Respiratory muscle training for cervical spinal cord injury(Review)
Berlowitz D, Tamplin J

This is a reprint of a Cochrane review, prepared and maintained by The Cochrane Collaboration and published in The Cochrane Library
2013, Issue 7
http://www.thecochranelibrary.com

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

TABLE OF CONTENTSHEADER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ABSTRACT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
PLAIN LANGUAGE SUMMARY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
SUMMARY OF FINDINGS FOR THE MAIN COMPARISON . . . . . . . . . . . . . . . . . . .
BACKGROUND . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
OBJECTIVES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
METHODS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
RESULTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Figure 1.
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Figure 2.
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Figure 3.
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DISCUSSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
AUTHORS’ CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ACKNOWLEDGEMENTS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CHARACTERISTICS OF STUDIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
DATA AND ANALYSES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Analysis 1.1. Comparison 1 Respiratory muscle training versus control, Outcome 1 Dyspnoea. . . . . . . . .
Analysis 1.2. Comparison 1 Respiratory muscle training versus control, Outcome 2 Vital capacity (L). . . . . .
Analysis 1.3. Comparison 1 Respiratory muscle training versus control, Outcome 3 Maximal inspiratory pressure(cmH2 O). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Analysis 1.4. Comparison 1 Respiratory muscle training versus control, Outcome 4 Maximal expiratory pressure(cmH2 O). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Analysis 1.5. Comparison 1 Respiratory muscle training versus control, Outcome 5 Forced expiratory volume in 1 second(L). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ADDITIONAL TABLES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
APPENDICES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CONTRIBUTIONS OF AUTHORS . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
DECLARATIONS OF INTEREST . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
SOURCES OF SUPPORT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
DIFFERENCES BETWEEN PROTOCOL AND REVIEW . . . . . . . . . . . . . . . . . . . . .

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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[Intervention Review]

Respiratory muscle training for cervical spinal cord injury
David Berlowitz1 , Jeanette Tamplin1
1

Institute for Breathing and Sleep, Austin Health, Heidelberg, Australia

Contact address: David Berlowitz, Institute for Breathing and Sleep, Austin Health, 145 Studley Road, Heidelberg, 3084, Australia.
david.berlowitz@austin.org.au.
Editorial group: Cochrane Injuries Group.
Publication status and date: New, published in Issue 7, 2013.
Review content assessed as up-to-date: 28 June 2013.
Citation: Berlowitz D, Tamplin J. Respiratory muscle training for cervical spinal cord injury. Cochrane Database of Systematic Reviews
2013, Issue 7. Art. No.: CD008507. DOI: 10.1002/14651858.CD008507.pub2.
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

ABSTRACT
Background
Cervical spinal cord injury (SCI) severely comprises respiratory function due to paralysis and impairment of the respiratory muscles.
Various types of respiratory muscle training (RMT) to improve respiratory function for people with cervical SCI have been describedin the literature. A systematic review of this literature is needed to determine the effectiveness of RMT (either inspiratory or expiratory
muscle training) on pulmonary function, dyspnoea, respiratory complications, respiratory muscle strength, and quality of life for people
with cervical SCI.
Objectives
To evaluate the efficacy of RMT versus standard care or sham treatments in people with cervical SCI.
Search methods
We searched the Cochrane Injuries and Cochrane Neuromuscular Disease Groups’ Specialised Register, the Cochrane Central Registerof Controlled Trials (CENTRAL) (2012, Issue 1), MEDLINE, EMBASE, CINAHL, ISI Web of Science, PubMed, and clinical trials
registries (Australian New Zealand Clinical Trials Registry, ClinicalTrials, Controlled Trials metaRegister) on 5 to 8 March 2013. We
handsearched reference lists of relevant papers and literature reviews. We applied no date, language, or publication restrictions.
Selection criteria
All randomised controlled trials that involved an intervention described as RMT versus a control group using an alternative intervention,
placebo, usual care, or no intervention for people with cervical SCI were considered for inclusion.
Data collection and analysis
Two review authors independently selected articles for inclusion, evaluated the methodological quality of the studies, and extracted
data. We sought additional information from the trial authors when necessary. We presented results using mean differences (MD)(using post-test scores) and 95% confidence intervals (CI) for outcomes measured using the same scale or standardised mean differences(SMD) and 95% CI for outcomes measured using different scales.
Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Main results
We included 11 studies with 212 participants with cervical SCI. The meta-analysis revealed a statistically significant effect of RMT
for three outcomes: vital capacity (MD mean end point 0.4 L, 95% CI 0.12 to 0.69), maximal inspiratory pressure (MD mean end
point 10.50 cm/H2 O, 95% CI 3.42 to 17.57), and maximal expiratory pressure (MD mean end point 10.31 cm/H2 O, 95% CI 2.80
to 17.82). There was no effect on forced expiratory volume in one second or dyspnoea. We could not combine the results from qualityof life assessment tools from three studies for meta-analysis. Respiratory complication outcomes were infrequently reported and thus
we could not include them in the meta-analysis. Instead, we described the results narratively. We identified no adverse effects as a resultof RMT in cervical SCI.
Authors’ conclusions
In spite of the relatively small number of studies included in this review, meta-analysis of the pooled data indicates that RMT is effective
for increasing respiratory muscle strength and perhaps also lung volumes for people with cervical SCI. Further research is needed onfunctional outcomes following RMT, such as dyspnoea, cough efficacy, respiratory complications, hospital admissions, and quality oflife. In addition, longer-term studies are needed to ascertain optimal dosage and determine any carryover effects of RMT on respiratory
function, quality of life, respiratory morbidity, and mortality.

PLAIN LANGUAGE SUMMARY
Training the muscles used for breathing after a spinal cord injury
After an injury at a high point on the spinal cord (a cervical injury), the muscles responsible for breathing are paralysed or weakened.
This weakness reduces the volume of the lungs (lung capacity), the ability to take a deep breath and cough, and puts them at greater riskof lung infection. Just like other muscles of the body, it is possible to train the breathing (respiratory) muscles to be stronger; however, it
is not clear if such training is effective for people with a cervical spinal cord injury. This review compared any type of respiratory muscle
training with standard care or sham treatments. We reviewed 11 studies (including 212 people with cervical spinal cord injury) andsuggested that for people with cervical spinal cord injury there is a small beneficial effect of respiratory muscle training on lung volume
and on the strength of the muscles used to take a breath in and to breathe air out and cough. No effect was seen on the maximum
amount of air that can be pushed out in one breath, or shortness of breath. An insufficient number of studies had examined the effectof respiratory muscle training on the frequency of lung infections or quality of life, so we could not assess these outcomes in the review.
We identified no adverse effects of training the breathing muscles for people with a cervical spinal cord injury.

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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RMTControl147(8 studies)58(3 studies)

No of Participants(studies)

Maximum inspiratory The mean maximum in- The mean maximum inpressure
spiratory pressure ranged spiratory pressure in the
Follow-up: 6-12 weeks
across control groups intervention groups wasfrom
10.66 higher
43 to 102 cm/H2 O(3.59 to 17.72 higher)

Relative effect(95% CI)108(4 studies)

The mean dyspnoea in theintervention groups was
0.10 standard deviations
lower(1.65 lower to 1.44
higher)Corresponding risk

Assumed risk

Illustrative comparative risks* (95% CI)

The mean vital capac- The mean vital capacity
ity ranged across control in the intervention groups
groups fromwas
1.4 to 2.7 L
0.40 higher(0.12 to 0.69 higher)

Vital capacity
Follow-up: 6-12 weeks

Dyspnoea
Borg scale, modified Borg
scale, and visual analogue scale
Follow-up: 6-8 weeks

OutcomesPatient or population: cervical spinal cord injury
Settings: hospital and community
Intervention: RMTComparison: control

Respiratory muscle training compared with control for cervical spinal cord injury

S U M M A R Y O F F I N D I N G S F O R T H E M A I N C O M P A R I S O N [Explanation]⊕⊕
low1,2⊕⊕
low1,2,3⊕⊕
low1,2

Quality of the evidence(GRADE)

SMD 0.03 (-0.37 to 0.44)

SMD 0.97 (0.02 to 1.93)

SMD 0.23 (-0.45 to 0.91)

Comments

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Not estimable14(1 study)

⊕⊕⊕⊕
high

⊕⊕
low1,2,3⊕⊕
low1,2,3⊕⊕
low1,2,3

SMD 0.25 (-0.34 to 0.85)

SMD 0.02 (-0.37 to 0.42)3Blinding and allocation concealment unclear.

2 Inconsistency of results + small number of studies with small sample sizes.

1 High risk of attrition bias.

GRADE Working Group grades of evidenceHigh quality: Further research is very unlikely to change our confidence in the estimate of effect.
Moderate quality: Further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate.
Low quality: Further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate.
Very low quality: We are very uncertain about the estimate.

*The basis for the assumed risk (e.g. the median control group risk across studies) is provided in footnotes. The corresponding risk (and its 95% confidence interval) is based on theassumed risk in the comparison group and the relative effect of the intervention (and its 95% CI).
CI: confidence interval; RMT: respiratory muscle training; SMD: standardised mean difference

See comment

Respiratory complica- See comment
tions
Follow-up: 8 weeks

78(4 studies)

Not estimable

Quality of life
Follow-up: 6-12 weeks

See comment

97(4 studies)

Forced expiratory vol- The mean forced expi- The mean forced expiraume in 1 second
ratory volume in 1 sec- tory volume in 1 second
Follow-up: 6-12 weeks
ond ranged across con- in the intervention groups
trol groups fromwas
1.7 to 2.4 L
0.05 higher(0.23 lower to 0.34
higher)See comment

151(6 studies)

Maximum
expiratory The mean maximum ex- The mean maximum expipressurepiratory pressure ranged ratory pressure in the inacross control groups tervention groups was
Follow-up: 6-12 weeks
from
10.31 higher
41 to 91 cm/H2 O(2.80 to 17.82 higher)

BACKGROUND
Spinal cord injury (SCI) is damage to the spinal cord that results
in a loss or impairment of function resulting in reduced mobilityor sensation. When the spinal cord is injured, muscles below thelevel of injury become paralysed or impaired. Higher levels of
injury cause greater impairment. In addition to paralysis of lower
or upper limbs (or both), SCI may also affect respiratory function
due to complete or partial paralysis of the respiratory muscles.
The extent of the respiratory dysfunction is dependent on boththe level of injury and the completeness of the lesion. Typically,paralysis of all muscles involved in respiration occurs with spinal
cord lesions above C3. The phrenic nerve receives motor supplies
from C3, C4, and C5, and, therefore, injury above C6 may impair
diaphragm function.

2006; Chen 1990). In particular, paralysis of intercostal and abdominal muscles causes a decrease in inspiratory volume duringresting breathing, and the loss of expiratory force during cough(Alvarez 1981). This respiratory inefficiency also increases the riskof respiratory muscle fatigue, particularly when load is imposedon the muscles, as with pneumonia or obstruction of the airways(Fugl-Meyer 1984).

Description of the intervention

Respiratory complications following SCI are common, with a particularly high reported prevalence of mucous retention, atelectasis, pneumonia, and respiratory failure (Fishburn 1990; Reines
1987). Thus, any intervention that improves respiratory function
and thereby prevents or alleviates these conditions would be ofgreat benefit to people with SCI.

