
describe the major characteristics of the included
a randomised controlled study, non-randomised
studies. Effect sizes and 95% confidence intervals
controlled study, pre-test/post-test study or cohort
were calculated for data from randomised controlled
study. Studies were excluded if they included only
studies which provided means and standard devi-
healthy participants, or if only a single session of
ations using web-based software (Curriculum
expiratory muscle strength training was completed.
Evaluation and Management Centre, 2016). For
Narrative reviews, single case studies, case series
pre-test/post-test study designs, effect sizes were
designs, abstracts, posters and opinion pieces were
calculated by measuring the difference between pre-
excluded. The authors defined randomised con-
and post-test within group scores divided by the
trolled study as outlined with the CONSORT
standard deviation of the difference score. Where
statement (Moher et al., 2010) as an experiment
raw data were not available, approximations were
in which two or more interventions, possibly
made through comparison of the standard deviation
including a control intervention or no intervention,
to the re-test estimates of reliability for relevant
are compared by being randomly allocated to
outcomes or by d ¼ ptN, (where d ¼ effect size,
participants.
t ¼ reported t-test value, N ¼ number of participants)
with associated 95% confidence intervals
Data extraction
(Rosenthal, 1991). Effect size values were inter-
A customised form was developed for data extrac- preted as follows: a small effect if 0.2, a moderate
tion. The following data were extracted: character- effect if 0.5, and a large effect if 0.8 (Cohen, 1988).
istics of the study participants (e.g. age, gender and Meta-analysis was not performed due to the hetero-
diagnoses), details about the intervention (e.g. type, geneity of outcomes measures used.
4 M. Brooks et al.

Results Chiara et al. (2006) was excluded because the


participants with multiple sclerosis ‘‘had never
Study selection
received speech therapy for any speech or voice
The search strategy yielded 2898 potentially relevant problem’’ and it was unclear if all participants had
articles (Figure 1). After removal of duplicates, the dysarthria pre-treatment; Plowman et al. (2015) was
inclusion and exclusion criteria were applied to the excluded as only five of the 15 participants with
titles and abstracts of 1153 articles. There was good Amyotrophic Lateral Sclerosis (ALS) had dysphagia;
agreement between reviewers when applying eligi- and Hegland et al. (2016) was excluded as it was
bility criteria to titles and abstracts (k ¼ 0.969 95% unclear whether all participants had dysphagia.
CI 0.926–1.000). Full-text copies for 37 articles Seven articles reporting data from five studies were
were retrieved. Thirty articles were excluded after retained for inclusion in the review (Park, Oh,
review of the full text (Figure 1). For example, Chang, & Kim, 2016; Pitts et al., 2009; Roy et al.,
Wingate et al. (2007) was excluded because the 2003; Sapienza et al., 2011; Troche et al., 2010;
intervention combined voice therapy with expiratory Troche, Rosenbek, Okun, & Sapienza, 2014; Tsai,
muscle strength training; Reyes et al. (2015) was Huang, Liou, & Kuo, 2016).
excluded as it used a combined intervention of Four of the included studies were randomised
inspiratory and expiratory muscle strength training; control trials (Park et al., 2016; Roy et al., 2003;

Figure 1. Study selection process to identify eligible articles for inclusion in the review.
Expiratory muscle strength training for dysphagia 5

Idiopathic Parkinson’s disease

Idiopathic Parkinson’s disease


Idiopathic Parkinson’s disease
Idiopathic Parkinson’s disease
Troche et al., 2010; Tsai et al., 2016) and the fifth
had a single group pre-test/post-test study design

Dysphagia post stroke


(Pitts et al., 2009) (Table I). The five studies

Diagnoses
included 190 participants: 70 participants with

Voice impairment

Voice impairment
idiopathic Parkinson’s disease (mean age 69 years;
18% female), 93 participants with voice impairment
and 27 with dysphagia secondary to a recent stroke
(mean age 65 years, 55% female).