Respiratory muscle training (RMT) involves specific training of
inspiratory, expiratory, or both, muscles to yield improvements
in both strength and endurance. The respiratory muscles can betrained in a similar way to the limb muscles with devices that increase the load on the muscles. A training session typically consistsof a certain number of exercise repetitions, or a particular lengthof time spent exercising. Training intensity is individually set at apercentage of the maximum measured respiratory strength, respiratory pressure, or ventilatory capacity, depending on the chosen
technique.
Resistive training involves breathing through a small diameter hole(resistor), which limits available flow and thus increases ventilatory (training) load. Threshold training involves breathing with
sufficient force to overcome a spring-loaded valve and enable airflow. Both resistive and threshold trainers typically involve a oneway valve system such that either the inspiratory or the expiratory
muscles are trained selectively.
Normocapnic hyperpnoea is an alternative form of RMT that involves simultaneous training of inspiratory and expiratory muscles.
The device used for normocapnic hyperpnoea training consistsof a re-breathing bag (at 30% to 40% of the participant’s forcedVC) connected to a tube system and mouthpiece. Participants are
instructed to fill and empty the bag completely with each breath.
To avoid an increase in carbon dioxide, a small hole in the tube
permits additional inspiratory and expiratory flow. The training
load provided in hyperpnoea training results from high minuteventilation rather than high resistive loads as in resistive training.
Singing training may also have positive effects on respiratory function in this population as the act of singing places significant demands on the respiratory system. In particular, singing requires
strong and fast inspirations, extended, regulated expirations, andrecruitment of accessory respiratory muscles. Therapeutic singing
training was thus considered to constitute a form of RMT in thisreview.

Description of the condition

How the intervention might work

Respiratory dysfunction post SCI is characterised by weak or paralysed respiratory muscles, resulting in reduced lung volume, ineffective cough, increased respiratory tract infections, reduced chestwall compliance, and an increased oxygen cost of breathing (Brown

For RMT to produce a significant effect, vigorous and forceful efforts within an intensive training regimen are usually needed. Research suggests that people with quadriplegia use accessory respiratory muscles (sternocleidomastoid for inspiration and pectoralis

Respiratory dysfunction resulting from SCI remains a major causeof morbidity, mortality, and economic burden (van den Berg2010). It is the most common cause of death following SCI andcontributes to higher mortality rates for people with SCI than thegeneral population (DeVivo 1999). Alterations in the mechanical properties of the lungs and chest wall (particularly for people
with cervical SCIs) results in paradoxical (out of phase) movementof the chest wall, and reduced lung and chest wall compliance(flexibility). This, in turn, leads to reduced breathing efficiency,
reduced maximal static respiratory pressures, and reduced lungvolumes. Impairment of the muscles of inspiration reduces vital
capacity (VC), prevents deep breaths, and may lead to dyspnoea
with exertion or collapse of the lungs (atelectasis), or both dyspnoea and collapse of the lungs (Cardozo 2007). Dysfunctional
expiratory muscles impair cough and secretion clearance, increase
airways resistance, and increase the susceptibility to and persistence of lower respiratory tract infections (Brown 2006). Totallung capacity (TLC) is usually reduced following SCI (due to impaired inspiratory musculature) and residual volume is relatively
increased (due to impaired expiratory musculature and subsequent
reduced expiratory reserve volume) (Liaw 2000). VC is the difference between TLC and residual volume and is, therefore, reduced
following SCI.

Respiratory muscle training for cervical spinal cord injury (Review)
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major and latissimus dorsi for expiration) to improve performance
during maximal effort tasks (Fujiwara 1999), and that the strengthof these muscles improves with training (Estenne 1989).
The primary mechanisms that influence change of muscle strength
during the first four weeks of training are neural adaptations, suchas increased motor unit recruitment and synchronisation, and enhanced inter- and intra-muscle co-ordination (Sale 1988). These
neural adaptations occur as a result of the ability of the central nervous system to respond to changes in functional demands. Training of other mechanisms beyond four weeks, such as peripheral or
structural changes, may be responsible for further improvements
in strength.

METHODS

Criteria for considering studies for this review

Types of studies
We considered all randomised controlled trials (RCT) for inclusion.

Types of participants

Why it is important to do this review
Respiratory complications are prevalent following SCI due to
weakness of the respiratory muscles. It seems feasible that thesemuscles could be trained to increase in strength or endurance, orboth. This review is needed to determine whether such trainingof the respiratory muscles is effective for people with cervical SCI,
and if so, what are the best training techniques and methods toachieve improvements in respiratory function.
Previously, Brooks 2005, Sheel 2008, and Van Houtte 2006 attempted to review research systematically to evaluate the effectof RMT in people with SCI on respiratory muscle strength,
endurance, and pulmonary function. These reviews focused onparticular types of training, that is, inspiratory muscle training(Brooks 2005; Sheel 2008) and exercise training (Sheel 2008), andused different inclusion criteria, that is, randomised versus nonrandomised designs (Brooks 2005). The three reviews reported
that the included studies were too variable in terms of research
design, participant characteristics, training techniques used, andoutcomes measured, thus results could not be pooled for metaanalysis. Van Houtte 2006 concluded that RMT following SCI
tended to improve expiratory muscle strength and VC, and decrease residual volume. However, Sheel 2008 excluded expiratory
muscle training but reported some evidence for the efficacy of inspiratory muscle training and exercise training.
We believe that a systematic review of all types of RMT is neededin order to synthesise these disparate findings for people livingwith SCI, clinicians, and clinical researchers working in this area.
First, the review will aim to establish the effect of any form of
RMT on respiratory function for people with cervical SCI, andsecond, it will aim to provide methodological recommendations
for future clinical research in this area.

We included studies involving people with any level of acquired
cervical SCI, both acute and chronic. We excluded studies of
RMT for people with inherited or congenital neuromuscular disorders, such as muscular dystrophies, congenital and acquired myopathies, and spinal muscular atrophy. We also excluded studies
that investigated the effect of RMT on respiratory disorders notcaused by SCI (such as chronic obstructive pulmonary disease andasthma).

Types of interventions
We considered trials for inclusion if the trial author(s) described
an intervention as RMT and compared it with a control groupusing an alternative intervention, placebo, usual care, or no intervention. RMT may involve inspiratory or expiratory muscle
training (including normocapnic hyperpnoea training and singing
training), or both.

Types of outcome measures
We conducted a survey of 20 people with cervical SCI to identify
their needs and determine outcome measures that were patient-focused. Consequently, the primary outcomes included respiratorycomplications, dyspnoea, and VC. Respiratory complications aredefined clinically as when a person sought medical attention for a
respiratory symptom and this was ’confirmed clinically’ as a respiratory complication by objective data as decided by a physician.
This is the definition of respiratory complications employed by
Van Houtte 2008 and uses the GOLD criteria for acute exacerbations (Rodriguez-Roisin 2009). Secondary outcomes included
measures of respiratory muscle strength (maximal inspiratory pressure (MIP), maximal expiratory pressure (MEP)), forced expiratory volume in one second (FEV1 ), and quality of life.

Primary outcomes

OBJECTIVES
To assess the effects of RMT on function for people with cervical
SCI.

1. Respiratory complications
2. Dyspnoea
3. VC

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Secondary outcomes

1. MIP
2. MEP
3. FEV1
4. Quality of life

When a title or abstract could not be rejected with certainty, both
review authors obtained the full-text article and independently
inspected the article.
Both review authors used an inclusion criteria form to assess thetrial’s eligibility for inclusion. Review authors reported and resolved disagreements by discussion. We noted the reasons for excluding studies.

Search methods for identification of studies
We did not restrict searches by date, language, or publication status.
Electronic searches
The Cochrane Injuries Group Trials Search Co-ordinator searched
the following:
1. Cochrane Injuries Group’s Specialised Register (6 March2013);
2. CENTRAL (Issue 2, 2013);
3. MEDLINE (Ovid SP) (1946 to February week 3 2013);
4. PubMed (6 March 2013);
5. EMBASE Classic + EMBASE (Ovid SP) (1947 to 5 March2013);
6. CINAHL Plus (EBSCO) (1937 to 6 March 2013);
7. ISI Web of Science: Science Citation Index Expanded (SCIEXPANDED) (1970 to 6 March 2013);
8. ISI Web of Science: Conference Proceedings Citation
Index-Science (CPCI-S) (1990 to 6 March 2013).
Appendix 1 lists the search strategies used. Due to the paucity oftrials in this area, we did not restrict our search by using a filter for
RCTs but sought to identify all types of trials in order to identify
those that we may have otherwise missed.
Searching other resources
We also searched the following trials registries:
1. Australian New Zealand Clinical Trials Registry (www.anzctr.org.au/trialSearch.aspx) (8 March 2013);
2. ClinicalTrials (www.clinicaltrials.gov) (8 March 2013);
3. Controlled Trials metaRegister (www.controlled-trials.com)(8 March 2013).
We sought further, potentially relevant, published and unpublished studies by checking reference lists of relevant papers andliterature reviews. We communicated with trial authors to identify
ongoing studies.

Data collection and analysis
Selection of studies
One review author (JT) scanned titles and abstracts of each record
retrieved by the search and rejected obviously irrelevant references.

Data extraction and management
Both review authors independently extracted data using a data collection form (based on recommendations in the Cochrane Handbook for Systematic Reviews of Interventions) (Higgins 2011) andassessed the methodological quality of the selected articles. We
resolved disagreement by discussion. Whenever possible, we contacted the author of each included trial to verify the accuracy ofthe data and, if possible, to obtain further data or information.
One review author (JT) entered all trials included in this systematic review into Review Manager 5 (RevMan 2011). Both review
authors independently conducted data analysis.
Assessment of risk of bias in included studies
We used The Cochrane Collaboration’s tool for assessing risk ofbias (Higgins 2011). This tool assesses the following domains: sequence generation, allocation concealment, blinding, incomplete
outcome data, selective outcome reporting, and other sources ofbias. On each domain, the review authors made a judgement of
low risk of bias (’Yes’), high risk of bias (’No’), or unclear risk ofbias (’Unclear’). Both review authors independently assessed trial
quality and agreement between review authors was measured.
We assessed risk of bias in these domains as follows:
Sequence generation of the randomisation process• Yes: using random-number tables, computer random
number generation, coin tossing, shuffling cards or envelopes,
throwing dice, drawing of lots, or minimisation.
• No: sequence generation described, but is not one of therandomisation methods under ’Yes’ above.
• Unclear: insufficient information about the sequence
generation process to permit judgement of ’Yes’ or ’No’.
Adequacy of allocation concealment• Yes: allocation concealment was described, and would notallow either investigators or participants to know or influence
treatment group assignment at the time of study entry.
Acceptable methods included central allocation or sequentiallynumbered, opaque, sealed envelopes.
• No: the method of allocation was not concealed (e.g.
alternating participants, odd-even day) or one in which theinvestigators or participants could have been aware of allocation
prior to study commencement.
• Unclear: trial either did not describe the method of
allocation concealment, or reported an approach that was notclearly adequate.

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Blinding of outcome assessors• Yes: blinding of outcome assessors was clearly maintained.
• No: outcome assessors were not blinded to treatment groupassignment, or the blinding was incomplete.
• Unclear: insufficient information to permit judgement of’Yes’ or ’No’.

were reported. Where data were missing, we attempted to contact
the author(s) of the trial to obtain the missing data. We analysed
only the available data (without imputing missing data).

Intention-to-treat (ITT) analysis• Yes: specifically reported by the authors that ITT analysis
was undertaken, or report that makes it unmistakable that ITT
was undertaken, for the primary analysis.
• No: lack of ITT was confirmed on study assessment.
• Unclear: ITT analysis was mentioned, but it is uncertainfrom the report whether this was fully carried out.

We calculated pooled estimates of treatment effect differences using the fixed-effect model (unless there was substantial heterogeneity) and calculated 95% CI for each effect size estimate. Levels ofheterogeneity were determined using the I2 statistic (I2 greater than
50% was considered substantial heterogeneity) (Higgins 2011).
If we found that heterogeneity was present, we used the randomeffects model for the meta-analysis and explored and presented
possible causes for the heterogeneity. We also used visual inspection of the forest plots to assess heterogeneity.

Completeness of outcome data
• Yes: no missing outcome data, reason for missing data
unlikely to be related to true outcome, or missing data imputed
using appropriate methods.
• No: reason for missing outcome data likely to be related totrue outcome, with either imbalance in numbers or reasons formissing data across intervention groups, or potentiallyinappropriate application of simple imputation.
• Unclear: insufficient reporting of attrition/exclusions topermit judgement of ’Yes’ or ’No’ (e.g. number randomised notstated, no reasons for missing data provided).
Selectiveness of outcome reporting• Yes: the study protocol was available and all of the study’sprespecified (primary and secondary) outcomes that are ofinterest in the review have been reported in the prespecified way;or the study protocol is not available but it is clear that the
published reports included all expected outcomes, including
those that were prespecified (convincing text of this nature may
be uncommon).
• No: not all of the study’s prespecified primary outcomes
were reported, one or more reported primary outcomes were notprespecified, or were reported incompletely so that they could
not be included in a meta-analysis.
• Unclear: insufficient information to permit judgement of’Yes’ or ’No’. It is likely that the majority of studies will fall into
this category.

Assessment of heterogeneity

Assessment of reporting biases
We created funnel plots to explore possible publication bias.

Data synthesis
For continuous variables, we calculated MD and 95% CIs for eachstudy. We pooled all similar studies using MD and 95% CIs.

Subgroup analysis and investigation of heterogeneity
Due to the anticipated small number of trials available for systematic review, we planned only one a priori subgroup analysis, which
was for acute (less than one year) versus chronic cervical SCI participants. We conducted dose-response analyses where possible todetermine any relationship between treatment intensity or duration and an intervention effect.

Sensitivity analysis
We performed sensitivity analyses based on the methodologicalquality of the included studies. The analyses examined the effectof excluding studies that either failed to report or did not include
evidence of concealed allocation, blinding of outcome assessments,
and analyses performed on an ITT basis.

Measures of treatment effectWe anticipated that all outcomes measured in this review would
be continuous variables. Thus, we calculated standardised meandifferences (SMD) with 95 confidence intervals (CI) for outcome
measures using the results from different scales and mean differences (MD) for results using the same scales.

RESULTS

Dealing with missing data

Description of studies

We considered an ITT analysis adequate when the numbers ofpeople who dropped out and the reasons why they dropped out

See: Characteristics of included studies; Characteristics of excluded
studies.

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Results of the search
The database searches identified 843 citations. After duplicatesand animal studies were removed, 747 citations remained. We
screened the abstracts of these 747 citations and retrieved 40 fulltext references for possible inclusion based on titles and abstracts.
In several cases, we contacted chief investigators to obtain additional information on study details and data. We examined thereference lists of these 40 papers for possible additional studies toinclude. This generated a further six studies. Three of the 40 studies were not written in English. A native speaker of the languagethat the paper was written in screened these three studies against
the inclusion criteria. As none of these met the inclusion criteria,
we deemed that full-text translations were unnecessary.
Following full-text review of the remaining 37 studies, we excluded a further 25 studies. Reasons for exclusion are detailed in
the Characteristics of excluded studies table. Initial disagreement
between authors occurred with three studies and this was resolved
through discussion and consensus. Twelve publications of 11 studies met all the inclusion criteria and were included in the review.
Figure 1 shows a study flow diagram.

Respiratory muscle training for cervical spinal cord injury (Review)
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Figure 1. Flow diagram.

Respiratory muscle training for cervical spinal cord injury (Review)
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Included studies
We included 11 studies with 212 participants in this review. Thesestudies examined the effects of RMT on physiological and psychological outcomes in people with cervical SCI. The majority of participants were male (82%). Four studies were from the
USA (Derrickson 1992; Litchke 2008; Litchke 2010; Roth 2010),
with one each from Canada (Loveridge 1989), Australia (Tamplin
2013), Belgium (Van Houtte 2008), Switzerland (Mueller 2013),
Taiwan (Liaw 2000), Slovenia (Zupan 1997), and South Africa(Gounden 1990). Not all studies measured every outcome identified for this review. Two studies utilised a three-way comparison
between two different RMT interventions and control condition(Litchke 2010; Mueller 2013). To enable both training interventions to be included in the meta-analysis, these have been listed
as Mueller 2013 (A) and (B) and Litchke 2010 (A) and (B) in thedata analysis. Completed details of all included studies are provided in the Characteristics of included studies table. Below is abrief summary of the 11 included studies.

DesignAll studies had an RCT design. One study had a cross-over design(Zupan 1997), and in the remaining 10 studies there were four
comparisons between RMT and an alternative intervention andseven comparisons between RMT and a control condition (threesham treatments and four ’usual care’). Studies were conducted in
hospital (N = 6) and community (N = 4) settings (and one study
recruited from both). Sample sizes ranged from nine to 40 participants with injury levels ranging from C4 to C8. Two studies also
included participants with thoracic level injuries (Roth 2010; Van
Houtte 2008) and two with non-traumatic SCI (Litchke 2008;
Litchke 2010). Testing position was not consistent across the included studies. Two studies tested participants in the supine position (Derrickson 1992; Liaw 2000), six studies tested participants
when sitting upright (Litchke 2008; Litchke 2010; Mueller 2013;
Roth 2010; Tamplin 2013; Van Houtte 2008), two studies tested
in both positions (Gounden 1990; Zupan 1997), and testing position was not able to be determined for one study (Loveridge1989) (see Table 1). Testing with an abdominal binder has beenreported to deliver a similar result as testing in the supine position
for people with cervical SCI (Estenne 1987). Of the six studies
that tested participants in a seated position, only two confirmedthat an abdominal binder was not used (Mueller 2013; Tamplin
2013).

Interventions

Two of the included studies compared two RMT interventions
with a control condition (Litchke 2010; Mueller 2013). Mueller
2013 compared inspiratory resistance training and isocapnic hyperpnoea training versus a placebo condition (incentive spirometry). To enable clear comparison of interventions, the inspiratory
resistance training comparison is referred to as Mueller 2013 (A)and the isocapnic hyperpnoea comparison is referred to as Mueller
2013 (B). Litchke 2010 compared concurrent flow resistance training and concurrent pressure threshold resistance training to a usual
care control condition. The concurrent flow resistance training
comparison is thus referred to as Litchke 2010 (A) and concurrent pressure threshold resistance training as Litchke 2010 (B).
Five studies used an inspiratory muscle resistance training intervention (Derrickson 1992; Liaw 2000; Loveridge 1989; Mueller
2013 (A); Zupan 1997) and three studies used an expiratory muscle resistance training intervention (Gounden 1990; Roth 2010;
Zupan 1997). In these studies, resistive muscle training devices
were used. Five studies used an intervention described as simultaneous training of both inspiratory and expiratory muscle function(Litchke 2008; Litchke 2010; Mueller 2013 (B); Tamplin 2013;
Van Houtte 2008). Van Houtte 2008 and Mueller 2013 (B) usednormocapnic or isocapnic hyperpnoea and Tamplin 2013 usedsinging training. Training intensity ranged from 10 to 60 minutes per day, three to seven days per week, and the training length
ranged from four to 12 weeks (mean eight weeks).
We could not pool the data of two studies with the other studies
because outcomes were presented as percentages of predicted normal values rather than raw scores (Loveridge 1989; Zupan 1997).
In addition, there were no common outcomes between these twostudies that could enable comparison of percentage of predictedscores. We were unable to contact the authors of these studies toobtain raw data. Thus, we only included the data from these studies in narrative form in this review.
Excluded studies
We excluded 25 studies because they were not RCTs. Of these
25 studies, three did not use a RMT intervention, and three did
not recruit only participants with cervical SCI. The reasons for
exclusion are listed in the Characteristics of excluded studies table.

Risk of bias in included studies
Figure 2 and Figure 3 show a summary of risk of bias judgements
for all included studies. Risk of bias is detailed for each study inthe risk of bias tables included with the Characteristics of included
studies table.

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Figure 2. Risk of bias graph: review authors’ judgements about each risk of bias item presented aspercentages across all included studies.

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Figure 3. Risk of bias summary: review authors’ judgements about each risk of bias item for each included
study.

Respiratory muscle training for cervical spinal cord injury (Review)
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Allocation
Only two studies (18%) described adequate allocation concealment (Tamplin 2013; Van Houtte 2008).

Respiratory complications

Only one study reported on respiratory complications that occurred during the trial (Van Houtte 2008). In this study, 14
episodes of respiratory complications were reported for the control
group and one episode for the RMT group.

Blinding
Only four studies (36%) described blinding of participants andassessors (Mueller 2013; Roth 2010; Tamplin 2013; Van Houtte2008).

Dyspnoea

We classified six of the included studies (55%) as having a highrisk of incomplete outcome data (Derrickson 1992; Liaw 2000;
Litchke 2008; Litchke 2010; Mueller 2013; Roth 2010). This risk
was attributable to a failure to report outcome data for participants
who were recruited but did not complete the study. The dropout
rate was 0% for five of the trials and between 8% and 73% for theremaining six trials.

Three studies reported dyspnoea outcomes (Liaw 2000; Mueller
2013; Van Houtte 2008). Two studies used different versions of
the Borg scale (the original Borg scale has 15 points whereas themodified has only 10 points) (Liaw 2000; Van Houtte 2008),
and one study used a 10-point visual analogue scale (Mueller2013). Thus, we used SMDs to compare dyspnoea outcomes. On
each scale, a higher score equated to worse dyspnoea. The pooled
estimate of the four data sets from these three studies found no
significant effect of RMT on reported dyspnoea (SMD -0.10, 95%
CI -1.65 to 1.44, P value = 0.89). A random-effects model wasapplied due to the high level of heterogeneity between the threestudies (I2 = 81%) (Analysis 1.1).

Selective reporting

Vital capacity

We classified only one study (9%) as selectively reporting results(Gounden 1990). In this study, MIP was measured at baseline,
but no post assessment measures of MIP were presented.

The pooled estimate of four studies examining five data sets (Gounden 1990; Liaw 2000; Mueller 2013 (A); Mueller 2013 (B);
Tamplin 2013) indicated that RMT significantly increased VC(MD mean end point 0.4 L, 95% CI 0.12 to 0.69, P value = 0.006;
I2 = 0%) (Analysis 1.2). In the included studies, the mean control
VC ranged from 1.4 to 2.7 L. As such, an improvement of 0.40 L
represents approximately a 15% to 30% improvement.