Risk of bias assessment

22M 8F
22M 8F

2M 12F
Control

6M 7F
The overall average quality of the five studies was

NR
moderate (mean PEDro score was 5, range 1–9;

Gender
Table I). Two of the five studies employed blinded
assessment (Park et al., 2016; Troche et al., 2010)

25M 5F
25M 5F

1M 14F
EMST

8M 2F

6M 8F
and two studies used intention to treat analysis

10M

NR
(Troche et al., 2010; Tsai et al., 2016). There was
one high quality study that was a randomised,
blinded, sham-controlled trial where the participants

65.8 (11.3) (47–82)


and therapists were blinded to the intervention

Control
(Troche et al., 2010). The quality of the two single

Age (years) Mean (SD)

68.5 (10.3)
68.5 (10.3)
group pre-test/post-test studies was lower (Table I).

Note: EMST ¼ Expiratory Muscle Strength Training; NR ¼ not reported; RCT ¼ Randomised Control Trial; M ¼ male; F ¼ female.
There was moderate agreement between reviewers

NR

NR
when rating the quality of the included studies
(k ¼ 0.571 95% CI 0.378–0.763).

42.0 (10.6)

64.3 (10.7)
66.7 (8.9)
66.7 (8.9)
70.0 (6.4)
Description of the expiratory muscle
EMST

(50–80)
strength training
72.9

NR
Table II summarises the key features of the expira-
tory muscle strength training intervention delivered
10

60
60
10

64

29
27
in the included studies and highlight their simila-
n

rities in terms of the content of the programmes


implemented. Two studies (Park et al., 2016; Troche
Control – no intervention
Voice amplification OR
Comparison/Control

et al., 2010) included a sham control group, one


study (Roy et al., 2003) compared expiratory muscle
resonance therapy
Sham controlled
Sham controlled

Sham controlled
strength training to voice amplification and reson-
ance therapy and one study (Tsai et al., 2016) had a
no intervention control group. The programmes
ranged from 4 to 6 weeks in duration, using an
intensity of between 70 and 80% MEP. The resist-

ance was adjusted weekly in three studies (Pitts


et al., 2009; Troche et al., 2010; Tsai et al., 2016),
Pre-post single

Pre-post single
group study

group study
Study Design

twice in 6 weeks in one study (Roy et al., 2003) and


was not adjusted at all in one study (Park et al.,
RCT
RCT

RCT

RCT
RCT

2016). Participants in all studies were instructed


how to complete the training in a health clinic or
hospital and the intervention was completed at home
Table I. Characteristics of included studies.

PEDro Score

except for one study that was completed in the


(max 10)

inpatient hospital setting (Park et al., 2016). In two


2

8
8
1

6
7

studies (Troche et al., 2010; Tsai et al., 2016),


participants were reviewed weekly by a health
professional either in the clinic or at home. Written
instructions were provided to participants in three of
Sapienza et al. (2011)
Troche et al. (2010)

Troche et al. (2014)

the studies (Pitts et al., 2009; Roy et al., 2003;


Park et al. (2016)
Pitts et al. (2009)

Tsai et al. (2016)


Roy et al. (2003)

Troche et al., 2010). Two studies (Roy et al., 2003;


Troche et al, 2010) requested participants complete
a training logbook but data on programme adher-
Study

ence was only reported in one study (Roy et al.,


2003) that rated adherence as 4.3 out of 5.
6
M. Brooks et al.

Table II. Characteristics of the intervention and control programmes.


Intervention Control

Frequency Description Resistance/load Description


Study Description Duration (days/week) (reps) (%MEP) Delivery Description Duration Frequency (reps) Resistance Delivery
Pitts et al. EMST 4 weeks 5 days 5 sets  5 75% MEP, Handheld device, – – – – – –
(2009) breaths ¼ 25 adjusted weekly home practice
Troche et al. EMST 4 weeks 5 days 5 sets  5 75% MEP, Handheld device, Sham EMST 4 weeks 5 days per 5 sets  5 Adjusted Hand held
(2010), breaths ¼ 25 adjusted weekly home practice device week breaths ¼ 25 weekly EMST
Sapienza et al. breaths however device,
(2011) no actual home
Troche et al. resistance practice
(2014) load
Roy et al. Respiratory 6 weeks 5 days 5 sets  5 80% MEP, Hand held treat- No control, 2 VA and RT using Daily – – –
(2003) Muscle breaths ¼ adjusted twice ment device, other therapy
Training 25 breaths in week 2 and Trained by clin- intervention programme.
using a pressure week 4 ician and groups, 1.
threshold then home VA, 2 RT.
device practice
Tsai et al. EMST 5 weeks 3 days 5 sets  75% MEP, Handheld device, No intervention – – – – –
(2016) 5 breaths ¼ adjusted weekly location not
25 breaths specified
Park et al. EMST 4 weeks 5 days 5 sets  70% MEP, not Expiratory muscle Sham EMST 4 weeks 5 days 5 sets  5 Adjusted Hand held
(2016) 5 breaths ¼ specified strength trainer device breaths ¼ 25 weekly EMST
25 breaths device, in breaths however device, in
hospital no actual hospital
resistance
load