Incomplete outcome data

Other potential sources of bias
We identified no other potential sources of bias.

Effects of interventions
See: Summary of findings for the main comparison Respiratory
muscle training compared with control for cervical spinal cord
injurySee: Summary of findings for the main comparison for the main
comparison of RMT versus control.

Primary outcomes
Although most outcomes were reported using the same measuresor scales, most studies did not provide change score standard deviations. Thus, we conducted the meta-analysis using mean post-testscores for control and intervention groups. Although this meantthat we could not account for baseline scores between groups andbetween studies, random allocation should account for any baseline differences.

Secondary outcomes

Maximal inspiratory pressure

MIP was measured in nine trials (11 data sets; Derrickson 1992;
Liaw 2000; Litchke 2008; Litchke 2010 (A); Litchke 2010 (B);
Loveridge 1989; Mueller 2013 (A); Mueller 2013 (B); Roth 2010;
Tamplin 2013; Van Houtte 2008). All respiratory pressures are
expressed as absolute values (e.g. MIP is positive not negative).
As discussed previously, the data from Loveridge 1989 could not
be included in the meta-analysis because raw scores were not presented. The pooled estimate of the 11 data sets included in themeta-analysis indicated a significant effect of RMT on MIP (MDmean end point 10.66 cm/H2 O, 95% CI 3.59 to 17.72, P value= 0.003; I2 = 0%) (Analysis 1.3). In the included studies, themean control MIP ranged from 43 to -102 cm/H2 O. As such,an improvement of 10 cm/H2 O represents approximately a 10%

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to 25% improvement. The Derrickson 1992 study used anotherform of inspiratory muscle training (abdominal weights training)as a control condition rather than standard care, no intervention,or sham training. As such, this could represent a potential bias
for the meta-analysis. A post-hoc sensitivity analysis excluding thedata from this study did not significantly alter the result (MDmean end point 9.47 cm/H2 O, 95% CI 8.28 to 59.72, P value= 0.02; I2 = 6%). Loveridge 1989 also reported greater improvements in MIP for the RMT group versus control; however, these
improvements did not achieve statistical significance.

Maximal expiratory pressure

Six studies (seven data sets) examined the effect of RMT on MEP(Gounden 1990; Liaw 2000; Mueller 2013 (A); Mueller 2013
(B); Roth 2010; Tamplin 2013; Van Houtte 2008). The pooled
estimate of these studies indicated a significant intervention effect(MD mean end point 10.31 cm/H2 O, 95% CI 2.80 to 17.82, P
value = 0.007; I2 = 42%). In the included studies, the mean control
MEP ranged from 41 to 91 cm/H2 O. As such, an improvementof 10 cm/H2 O represents approximately a 10% to 25% improvement.

Forced expiratory volume in one second

The pooled estimate of four studies examining FEV1 indicated nostrong effect of RMT (MD mean end point 0.05 L, 95% CI 0.23 to 0.34, P value = 0.70; I2 = 0%) (five data sets: Liaw 2000;
Mueller 2013 (A); Mueller 2013 (B); Roth 2010; Tamplin 2013).

Quality of life

Quality of life outcomes were reported for four studies (Litchke
2010; Mueller 2013; Tamplin 2013; Van Houtte 2008). However, different instruments were used for each of these studies.
Litchke 2010 found that RMT improved some aspects of healthrelated quality of life for wheelchair rugby athletes with cervical
SCI. Specifically, they found perceived increases on the vitality
domain of the SF-36v2 and decreases on the bodily pain domain.
We found no significant differences for the remaining six domains:
physical functioning, role physical, role emotional, social functioning, general mental health, and general health perceptions.
Mueller 2013 found no statistically significant changes in quality of life outcomes after inspiratory resistance training comparedwith sham training; however, they demonstrated high positive effect sizes for the physical component of the generic SF-12 assessment (but not for the mental component). Tamplin 2013 foundno significant changes in quality of life as measured by the generic
Assessment of Quality of Life tool following a therapeutic singing
intervention. Van Houtte 2008 found a significant improvement
in disorder-specific Index of Pulmonary Dysfunction for the experimental group (P value = 0.03). It was not possible to conduct

a meta-analysis of the quality of life outcome data because of thediversity of instruments and subscales used between studies.

Sensitivity analyses

We conducted sensitivity analyses based on the methodologicalquality of the included studies. The analyses examined the effectof excluding studies that either did not report or did not include
evidence of concealed allocation, blinding of outcome assessments,
and analyses performed on an ITT basis. In some cases, this meantthat we removed all but one study from the analysis and, therefore,
meta-analysis was impossible. After removing the two studies witha high risk of attrition bias (Liaw 2000; Roth 2010), a stronger
effect was found for both MIP (MD mean end point 14.17 cm/
H2 O, 95% CI 5.85 to 22.49, P value = 0.0008) and MEP (MDmean end point 17.35 cm/H2 O, 95% CI 7.42 to 27.27, P value= 0.0006).

Subgroup analyses

We conducted subgroup analyses only on outcomes that had datafrom more than three trials (MIP and MEP). When we included
studies with only acute (less than one year) participants in theanalysis (Derrickson 1992; Liaw 2000; Mueller 2013 (A); Mueller
2013(B); Roth 2010; Van Houtte 2008), the effect on MIP wasminimal but the studies were more heterogeneous (MD mean end
point 9.99 cm/H2 O, 95% CI 1.79 to 18.28, P value = 0.02; I2= 43%). There was no significant effect on MEP for studies with
only acute participants (MD mean end point 5.95 cm/H2 O, 95%
CI -3.39 to 15.28, P value = 0.21; I2 = 33%).
It was difficult to conduct dose-response analyses due to the small
number of studies in the meta-analysis for each outcome. We
confirmed no relationship between treatment intensity and anintervention effect. We conducted subgroup analyses on MIP and
MEP outcomes to determine any relationship between treatment
duration (greater than eight weeks) and an intervention effect.
When we included only studies with a duration of less than eightweeks in the meta-analysis of MIP and MEP, there was no longer asignificant effect of RMT. However, this is probably because only
two or three studies were included (Derrickson 1992; Liaw 2000;
Roth 2010), thus increasing heterogeneity.

DISCUSSION
The results of the meta-analyses indicate that RMT may increase
VC and maximal respiratory pressures (MIP and MEP) for people
with cervical SCI. The findings overall are conservative due to thesmall number of included studies in the meta-analysis (N = 9),
and the small sample sizes in these studies (n = nine to 40). The
inability to use change scores makes the meta-analyses sensitive
to baseline differences. Although in theory, randomisation should

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adequately deal with baseline differences, it may not when there
are so few studies with small sample sizes. In addition, the measures
themselves are variable. There was a high co-efficient of variation
for MIP, MEP, and VC in the able-bodied and even more so in thecervical SCI population with a range of injury levels and severity (ATS/ERS 2002; ATS/ERS 2005). This increased ’measurespecific’ variability and the consequent larger standard deviationof summary effect estimates reduced the power of smaller studies
to find statistically significant treatment effects. Further, the inclusion of a range of different training mechanisms in this review
should be acknowledged. Subgroup analyses according to training
type were not feasible due to the small number of included studies.
Despite these limitations, the current meta-analysis revealed a significant treatment effect for these outcomes (MIP, MEP, and VC),
suggesting that training improves measures of respiratory function
after cervical SCI.

Summary of main results
The meta-analyses indicated an effect of RMT on VC and respiratory muscle strength (MIP and MEP). However, the small
number of studies (with limited sample sizes) (Gounden 1990;
Liaw 2000; Mueller 2013; Tamplin 2013), that reported VC data
warrant cautious interpretation of the findings in this variable andfurther research is needed. The respiratory muscle strength (MIPand MEP) results are more reliable due to the greater number ofincluded studies reporting these outcomes. The meta-analysis did
not provide evidence for the effect of RMT on FEV1 (P value =0.69).
Of the two studies assessing dyspnoea that could be combined
for the meta-analysis, one found an SMD favouring the intervention group (Van Houtte 2008), and the other found no difference between groups (Liaw 2000). However, the raw data fromthe Van Houtte 2008 study indicated minimal change in dyspnoea scores over time for either group, whereas the data from theLiaw 2000 study indicated a significant difference between groups
in improvement on dyspnoea scores. Mueller 2013 found a higheffect size on dyspnoea following isocapnic hyperpnoea training.
Mueller 2013 also found an improvement in quality of life as measured by the physical component of the SF-12, and Van Houtte
2008 found a significant improvement on the Index of Pulmonary
Dysfunction for the experimental group (P value = 0.03). Litchke
2010 found increases in vitality and decreases in bodily pain. In
contrast, Tamplin 2013 observed no significant changes in qualityof life by using the Assessment of Quality of Life. The study that
captured data on respiratory complications (Van Houtte 2008),
reported a much lower incidence of respiratory complications in
the group that received RMT in comparison to a control group.
The limited number of studies with small sample sizes makes it
difficult to draw any strong conclusions about the effect of RMTon these more functional outcomes (dyspnoea, quality of life, andrespiratory complications).

Overall completeness and applicability ofevidence
This review included 11 studies with 212 participants. In addition, we checked reference lists of relevant papers and literature
reviews. We contacted trial authors to request additional data andstudy information where necessary. Overall, the quality of reporting risk of bias was poor. Only four studies reported the methodof randomisation (Derrickson 1992; Mueller 2013; Roth 2010;
Tamplin 2013), and four studies provided details regarding allocation concealment or blinding, or both (Mueller 2013; Roth 2010;
Tamplin 2013; Van Houtte 2008). We had to contact most study
authors to gain additional methodological and statistical information.
It is important to note that we deliberately included a number ofdifferent types of RMT in this review. These included: inspiratory
muscle training, expiratory muscle training, and techniques thattrained both expiratory and inspiratory muscles, including isocapnic hyperpnoea and therapeutic singing. In addition, the ’control’
conditions to which these interventions were compared included:
no training, usual care, sham training, and alternate interventions.
Interestingly, the Mueller 2013 study data have provided support
for their hypothesis that low training volumes at higher intensities can improve respiratory muscle strength. Further research isneeded on this type of RMT as it has great potential to affect motivation and training compliance positively.

Quality of the evidence
All included studies explicitly stated that randomisation was used,
but allocation concealment was unclear in eight of the 11 studies and blinding was unclear in seven studies. Further, six of the
included studies had a high risk of attrition bias. We conducted
sensitivity analyses to determine the effect when these high-riskstudies were excluded. We found a stronger effect for MIP and
MEP as a result of these sensitivity analyses.

Potential biases in the review process
Lack of available data on the standard deviations of the change
scores made it difficult to account for baseline differences. Thismay have altered the estimate of the overall effect size for theintervention.
In cervical SCI, respiratory function measures may be substantiallyaffected by both the position in which the tests are performed andthe presence or not of an abdominal binder. For example, an increase in VC is observed in cervical SCI when changing from theseated to the supine posture. This is the opposite to that which isobserved in able-bodied people and, moreover, this postural dependence can be ameliorated when the abdomen is tightly supported by elastic straps or a binder (Hart 2005). The positionin which respiratory function and strength was measured varied

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across the 11 studies and while likely, it was uncertain whether
testing position and abdominal binder use was standardised withineach study (Table 1). Data for meta-analysis was restricted to end
scores (rather than change) and, as such, there was a risk of bias
attributable to position in the estimates of the magnitude of treatment effects that may not have been accounted for in our analyses.
Sensitivity analyses examining position were not selected a priori
in this review and are also not reported due to an insufficient number of studies per outcome.

(maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP)) for people with cervical spinal cord injury (SCI).
However, the effect size for all three outcomes was small and there
was no evidence of carryover beyond the training period. It is interesting that despite the significant and often reported effect of
respiratory dysfunction on health-related quality of life for people
with cervical SCI, few studies have examined the effect of RMT on
functional outcomes such as dyspnoea, cough efficacy, respiratorycomplications, hospital admissions, or quality of life.

Implications for research
Agreements and disagreements with otherstudies or reviews
Similar to reports from previous reviews (Brooks 2005; Sheel 2008;
Van Houtte 2006), this review provided no conclusive findings
for a number of reasons. Although this topic of RMT has received
considerable interest in the research literature, few publications
met the standards of methodological rigour for inclusion in thisreview. Furthermore, the small number of studies that were included were heterogeneous in terms of research design, participantcharacteristics, training techniques, and comparison conditions
used. The systematic review by Van Houtte 2006 found trends
towards improvement following RMT on VC and MEP (whichwere supported by this Cochrane review), but insufficient support
for the effect of MIP, quality of life, and respiratory complications
in SCI. The systematic review by Sheel 2008 indicated some evidence that inspiratory muscle training could improve respiratory
function and decrease dyspnoea. The current review provides further support for the effect of RMT on respiratory function (MIP,
MEP, and VC).

AUTHORS’ CONCLUSIONS

More large-scale studies are needed to examine the effect of RMTon respiratory and quality of life outcomes for people with cervical SCI further. In particular, the effects of RMT on dyspnoea,
incidence of respiratory complications, and quality of life were
not often reported and need to be assessed in future studies. Also,
the effect of RMT on standard respiratory function outcomes also
needs further study as results of our meta-analysis are currently
conservative. In addition, more studies are needed to ascertain adosage effect and longer-term follow-up studies will assist in determining any carryover effects of training. Without long-term
studies, it is impossible to determine effects of RMT on quality oflife, respiratory morbidity, and mortality.

ACKNOWLEDGEMENTS
The authors would like to thank the following people for valuable
help with the translation of trial reports:• Dr Charlotta Karner, systematic reviewer, Cochrane
Airways Group;

Implications for practice• Prof Ian Roberts, Professor of Epidemiology & Public
Health, Cochrane Injuries Group;

The results of this review suggest that respiratory muscle training(RMT) can improve vital capacity and respiratory muscle strength• Dr Vasiliy V. Vlassov, President, Society for Evidence Based
Medicine, Russia.

REFERENCES

References to studies included in this review
Derrickson 1992 {published data only}
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Litchke L, Lloyd L, Schmidt E, Russian C, Reardon R.
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Fugl-Meyer AR. Respiratory function and training intraumatic spinal cord injuries. Lakartidningen 1972;69(25):3038–40.
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Gross 1980 {published data only}
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Hornstein 1986 {published data only}
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Lin 1999 {published data only}
Lin KH, Chuang CC, Wu HD, Chang CW, Kou, YR.
Abdominal weight and inspiratory resistance: their
immediate effects on inspiratory muscle functions during
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Lin VW, Hsiao I N, Zhu E, Perkash I. Functional magnetic
stimulation for conditioning of expiratory muscles inpatients with spinal cord injury. Archives of Physical Medicine& Rehabilitation 2001;82(2):162–6.
Metcalf 1966 {published data only}
Metcalf VA. Vital capacity and glossopharyngeal breathingin traumatic quadriplegia. Physical Therapy 1966;46(8):835–8.
Moreno 2012 {published data only}
Moreno MA, Zamuner AR, Paris, JV, Teodori RM, Barros
RM. Effects of wheelchair sports on respiratory muscle
strength and thoracic mobility of individuals with spinal
cord injury. American Journal of Physical Medicine &Rehabilitation 2012;91(6):470–7.
Moreno 2013 {published data only}
Moreno MA, Paris JV, Sarro KJ, Lodovico A, Silvatti
AP, Barros RML. Wheelchair rugby improves pulmonary
function in people with tetraplegia after 1 year of training.
Journal of Strength and Conditioning Research 2013;27(1):50–6.
Nygren-Bonnier 2009 {published data only}
Nygren-Bonnier M, Wahman K, Lindholm P, Markstrom
A, Westgren N, Klefbeck B. Glossopharyngeal pistoning forlung insufflation in patients with cervical spinal cord injury.
Spinal Cord 2009;47(5):418–22.
Rutchik 1998 {published data only}
Rutchik A, Weissman AR, Almenoff PL, Spungen AM,
Bauman WA, Grimm DR. Resistive inspiratory muscle
training in subjects with chronic cervical spinal cord injury.
Archives of Physical Medicine & Rehabilitation 1998;79(3):293–7.
Sapienza 2006 {published data only}
Sapienza CM, Wheeler K. Respiratory muscle strength
training: functional outcomes versus plasticity. Seminars in
Speech & Language 2006;27(4):236–44.
Sutbeyaz 2005 {published data only}
Sutbeyaz ST, Koseoglu BF, Gokkaya NKO. The combined
effects of controlled breathing techniques and ventilatory
and upper extremity muscle exercise on cardiopulmonary
responses in patients with spinal cord injury. International
Journal of Rehabilitation Research 2005;28(3):273–6.
Uijl 1999 {published data only}
Uijl SG, Houtman S, Folgering HT, Hopman MT. Trainingof the respiratory muscles in individuals with tetraplegia.
Spinal Cord 1999;37(8):575–9.
Valent 2009 {published data only}
Valent LJ, Dallmeijer AJ, Houdijk H, Slootman HJ, Janssen
TW, Post MW, et al.Effects of hand cycle training on

physical capacity in individuals with tetraplegia: a clinical
trial. Physical Therapy 2009;89(10):1051–60.
Walker 1987 {published data only}
Walker J, Cooney M. Improved respiratory function inquadriplegics after pulmonary therapy and arm ergometry.
New England Journal of Medicine 1987;316(8):486–7.
Wang 2002 {published data only}
Wang T-G, Wang Y-H, Tang F-T, Lin K-H, Lien IN.
Resistive inspiratory muscle training in sleep-disorderedbreathing of traumatic tetraplegia. Archives of Physical
Medicine & Rehabilitation 2002;83(4):491–6.

Additional references
ATS/ERS 2002
American Thoracic Society/European Respiratory Society.
ATS/ERS statement on respiratory muscle testing. American
Journal of Respiratory and Critical Care Medicine 2002;166:518–624.
ATS/ERS 2005
American Thoracic Society/European Respiratory Society.
ATS/ERS Taskforce: Standardization of spirometry.
European Respiratory Journal 2005;26:319–38.
Brooks 2005
Brooks D, O’Brien K, Geddes EL, Crowe J, Reid D. Is
inspiratory muscle training effective for individuals withcervical spinal cord injury? A qualitative systematic review.
Clinical Rehabilitation 2005; Vol. 19, issue 3:237–46.
Brown 2006
Brown R, DiMarco AF, Hoit JD, Garshick E. Respiratory
dysfunction and management in spinal cord injury.
Respiratory Care 2006; Vol. 52, issue 8:853–68.
Cardozo 2007
Cardozo CP. Respiratory complications of spinal cord
injury. Journal of Spinal Cord Medicine 2007; Vol. 30,
issue 4:307–8.
Chen 1990
Chen CF, Lien IN, Wu MC. Respiratory function inpatients with spinal cord injuries: effects of posture.
Paraplegia 1990; Vol. 28, issue 2:81–6.
DeVivo 1999
DeVivo MJ, Krause S, Lammertse DP. Recent trends
in mortality and causes of death among persons withspinal cord injury. Archives of Physical Medicine andRehabilitation 1999; Vol. 80, issue 11:1411–9. [PUBMED:
10569435]
Estenne 1987
Estenne M, De Troyer A. Mechanism of the posturaldependence of vital capacity in tetraplegic subjects.
American Review of Respiratory Disease 1987;135(2):367–71.
Estenne 1989
Estenne M, Knoop C, Van Vaerenbergh J, Heilporn A,
De Troyer A. The effect of pectoralis muscle training
in tetraplegic subjects. American Review of Respiratory
Disease 1989; Vol. 139, issue 5:1218–22.

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

19

Fishburn 1990
Fishburn MJ, Marino RJ, Ditunno JF. Atelectasis andpneumonia in acute spinal cord injury. Archives of Physical
Medicine and Rehabilitation 1990; Vol. 71:197–200.
Fugl-Meyer 1984
Fugl-Meyer AR, Grimby G. Respiration in tetraplegia
and in hemiplegia: a review. International Rehabilitation
Medicine 1984; Vol. 6, issue 4:186–90.
Fujiwara 1999
Fujiwara T, Hara Y, Chino N. Expiratory function incomplete tetraplegics: study of spirometry, maximal
expiratory pressure, and muscle activity of pectoralis major
and latissimus dorsi muscles. American Journal of Physical
Medicine and Rehabilitation 1999; Vol. 78, issue 5:464–73.
Hart 2005
Hart N, Laffont I, Perez de la Sota A, Lejaille M, Madadou
G, Polkey MI, et al.Respiratory effects of combined truncal
and abdominal support in patients with spinal cord injury.
Archives of Physical Medicine and Rehabilitation 2005;86(7):1447–51.
Higgins 2011
Higgins JPT, Green S (editors). Cochrane Handbook
for Systematic Reviews of Interventions Version 5.1.0[updated March 2011]. The Cochrane Collaboration,
2011. Available from www.cochrane-handbook.org.
Reines 1987
Reines HH, Harris RC. Pulmonary complications of acutespinal cord injuries. Neurosurgery 1987; Vol. 21:193–6.