Note: Pemax ¼ measurement of expiratory respiratory strength; MEP ¼ Maximal Expiratory Pressure; EMST ¼ Expiratory Muscle Strength Training; VA ¼Voice amplification; RT ¼ Resonance therapy.
Expiratory muscle strength training for dysphagia 7

Effectiveness of expiratory muscle strength after expiratory muscle strength training programme
training was discontinued and found mean scores remained
17% above baseline values (Troche et al., 2010).
The five studies measured quantitative outcomes
Seven participants had no change in their
related to swallowing (Park et al., 2016; Pitts et al.,
Penetration–Aspiration Scale scores, one partici-
2009; Troche et al., 2010); communication (Roy
pant’s scores had deteriorated, and two participants
et al., 2003; Tsai et al., 2016) and respiration (Roy
had improved scores (Troche et al., 2010). This is a
et al., 2003; Sapienza et al., 2011; Troche et al.,
small participant sample and so these data (includ-
2010; Tsai et al., 2016). Figure 2 displays the effect
ing their generalisability to the broader population)
sizes for these outcomes at completion of expiratory
should be interpreted with caution.
muscle strength training. No studies explicitly
Park et al. (2016) demonstrated a significant
reported on adverse events as a result of expiratory
improvement in activity of the suprahyoid muscles in
muscle strength training.
favour of the expiratory muscle strength training
group. Troche et al. (2010) study revealed that there
Effect on swallowing
was no statistically significant change in the duration
The effect of expiratory muscle strength training
of hyoid movement over time in the expiratory
on swallow function was evaluated in three studies muscle strength training group, but there was a
(Park et al., 2016; Pitts et al., 2009; Troche et al., significant decrease over time for this outcome in the
2010), using four different outcome measures; the sham group.
Penetration–Aspiration Scale (Rosenbek, Robbins,
Roecker, Coyle, & Woods, 1996) (a validated Effect on communication
ordinal measure used to rate the degree of laryn- Two studies (Roy et al., 2003; Tsai et al., 2016)
geal penetration and/or aspiration observed during investigated the effect of expiratory muscle strength
swallowing), the Functional Oral Intake Scale training on communication outcomes. Both studies
(Crary, Mann, & Groher, 2005) (a 7-point scale used voice related quality outcome measures as their
used to evaluate oral intake of foods and liquids), primary outcome measure. Roy et al. (2003) found
activity of the suprahyoid muscles as measured by no reduction in perceived voice handicap as mea-
surface electromyography (sEMG) and hyolaryn- sured by the Voice Handicap Index (Jacobsen et al.,
geal movement analysed via digital recordings 1997), which assesses self-perceived psychosocial
post-Videofluorscopy Swallowing Studies (VFSS). consequences of voice disorders, nor demonstrated a
All three studies (Park et al., 2016; Pitts et al., reduction in self-perceived voice severity, in the
2009; Troche et al., 2010) reported a reduction in group allocated the expiratory muscle strength
scores on the Penetration–Aspiration Scale after training intervention. Tsai et al. (2016) found
expiratory muscle training intervention. These significant improvement in self-awareness of vocal
results suggest that an intervention targeting symptoms in the domains of ‘‘effects on work’’ and
expiratory muscle strength and activation of the ‘‘effects on mood’’ in favour of the expiratory muscle
suprahyoid muscle group resulted in decreased strength training group using a questionnaire
aspiration, with a large effect for fluids and a designed specifically for their study (Figure 2).
moderate effect size for solids (Figure 2). It is Tsai et al. (2016) also reported no change in
important to highlight that Troche et al. (2010) maximum phonation time (maximum time in sec-
reported 11 participants had improved onds for which a person can sustain a vowel sound
Penetration–Aspiration Scale scores following the when produced on one deep breath) and s/z ratio (a
training programme as compared to five in the measure of vocal adduction efficiency and laryngeal
sham group. Furthermore, the Penetration- control) after expiratory muscle strength training.
Aspiration scores of three participants had deterio- Maximal phonation time and s/z ratio measures have
rated following the intervention compared to 16 in been suggested for diagnostic use in voice evalu-
the sham group. This study also reported that the ations. Limited normative data are available for
number needed to treat to gain one additional maximum phonation time in healthy older individ-
benefit was 1.8 (95% CI 1.2–3.4). Despite the uals, and research reporting normative data for s/z
small participant numbers reported, mean ratios has been inconsistent with differing proced-
Penetration–Aspiration Scale scores improved for ures and practice effects impacting the reliability and
the expiratory muscle strength training group only validity of this measure (Gelfer & Pazera, 2006).
(0.61  1.43; 95% CI 0.10–1.11) and age and Tsai et al. (2016) did not report clear procedures or
disease severity had no significant influence on the inter-rater reliability scores for either of these
treatment effects (Troche et al., 2010). Raw scores outcomes. Standardised procedures for maximum
for penetration and aspiration numbers were not phonation time and s/z ratio would improve meas-
reported by Park et al. (2016). urement of these outcomes within studies, diminish
Detraining effects on swallow function were the impact of errors and improve the ability to
investigated in a small convenience sample of 10 reliably measure treatment effects (Maslan et al.,
participants with Parkinson’s disease three months 2011).
8 M. Brooks et al.