RevMan 2011
The Nordic Cochrane Centre, The Cochrane Collaboration.
Review Manager (RevMan). 5.1. Copenhagen: The Nordic
Cochrane Centre, The Cochrane Collaboration, 2011.
Rodriguez-Roisin 2009Rodriguez-Roisin R, Anzueto A, Bourbeau J, Calverly
P, deGuia TS, Fukuchi Y, et al.Global strategy for the
diagnosis, management, and prevention of chronic
obstructive pulmonary disease. Executive Summary[updated 2009]. www.goldcopd.org (accessed 14 July2013).
Sale 1988
Sale DG. Neural adaptation to resistance exercise. Medicine
and Science in Sports and Exercise 1988; Vol. 20:S135–45.
Sheel 2008
Sheel AW, Reid WD, Townson AF, Ayas NT, Konnyu KJ,
Team tSCRESR. Effects of exercise training and inspiratory
muscle training in spinal cord injury: a systematic review.
Journal of Spinal Cord Medicine 2008; Vol. 31:500–8.
van den Berg 2010
van den Berg ME, Castellote JM, de Pedro-Cuesta J,
Mahillo-Fernandez I. Survival after spinal cord injury:a systematic review. Journal of Neurotrauma 2010;27:
1517–28.
Van Houtte 2006
Van Houtte S, Vanlandewijck Y, Gosselink R. Respiratory
muscle training in persons with spinal cord injury: asystematic review. Respiratory Medicine 2006; Vol. 100,
issue 11:1886–95.
∗
Indicates the major publication for the study

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

20

CHARACTERISTICS OF STUDIES

Characteristics of included studies [ordered by study ID]
Derrickson 1992
Methods

RCT
Randomisation method: table of random numbers

Participants

11 acute inpatients with C4-C7 complete quadriplegia (9 males, 2 females), aged 16-41
years, USA

Interventions

Inspiratory resistance muscle training (continuous for 15 min/day) vs. abdominal
weights training (10 breaths x 4). The inspiratory resistance group initially trained withleast amount of resistance. Resistance increased when participant was able to complete
3 consecutive sessions of continuous breathing for 15 min. Abdominal weights training
used the maximum weight that did not alter IC and required 4 x 10 maximal inspirations,holding each breath for several seconds
Training intensity: 2 x daily (5 days/week) for 7 weeks

Outcomes

FVC, MVV, PEFR, PImax (also known as MIP), and IC were measured pre and postintervention

Notes

No ’control’ group, likely post randomisation withdrawal not reported

Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Table of random numbers used

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomesHigh risk

40 participants met admission criteria, but
only 11 full sets of data reported (dropout
rate of 73%)

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Respiratory muscle training for cervical spinal cord injury (Review)
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Gounden 1990
Methods

RCT
Randomisation method: not specified

Participants

40 inpatients and outpatients with C5-C7 quadriplegia (32 males, 8 females), aged 1664 years, South Africa

Interventions

Expiratory muscle training (progressive resistive loading) vs. no training. Experimentalgroup trained using the PFLEX Inspiratory Muscle Trainer® and expired against a
resistance set at 60% of maximal expiratory mouth pressure
Training intensity: 5-8 min x 5 daily (6 days/week) for 8 weeks

Outcomes

MEP, VC

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomes

Low risk

No dropouts reported

Selective reporting (reporting bias)

Low risk

Liaw 2000
Methods

RCT
Randomisation method: not specified

Participants

20 inpatients with C4-C7 complete quadriplegia at least 6 months post injury (16 males,
4 females), aged 16-52 years, Taiwan

Interventions

Resistive inspiratory muscle training vs. usual care. Initially trained with at lowest
resistance setting. Resistance level increased when participant able to complete 3 consecutive sessions of continuous breathing
Training intensity: 15-20 min x 2 daily (12-16 breaths/min) for 6 weeks

Outcomes

FVC, FEV1 , PEFR, VC, TLC, RV, RV/TLC, FRC, VE, MIP, MEP, and dyspnoea (Borg
scale) were measured pre and post intervention

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Liaw 2000

(Continued)

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomesHigh risk

30 participants recruited, but 10 dropped
out. Outcome data only presented for the
20 participants who completed the study(dropout rate of 33%)

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Litchke 2008
Methods

RCT with block randomisation (matched by lesion level or track rating, or both)Randomisation method: not specified

Participants

9 wheelchair athletes with C5-T12 SCI (1 neuro disorder, 1 postpolio). All males aged
21-49 years, USA

Interventions

Respiratory resistance training (inspiratory and expiratory) + usual exercise vs. usual
exercise only. Participants instructed to inhale slowly and deeply through the concurrent
flow resistance device, hold their breath for 2 seconds, exhale until almost out of air, thenforcefully blow out as much of the remaining residual air as possible. This sequence wasrepeated up to 10 times with 10-20 seconds of rest between each sequence. Respiratory
resistance was increased by 1 level when able to complete 1 set of 10 without experiencing
respiratory fatigue, dizziness, or light-headedness
Training intensity: (set of 10) 3 x daily for 10 weeks

Outcomes

MIP, MVV, and VO2 peak were measured pre and post intervention

Notes

Only 5 of 9 subjects fit inclusion criteria for this review

Risk of bias
Bias

Authors’ judgement

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

Support for judgement23Litchke 2008

(Continued)

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomesHigh risk

Data not reported for 1 participant who
withdrew from the study (dropout rate of
11%)

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Litchke 2010
Methods

RCT
Randomisation method: not specified

Participants

16 wheelchair athletes with C5-C7 quadriplegia (11 complete, 11 incomplete, 1 spastic
cerebral palsy, 1 congenital deformities). All male, aged 18-50 years, USA

Interventions

Concurrent flow resistance (1 set of 10 breaths) vs. concurrent pressure thresholdresistance (3 sets of 10 breaths) vs. no training. The flow resistance training consisted ofinhaling slowly and deeply through the concurrent flow resistance device, holding breathfor 2-5 seconds, exhaling until almost out of air, then forcefully blowing out as much of
the remaining residual air as possible. This sequence was repeated up to 10 times with
10-20 seconds of rest between each sequence
The pressure resistance training consisted of inhaling fully and forcefully through theconcurrent pressure resistance device for 3 seconds (completely filling the lungs), holding
breath for 1-2 seconds, exhaling fully and forcefully through the device (completely
emptying the lungs), and pausing for 1-2 seconds. For both conditions, respiratory
resistance was increased by 1 level when able to complete 1 set of 10 without experiencing
respiratory fatigue, dizziness, or light-headedness
Training intensity: 3 times daily for 9 weeks

Outcomes

MVV, MIP, and 1-mile time trial performance were measured pre and post intervention

Notes
Risk of bias
Bias

Authors’ judgement

Random sequence generation (selection Low risk
bias)
Respiratory muscle training for cervical spinal cord injury (Review)
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Support for judgement
Random group assignment

24

Litchke 2010

(Continued)

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomesHigh risk

Data reported only for 16 participants whocompleted the study (24 were initially recruited) - dropout rate of 33%

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Loveridge 1989
Methods

RCT
Randomisation method: not specified

Participants

12 outpatients with C6-C7 complete quadriplegia, aged 22-49 years, Canada

Interventions

Inspiratory resistance training vs. no treatment. Participants trained with an inspiratory resistance device at 85% of their SIP at normal resting flow rates
Training intensity: 15 min twice daily (5 days/week) for 8 weeks

Outcomes

MIP, SIP, TLC, RV, FRC, IC, FVC, and breathing frequency were measured every 2
weeks from baseline

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomes

Low risk

No dropouts reported

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Respiratory muscle training for cervical spinal cord injury (Review)
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Mueller 2013
Methods

RCT

Participants

24 participants with C5-C8 complete quadriplegia, aged 22-58 years, Switzerland

Interventions

Inspiratory resistance training vs. isocapnic hyperpnoea vs. placebo (incentive
spirometry). Inspiratory resistance training utilised an electronic inspiratory threshold
device with visual feedback of achieved resistance. Participants were instructed to inhale
with maximal inspiratory power during each of the 90 repetitions. Inhalations with lessthan 80% of the individual maximal inspiratory power had to be repeated. Isocapnic
hyperpnoea utilised a device allowing intensive hyperventilation by partial re-breathingof ventilated air, supported by visual and acoustic feedback of breathing volume andfrequency. Participants had to hyperventilate for 10 min continuously at 40-50% of theirindividual MVV. Intensity was increased by increasing breathing frequency by 1 breath/min every second or third training session. Placebo involved ’volume training’ with an
incentive spirometer, inhaling 16 times from RV to TLC with 30-40 seconds of rest in
between repetitions
Training intensity: 4 x 10 min/week for 8 weeks

Outcomes

TLC, RV, ERV, VC, FEV1 , PEF, MVV, PImax (also known as MIP), PEmax (also known
as MEP), voice loudness and sustain time, subjective ability to cough, clear secretions,blow one’s nose, and breathlessness during exercise, as well as physical and mental qualityof life were measured pre and post intervention

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Not reported

Unclear risk

Blinding (performance bias and detection Low riskbias)
All outcomesSham treatment used for control group. Assessors blinded togroup allocation

Incomplete outcome data (attrition bias)
All outcomesHigh risk

2 dropouts reported

Selective reporting (reporting bias)

Low risk

Results presented for all original variables recorded

Respiratory muscle training for cervical spinal cord injury (Review)
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Roth 2010
Methods

RCT
Randomisation method: based on medical record number

Participants

29 acute inpatients with C4-T1 complete SCI < 6 months post injury (22 males, 7
females), aged 16-60 years, USA

Interventions

Expiratory muscle resistance training vs. sham. The training group exhaled quickly
and forcefully through a high-pressure gauge providing resistance to expiration. The
sham group exhaled forcefully through the same device but with no pressure gauge andthus no resistance. Each participant performed 10 repetitions without resting between
breaths
Training intensity: 2 x 10 repetitions daily (5 days/week) for 6 weeks

Outcomes

FVC, FEV1 , MEP, MIP, IC, ERV, TLC, FRC, and RV were measured pre and postintervention

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Low risk

The randomisation allocations were madeby an investigator who had no contact withany of the subjects and who had no knowledge of the any of the subjects’ demographic or injury characteristics

Blinding (performance bias and detection Low riskbias)
All outcomesSham treatment used for control group. Assessors blinded to group allocation

Incomplete outcome data (attrition bias)
All outcomesHigh risk

Data reported only for 29 participants whocompleted the study (52 were initially recruited) - dropout rate of 42%

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Respiratory muscle training for cervical spinal cord injury (Review)
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Tamplin 2013
Methods

RCT with block randomisation (matched by history of tracheostomy)
Randomisation method: computer-generated table of random numbers

Participants

24 participants with C4-C8 quadriplegia (ASIA A or B), aged 27-70 years, Australia

Interventions

Singing training vs. music appreciation. Singing training included oral motor andrespiratory exercises, vocal warm-ups, and singing familiar songs. Music appreciation
included song sharing and discussion, musical games, and music-assisted relaxation
Training intensity: 1 hour daily (3 days/week) for 12 weeks

Outcomes

FVC, FEV1 , FEV1 /FVC, MEP, MIP, SNIP, IC, TLC, FRC, RV, voice loudness andsustain time, mood and quality of life were measured pre and post intervention

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)Computer-generated randomisation sequence

Allocation concealment (selection bias)

Low risk

Randomised sequence concealed in sealed,
opaque envelopes

Blinding (performance bias and detection Low riskbias)
All outcomes

Participants blinded to which intervention
was the experimental condition. Assessors
blinded to group allocation

Incomplete outcome data (attrition bias)
All outcomes

Low risk

No dropouts reported

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Van Houtte 2008
Methods

RCT with block randomisation (match by lesion level)
Randomisation method: not specified

Participants

14 acute inpatients with C4-T1 SCI (ASIA A, B, or C) at least 6 weeks, but < 6 months
post injury (12 males, 2 females), aged 17-66 years, Belgium

Interventions

Normocapnic hyperpnoea training vs. sham. Normocapnic hyperpnoea training
utilised a re-breathing bag device set at 30-40% of FVC, filling and emptying the bag
completely with each breath at 30-45 breaths/min. Pace or volume (or both) were increased if the participant sustained these targets for 25 min. Sham training breathed at
a constant ventilation of 15% MVV at 15-25 breaths/min

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Van Houtte 2008

(Continued)