Figure 2. Standardised mean differences and 95% confidence intervals for swallowing outcome measures respiratory outcomes measures
and communication outcomes measures for expiratory muscles strength training. *RCT, }pre/post, ^pre-/post-data from single group
within a RCT.

Effect on respiration muscle strength training intervention (Figure 2).


Four studies (Pitts et al., 2009; Roy et al., 2003; Additional MEP data of only half of the participants
Troche et al., 2010; Tsai et al., 2016) investigated allocated into the expiratory muscle strength group
the effect of expiratory muscle strength training on (n ¼ 12) was provided by Roy et al. (2003) for
respiratory outcome measures and found improve- participants randomly allocated into their expiratory
ments in MEP across all studies post-expiratory muscle strength training group. Results from these
Expiratory muscle strength training for dysphagia 9

four studies suggest the intervention was effective in training is probably related to a change in supra-
improving MEP scores using an expiratory muscle hyoid muscle function. The suprahyoid muscles are
strength training intervention. Pitts et al. (2009) also responsible for elevation of the hyolaryngeal com-
reported improvements in some parameters of the plex and opening the upper oesophageal sphincter
cough wave form (e.g. cough acceleration volume) during swallowing (Wheeler et al., 2007). Research
related to increased effort in the expiratory phase of shows targeted exercise can activate the suprahyoid
respiration. Parameters of the cough wave form muscles in stroke survivors with dysphagia (Shaker
dependent on pulmonary function did not change et al., 2002), producing improved swallow outcomes
significantly due to 80% of the participants with by increasing anterior hyolaryngeal excursion and
Parkinson’s disease in this study having restrictive opening the upper oesophageal sphincter (Shaker
lung disease. No improvement in pulmonary func- et al., 2002). There is also preliminary evidence
tion parameters was demonstrated in two studies from sEMG studies in healthy participants showing
that investigated this outcome (Troche et al., 2010; that expiratory muscle strength training increases
Tsai et al., 2016). the timing and amplitude of suprahyoid muscle
activity (Wheeler et al., 2007). This suggests that
Effect on quality of life expiratory muscle strength training increases motor
Only one study (Troche et al., 2010) evaluated the unit recruitment of the suprahyoid muscle complex
effect of expiratory muscle strength training inter- (Wheeler et al., 2007). Together this literature
vention on quality of life. This study reported an suggests that speech–language pathologists may
improvement in swallowing-related quality of life implement expiratory muscle strength training as
overall (F ¼ 3.007, p ¼ 0.007) but found no differ- one way to achieve improved airway protection in
ence between the groups that received active and patients with dysphagia. Studies are needed to
sham expiratory muscle strength training compare expiratory muscle strength training and
intervention.
other more traditional ways of improving swallowing
safety.
Discussion The effect of expiratory muscle strength training
on voice function remains unclear and there is no
Data from this review found that expiratory muscle
conclusive evidence supporting this intervention in
strength training improved maximal expiratory pres-
isolation for voice therapy. Roy et al. (2003)
sure scores across four studies including participants
acknowledge that within their participant group
with different conditions: people with Parkinson’s
they did not define/diagnose the precise nature of
disease, stroke survivors and people with self-
voice disturbance or identify severity of vocal fold
reported voice problems (Pitts et al., 2009; Roy
pathology. Nonetheless, despite significant changes
et al., 2003; Troche et al., 2010; Tsai et al., 2016).
in MEP following treatment, this did not translate
This review also provides preliminary evidence that
expiratory muscle strength training may be effective into functionally perceived voice improvements by
in improving airway protection in adults with participants (Roy et al., 2003; Tsai et al., 2016). It is
dysphagia secondary to Parkinson’s disease or clear that further research is needed, utilising func-
stroke (Park et al., 2016; Pitts et al., 2009; Troche tional communication outcome measures, to identify
et al., 2010). This could have significant implica- which populations benefit from expiratory muscle
tions for the management of dysphagia by speech– strength training as a clinical utility in relation to
language pathologists in the health setting as effect- motor based communication impairments.
iveness of airway protection and the presence/ Overall, there is a paucity of research investigating
absence of penetration and/or aspiration are often the effects of expiratory muscle strength training,
key factors underpinning a variety of safe swallowing among people with swallowing and/or acquired
recommendations (Troche et al., 2010). motor-based communication impairments, on out-
Preliminary evidence from three studies suggests comes relevant to speech–language pathologists.
expiratory muscle strength training may improve Only three studies (Park et al., 2016; Pitts et al.,
airway protection in adults with dysphagia (Park 2009; Troche et al., 2010) assessed swallow related
et al., 2016; Pitts et al., 2009; Troche et al., 2010). outcomes and two studies (Roy et al., 2003; Tsai
These studies found a reduction in participant et al., 2016) assessed communication. Therefore, it
scores on the Penetration–Aspiration Scale after is unclear if individuals with dysphagia caused by
expiratory muscle training, that is, less laryngeal neuromuscular or neurodegenerative conditions
penetration and/or aspiration was observed during other than Parkinson’s disease or stroke would also
swallowing. This indicates a functional improvement benefit from expiratory muscle strength training.
in airway protection. Superior and anterior hyolar- Further research is required to understand the range
yngeal excursion is the pattern of movement directly of individuals with acquired motor based communi-
involved in airway protection and clearance of cation and swallowing impairments who might
material through the pharynx. Improved airway benefit most from this intervention and the optimal
protection as a result of expiratory muscle strength time to intervene.
10 M. Brooks et al.