Training intensity: 30 min daily (4 days/week) for 8 weeks
Outcomes

FVC, MVV, PImax (also known as MIP), PEmax (also known as MEP), and respiratory
endurance time were measured pre, mid (4 weeks), post (8 weeks), and at follow-up (16weeks)

Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Low risk

Both participants and assessors blinded togroup allocation

Blinding (performance bias and detection Low riskbias)
All outcomesSham treatment used for control group. Assessors blinded to group allocation

Incomplete outcome data (attrition bias)
All outcomes

Low risk

No dropouts reported

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

Zupan 1997
Methods

RCT (cross-over design)
Randomisation method: not specified

Participants

13 inpatients with C4-C7 quadriplegia (10 complete, 3 incomplete) (11 males, 2 females), aged 17-46 years, Slovenia

Interventions

Inspiratory muscle training (incentive spirometry) vs. expiratory muscle training+ electrical stimulation vs. control (no training). For inspiratory muscle training
the participants were instructed to inhale slowly to maximum value on the incentive
spirometer and attempt to hold the breath at 75% of this value for as long as possible.
For expiratory muscle training the participants were instructed to inhale slowly, holdthe breath, and then attempt to achieve maximal expiration on a peak flow meter (twice
without electrical stimulation of the abdominal muscles and 8 times with electricalstimulation) and blow bubbles through a thin straw for 3 min
Training intensity: 7 exercises x 10 sets twice daily (6 days/week) for 4 weeks

Outcomes

FVC and FEV1 (sitting and lying) were measured at baseline and monthly for 3 months.
FVC and FEV1 were measured under 4 conditions: unassisted, manual assistance, elec-

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Zupan 1997

(Continued)

trical simulation (patient), and electrical stimulation (therapist)
Notes
Risk of bias
Bias

Authors’ judgement

Support for judgement

Random sequence generation (selection Low risk
bias)

Random group assignment

Allocation concealment (selection bias)

Unclear risk

Not reported

Blinding (performance bias and detection Unclear riskbias)
All outcomes

Not reported

Incomplete outcome data (attrition bias)
All outcomes

Low risk

No dropouts reported

Selective reporting (reporting bias)

Low risk

Results presented for all original variables
recorded

ASIA: American Spinal Injury Association; ERV: expiratory reserve volume; FEV1 : forced expiratory volume in one second; FRC:
functional residual capacity; FVC: forced vital capacity; IC: inspiratory capacity; MEP: maximal expiratory pressure; MIP: maximal
inspiratory pressure; MVV: maximal voluntary ventilation; PEmax (also known as MEP): maximum expiratory pressure; PEF: peak
expiratory flow; PEFR; peak expiratory flow rate; PImax (also known as MIP): maximum inspiratory pressure; RCT: randomised
controlled trial; RV: residual volume; SCI: spinal cord injury; SIP: sustainable inspiratory pressure; SNIP: sniff nasal inspiratory
pressure; TLC: total lung capacity; VC: vital capacity; VE : volume of expired gas; VO2 : oxygen consumption.

Characteristics of excluded studies [ordered by study ID]

Study

Reason for exclusion

Alvarez 1981

Not an RCT, no RMT intervention

Biering-Sorensen 1991

Not an RCT, no control group, pre-post study

Crane 1994

Not an RCT, exercise training with retrospective sample

Ehrlich 1999

Not an RCT, case study

Epifanov 1987

Not an RCT, not quadriplegia

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(Continued)

Estrup 1986

Not an RCT

Fugl-Meyer 1972

Not an RCTGallego 1993

Not an RCTGoosey-Tolfrey 2010

Not an RCT, not quadriplegia

Gross 1980

Not an RCT

Hornstein 1986

Not an RCT

Imamura 1967

Not an RCT

Lee 2012

Poor description of the expiratory muscle training makes it is difficult to understand if it would have added
to the effect of the mechanical in-exsufflation (which would be expected to be large). Randomisation order
was determined by hospital admission, therefore, no allocation concealment and high potential for bias.
Also, no indication of when the lung volume measures were madeLerman 1987

Not an RCT

Lin 1999

Not an RMT, no training intervention

Lin 2001

Not an RCTMetcalf 1966

Not an RCTMoreno 2012

Not an RCTMoreno 2013

Not an RCT

Nygren-Bonnier 2009

Not an RCT

Rutchik 1998

Not an RCT

Sapienza 2006

Not an RCT

Sutbeyaz 2005

Not an RCT, not quadriplegia

Uijl 1999

Not an RCT, cross-over design, but not randomised

Valent 2009

Not an RCT, no control group, pre-post study, not RMT intervention

Walker 1987

Not an RCTWang 2002

Not an RCT

RCT: randomised controlled trial; RMT: respiratory muscle training.
Respiratory muscle training for cervical spinal cord injury (Review)
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31

DATA AND ANALYSES

Comparison 1. Respiratory muscle training versus control

Outcome or subgroup title
1 Dyspnoea
2 Vital capacity (L)3 Maximal inspiratory pressure(cmH2 O)
4 Maximal expiratory pressure(cmH2 O)
5 Forced expiratory volume in 1
second (L)No. ofstudiesNo. ofparticipants

Statistical method

Effect size

3
4
8

58
108
147

Std. Mean Difference (IV, Random, 95% CI)
Mean Difference (IV, Fixed, 95% CI)
Mean Difference (IV, Fixed, 95% CI)-0.10 [-1.65, 1.44]
0.40 [0.12, 0.69]
10.66 [3.59, 17.72]

6151

Mean Difference (IV, Fixed, 95% CI)

10.31 [2.80, 17.82]

497

Mean Difference (IV, Fixed, 95% CI)

0.05 [-0.23, 0.34]

Analysis 1.1. Comparison 1 Respiratory muscle training versus control, Outcome 1 Dyspnoea.
Review:

Respiratory muscle training for cervical spinal cord injury

Comparison: 1 Respiratory muscle training versus control
Outcome: 1 Dyspnoea

Study or subgroup

Intervention

Std.
Mean
Difference

Control

Std.
Mean
DifferenceN

Mean(SD)N

Mean(SD)

Liaw 2000

10

10.4 (0.7)

10

12 (1.2)

IV,Random,95% CI-1.56 [ -2.59, -0.53 ]IV,Random,95% CI

Mueller 2013 (1)88.5 (1.5)

4

7.3 (2.8)

0.56 [ -0.67, 1.79 ]Mueller 2013 (2)89 (1.5)4

7.3 (2.8)

0.79 [ -0.47, 2.05 ]Van Houtte 2008

7

0 (0)

7

0.7 (1.1)

0.0 [ 0.0, 0.0 ]Total (95% CI)

33-0.10 [ -1.65, 1.44 ]25

Heterogeneity: Tau2 = 1.51; Chi2 = 10.50, df = 2 (P = 0.01); I2 =81%
Test for overall effect: Z = 0.13 (P = 0.89)
Test for subgroup differences: Not applicable-2-1

Favours intervention

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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1

2

Favours control

32

(1) Mueller A(2) Mueller B

Analysis 1.2. Comparison 1 Respiratory muscle training versus control, Outcome 2 Vital capacity (L).
Review:

Respiratory muscle training for cervical spinal cord injury

Comparison: 1 Respiratory muscle training versus control
Outcome: 2 Vital capacity (L)Mean
Difference

WeightMean
Difference

1.41 (0.79)

46.5 %

0.56 [ 0.14, 0.98 ]

10

1.9 (0.9)

20.1 %

0.10 [ -0.54, 0.74 ]

2.7 (0.6)4

2.7 (0.8)

10.4 %

0.0 [ -0.89, 0.89 ]

8

3.4 (1.1)

4

2.7 (0.8)

6.8 %0.70 [ -0.39, 1.79 ]Tamplin 201312

2.96 (0.89)

122.49 (0.89)

16.1 %

0.47 [ -0.24, 1.18 ]Total (95% CI)

58

100.0 %

0.40 [ 0.12, 0.69 ]Study or subgroup

Intervention

ControlN

Mean(SD)N

Mean(SD)

Gounden 1990

20

1.97 (0.54)

20

Liaw 200010

2 (0.5)

Mueller 2013 (1)8Mueller 2013 (2)IV,Fixed,95% CI

IV,Fixed,95% CI

50Heterogeneity: Chi2 = 2.51, df = 4 (P = 0.64); I2 =0.0%
Test for overall effect: Z = 2.77 (P = 0.0056)
Test for subgroup differences: Not applicable-2-1

Favours control

0

1

2

Favours intervention(1) Mueller B(2) Mueller A

Respiratory muscle training for cervical spinal cord injury (Review)
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Analysis 1.3. Comparison 1 Respiratory muscle training versus control, Outcome 3 Maximal inspiratory
pressure (cmH2 O).
Review:

Respiratory muscle training for cervical spinal cord injury

Comparison: 1 Respiratory muscle training versus control
Outcome: 3 Maximal inspiratory pressure (cmH2 O)

Study or subgroup

Intervention

Mean
Difference

Control

WeightMean
DifferenceN

Mean(SD)N

Mean(SD)

Derrickson 1992

6

58.17 (12)5

43.4 (13)IV,Fixed,95% CI
22.5 %

14.77 [ -0.13, 29.67 ]IV,Fixed,95% CI

Liaw 2000

10

58.6 (16.7)

10

63.1 (17.9)

21.7 %-4.50 [ -19.67, 10.67 ]Litchke 20084

107.5 (21.2)

5

102.4 (18.5)

7.2 %

5.10 [ -21.25, 31.45 ]Litchke 2010 (1)4

94.5 (26.1)

3

88.29 (24)

3.6 %6.21 [ -31.10, 43.52 ]Litchke 2010 (2)5106 (16.09)

488.29 (24)

6.6 %

17.71 [ -9.71, 45.13 ]Mueller 2013 (3)876.4 (24.4)

4

78.3 (30.5)

4.2 %-1.90 [ -36.24, 32.44 ]Mueller 2013 (4)8

101.5 (38.2)

4

78.3 (30.5)

3.1 %

23.20 [ -16.73, 63.13 ]Roth 201016

71 (32)

13

56 (30)9.7 %15.00 [ -7.62, 37.62 ]Tamplin 201312

88.9 (20.4)

1275.3 (26.7)

13.8 %

13.60 [ -5.41, 32.61 ]Van Houtte 20087

95 (26)

7

61 (23)7.5 %34.00 [ 8.28, 59.72 ]Total (95% CI)

80

100.0 %

10.66 [ 3.59, 17.72 ]67

Heterogeneity: Chi2 = 8.90, df = 9 (P = 0.45); I2 =0.0%
Test for overall effect: Z = 2.96 (P = 0.0031)
Test for subgroup differences: Not applicable

-50

-25

Favours control

0

25

50

Favours intervention(1) Litchke B(2) Litchke A(3) Mueller A(4) Mueller B

Respiratory muscle training for cervical spinal cord injury (Review)
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Analysis 1.4. Comparison 1 Respiratory muscle training versus control, Outcome 4 Maximal expiratory
pressure (cmH2 O).
Review:

Respiratory muscle training for cervical spinal cord injury

Comparison: 1 Respiratory muscle training versus control
Outcome: 4 Maximal expiratory pressure (cmH2 O)

Mean
Difference

WeightMean
Difference

46.45 (19.91)

31.3 %

21.60 [ 8.17, 35.03 ]10

40.9 (8.9)