The strength training literature recommends muscle strength training and other interventions for
programmes of at least 6 weeks’ duration to observe their clients.
changes in muscle strength and implementing the Several of these excluded studies do have results,
principle of progressive overload (i.e. need to con- relevant to speech–language pathologists, in clinical
tinually increase the exercise demands on the populations that often present with acquired com-
muscle) (Burkhead, Sapienza, & Rosenbek, 2007). munication or swallowing difficulties during the
An expiratory muscle strength training hand-held trajectory of their disease (Chiara et al., 2006;
device as utilised in the reviewed studies can be Hegland et al., 2016; Plowman et al., 2015; Reyes
adjusted to increase the load or resistance of the et al., 2015). Many of these excluded studies report
training. None of the included studies implemented significant improvements in MEP post-expiratory
both of these recommendations. The three studies muscle strength training intervention (Chiara et al.,
that included progressive overload were of less than 2006; Hegland et al., 2016; Plowman et al., 2015) as
6 weeks duration (Pitts et al., 2009; Troche et al., found in this review. However, these excluded
2010; Tsai et al., 2016) and the one study that studies report mixed results on the effect of expira-
implemented a 6-week programme did not apply tory muscle strength training on dysphagia. For
progressive overload (Roy et al., 2003). It is unclear example, there was no significant reduction in
if a 6-week programme combined with progressive Penetration–Aspiration Scale scores after expiratory
overload would have resulted in greater change in muscle strength training in a group of stroke patients
the swallow and communication outcomes mea- (Hegland et al., 2016) or in five people with ALS
sured. Further research is also needed on the (Plowman et al., 2015). One excluded study also
adherence of participants to the training programme reported no change in voice production outcome
as this was not documented adequately in any study. measures or voice related quality of life in people
Adverse outcomes were not reported by any with multiple sclerosis (Chiara et al., 2006). Further
study. Completion of the intervention each day research is important to investigate the benefit of
does require a small time commitment; however, no expiratory muscle strength training in conjunction
with a swallow specific or communication specific
reports of hardship or burden were reported.
rehabilitation programme in patient groups with
Anecdotally, improved swallow function for individ-
conditions of neurological aetiology.
uals with dysphagia is a strong motivator.
This review was registered with PROSPERO and
Swallowing rehabilitation techniques aimed at res-
used a broad search strategy to identify the evidence
toration of function provide an opportunity for the
base. However, the final yield was small, comprising
individual to actively participate in their rehabilita-
seven articles that reported outcomes for five
tion and recovery. Troche et al. (2010) concluded
studies. Five of the seven articles included were
from their study that in addition to expiratory
generated by the same research group (Pitts et al.,
muscle strength training being beneficial it was also
2009; Troche et al., 2010, 2014) and it is unclear the
not considered burdensome for patients and can extent to which the participants recruited to these
result in improved quality of life. studies overlap. Therefore, participant duplication
Expiratory muscle strength training has been cannot be ruled out as a source of bias. The available
investigated in other populations including seden- data from the five included studies were also
tary older adults, and people with multiple sclerosis, heterogeneous representing different diagnostic
chronic obstructive pulmonary disease, spinal cord groups (dysphagia and voice impairment), and in
injury, myasthenia gravis, ALS and Huntington’s one case (Roy et al., 2003) additional data on MEP
Disease, among others. We acknowledge that there was provided for 12 participants who had been
are other studies that are potentially relevant to this randomly allocated to the expiratory muscle strength
area that were not included in this review as it was training group.
unclear if the participants in these studies had an Other limitations of this review include that only
existing communication and/or swallowing impair- English language articles were considered. However,
ment (Chiara et al., 2006; Hegland et al., 2016; the titles and abstracts of articles written in other
Plowman et al., 2015) or because a combined languages were reviewed, and none appeared to
intervention was employed (Reyes et al., 2015; meet the inclusion criteria. Research using more
Wingate et al., 2007). This highlights the need for than one or combining multiple interventions, such
speech–language pathologists to advocate for as expiratory and inspiratory muscle training were
improved reporting of participant characteristics in also excluded. This was to ensure that any change in
publications and the inclusion of participants with outcome measures could be attributed solely to the
communication and swallowing difficulties in clin- expiratory muscle strength training programme. We
ical trials. It is important that studies in these also excluded data that had not been published in a
population groups more comprehensively describe peer-reviewed journal and therefore grey literature
the characteristics of their participants in relation to that may include other relevant data were not
communication and/or swallowing to enable clin- included in the review. Finally, it is also acknowl-
icians to ascertain the clinical utility of expiratory edged that a further limitation of this review is the
Expiratory muscle strength training for dysphagia 11

use of the PEDro scale to assess the methodological maximal expiratory pressure, pulmonary function, and max-
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e1000097. doi: 10.1371/journal.pmed1000097
The authors report no declarations of interest. Moher, D., Hopewell, S., Schulz, K.F., Montori, V., Gøtzsche,
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Supplementary material 9514(14)60281-6
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Supplemental data for this article can be accessed at of expiratory muscle strength training on oropharyngeal
https://doi.org/10.1080/17549507.2017.1387285. dysphagia in subacute stroke patients: A randomised control
trial. Journal of Oral Rehabilitation, 43, 364–372. doi: 10.1111/
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