34.0 %-1.20 [ -14.09, 11.69 ]67.3 (35.9)

4

65 (40.1)

2.6 %2.30 [ -44.21, 48.81 ]8

63 (38.6)

4

65 (40.1)

2.5 %-2.00 [ -49.54, 45.54 ]Roth 201016

98 (35)13

91.2 (26)

11.4 %

6.80 [ -15.42, 29.02 ]Tamplin 201312

86.6 (37.96)

1291.2 (35.04)

6.6 %-4.60 [ -33.83, 24.63 ]Van Houtte 2008

7

64 (23)734 (19)11.6 %

30.00 [ 7.90, 52.10 ]Total (95% CI)

81

100.0 %

10.31 [ 2.80, 17.82 ]Study or subgroup

Intervention

ControlN

Mean(SD)N

Mean(SD)

Gounden 1990

20

68.05 (23.28)

20

Liaw 2000

10

39.7 (18.8)

Mueller 2013 (1)8Mueller 2013 (2)IV,Fixed,95% CI

IV,Fixed,95% CI

70Heterogeneity: Chi2 = 10.30, df = 6 (P = 0.11); I2 =42%
Test for overall effect: Z = 2.69 (P = 0.0072)
Test for subgroup differences: Not applicable

-50

-25

Favours control

0

25

50

Favours intervention(1) Mueller A(2) Mueller B

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Analysis 1.5. Comparison 1 Respiratory muscle training versus control, Outcome 5 Forced expiratory
volume in 1 second (L).
Review:

Respiratory muscle training for cervical spinal cord injury

Comparison: 1 Respiratory muscle training versus control
Outcome: 5 Forced expiratory volume in 1 second (L)Study or subgroup

Intervention

Mean
Difference

Control

WeightMean
DifferenceN

Mean(SD)N

Mean(SD)

Liaw 2000

10

1.6 (0.4)10

1.7 (0.8)

IV,Fixed,95% CI
25.8 %-0.10 [ -0.65, 0.45 ]IV,Fixed,95% CI

Mueller 2013 (1)8

2.8 (0.9)4

2.4 (0.6)

10.8 %

0.40 [ -0.46, 1.26 ]Mueller 2013 (2)82.3 (0.6)4

2.4 (0.6)

15.3 %-0.10 [ -0.82, 0.62 ]Roth 201016

2 (0.62)13

2.03 (0.81)

27.7 %-0.03 [ -0.56, 0.50 ]Tamplin 201312

2.57 (0.64)

122.27 (0.9)

20.3 %

0.30 [ -0.32, 0.92 ]Total (95% CI)

54100.0 %

0.05 [ -0.23, 0.34 ]43

Heterogeneity: Chi2 = 1.79, df = 4 (P = 0.77); I2 =0.0%
Test for overall effect: Z = 0.38 (P = 0.70)
Test for subgroup differences: Not applicable

-2

-1

0

Favours control

1

2

Favours intervention(1) Mueller A(2) Mueller B

ADDITIONAL TABLES
Table 1. Body position in which respiratory outcomes were measured

Study

Test position

Derrickson 1992 Supine

BinderVital capacity

n/a

MIP

MEP

FEV1

X

Gounden 1990

Supine and sit- ?
ting

X

X

Liaw 2000

Supinen/aX

Litchke 2008

Sitting?

X

Litchke 2010

Sitting?

X

Loveridge 1989

Sitting

?

X

X

X

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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Table 1. Body position in which respiratory outcomes were measured

Mueller 2013

SittingnoRoth 2010

Sitting?

Tamplin 2013

Sittingno

Houtte Sitting

?

Van
2008

Zupan 1997

X

X

(Continued)

X

X

X

X

X

X

X

X

X

X

X

Supine and sit- ?
ting

XGounden 1990 included the ’best’ measure obtained during testing. It was not stated whether data were standardised within participant
for both pre- and post-test measures.
FEV1 : forced expiratory volume in one second; MEP: maximal expiratory pressure; MIP: maximal inspiratory pressure.

APPENDICES
Appendix 1. Search strategies
Cochrane Injuries Group Specialised Register
myelopathy and (traumatic or post-traumatic) OR ((spine or spinal)) and (fracture* or wound* or trauma* or injur* or damage*) OR((“spinal cord”) and (contusion or laceration or transaction or trauma or ischemia or syndrome)) OR SCI
AND((Breath* or respirat*) and (muscle* or exercise*)) OR ((Breath* or respirat*) and (train* or “exercise therap*” or endurance or strength*or resist*)) OR ((normocapnic or hyperpnoea) and train*) OR ((inspiratory or respiratory or breath*) and (endurance or train* or
exercis* or resist* or strength*)) OR RMTCochrane Central Register of Controlled Trials (The Cochrane Library)#1 MeSH descriptor: [Spinal Cord Injuries] explode all trees#2 MeSH descriptor: [Spinal Cord Ischemia] explode all trees#3 MeSH descriptor: [Central Cord Syndrome] explode all trees#4 myelopathy near/3 (traumatic or post-traumatic):ti,ab,kw (Word variations have been searched)#5 (spine or spinal) near/3 (fracture* or wound* or trauma* or injur* or damag*):ti,ab,kw (Word variations have been searched)#6 spinal cord near/3 (contusion* or laceration* or transaction* or trauma* or ischemia*):ti,ab,kw (Word variations have been searched)#7 “central cord injury syndrome”:ti,ab,kw (Word variations have been searched)#8 “central spinal cord syndrome”:ti,ab,kw (Word variations have been searched)#9 MeSH descriptor: [Cervical Vertebrae] explode all trees and with qualifiers: [Injuries - IN]#10 MeSH descriptor: [Spinal Cord] explode all trees#11 MeSH descriptor: [Paraplegia] explode all trees#12 MeSH descriptor: [Quadriplegia] explode all trees#13 SCI:ti,ab,kw (Word variations have been searched)#14 #1 or #2 or #3 or #4 or #5 or #6 or #7 or #8 or #9 or #10 or #11 or #12 or #13#15 MeSH descriptor: [Breathing Exercises] explode all trees#16 MeSH descriptor: [Exercise Therapy] explode all trees
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#17 train* or exercis* or endurance or strength* or resistive:ti,ab,kw (Word variations have been searched)#18 (#15 or #16 or #17)
#19 MeSH descriptor: [Respiratory Muscles] explode all trees#20 #18 and #19#21 normocapnic hyperpnoea training:ti,ab,kw (Word variations have been searched)#22 (inspiratory or respiratory or breath*) near/5 (endurance or train* or exercis* or resist* or strength*):ti,ab,kw (Word variations havebeen searched)#23 RMT:ti,ab,kw (Word variations have been searched)#24 (#15 or #20 or #21 or #22 or #23)
#25 (#14 and #24)
MEDLINE (Ovid SP)
1. exp Spinal Cord Injuries/
2. exp Spinal Cord Ischemia/
3. exp Central Cord Syndrome/
4. (myelopathy adj3 (traumatic or post-traumatic)).ab,ti.
5. ((spine or spinal) adj3 (fracture$ or wound$ or trauma$ or injur$ or damag$)).ab,ti.
6. (spinal cord adj3 (contusion or laceration or transaction or trauma or ischemia)).ab,ti.
7. central cord injury syndrome.ab,ti.
8. central spinal cord syndrome.ab,ti.
9. exp Cervical Vertebrae/in [Injuries]
10. exp Spinal Cord/
11. SCI.ab,ti.
12. exp Paraplegia/
13. exp Quadriplegia/
14. (paraplegia* or quadriplegia* or tetraplegia*).ab,ti.
15. or/1-14
16. exp Breathing Exercises/
17. exp Respiratory Muscles/
18. exp exercise therapy/
19. (train* or exercis* or endurance or strength* or resistive).ab,ti.
20.18 or 19
21.17 and 20
22. normocapnic hyperpnoea training.ab,ti.
23. ((inspiratory or respiratory or breath*) adj5 (endurance or train* or exercis* or resist* or strength*)).ab,ti.
24. RMT.ab,ti.
25. 16 or 21 or 22 or 23 or 24
26. 15 and 25
EMBASE (Ovid SP)
1. exp Spinal Cord Injuries/
2. exp Spinal Cord Ischemia/
3. exp Central Cord Syndrome/
4. (myelopathy adj3 (traumatic or post-traumatic)).ab,ti.
5. ((spine or spinal) adj3 (fracture$ or wound$ or trauma$ or injur$ or damag$)).ab,ti.
6. (spinal cord adj3 (contusion or laceration or transaction or trauma or ischemia)).ab,ti.
7. central cord injury syndrome.ab,ti.
8. central spinal cord syndrome.ab,ti.
9. exp cervical spine/
10. exp Spinal Cord/
11. SCI.ab,ti.
12. exp Paraplegia/
13. exp Quadriplegia/
14. (paraplegia* or quadriplegia* or tetraplegia*).ab,ti.
15. or/1-14
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16. exp Breathing Exercises/
17. exp Respiratory Muscles/
18. exp exercise therapy/
19. (train* or exercis* or endurance or strength* or resistive).ab,ti.
20. 18 or 19
21. 17 and 20
22. normocapnic hyperpnoea training.ab,ti.
23. ((inspiratory or respiratory or breath*) adj5 (endurance or train* or exercis* or resist* or strength*)).ab,ti.
24. RMT.ab,ti.
25. 16 or 21 or 22 or 23 or 24
26. 15 and 25
27. limit 26 to exclude MEDLINE journals
PubMed((publisher[SB])) AND (((((((((((paraplegi*[title/abstract] OR quadriplegi*[title/abstract] OR tetraplegi*[title/abstract])) OR(SCI[Title/Abstract])) OR ((((“Cervical Vertebrae/injuries”[Mesh]) OR “Spinal Cord”[Mesh]) OR “Paraplegia”[Mesh]) OR“Quadriplegia”[Mesh])) OR (central cord injury syndrome[Title/Abstract] OR “central spinal cord syndrome”[Title/Abstract])) OR(((((((contusion*[Title/Abstract]) OR laceration*[Title/Abstract]) OR transaction*[Title/Abstract]) OR trauma*[Title/Abstract]) OR
ischemia*[Title/Abstract])) AND (spinal cord[Title/Abstract]))) OR (((((((fracture*[Title/Abstract]) OR wound*[Title/Abstract]) OR
trauma*[Title/Abstract]) OR injur*[Title/Abstract]) OR damag*[Title/Abstract])) AND ((spine[Title/Abstract]) OR spinal[Title/Abstract]))) OR ((((post-traumatic[Title/Abstract]) OR traumatic[Title/Abstract])) AND (myelopathy[Title/Abstract]))) OR (((“Spinal
Cord Injuries”[Mesh:noexp]) OR “Central Cord Syndrome”[Mesh]) OR “Spinal Cord Ischemia”[Mesh]))) AND (((((((“Respiratory Muscles”[Mesh])) AND ((((“Breathing Exercises”[Mesh]) OR “Exercise Therapy”[Mesh])) OR (train*[title/abstract] OR exercis*[title/abstract] OR endurance[title/abstract] OR strength*[title/abstract] OR resistive[title/abstract])))) OR (normocapnic hyperpnoea training[Title/Abstract])) OR (RMT[Title/Abstract])) OR (((inspiratory[title/abstract] OR respiratory[title/abstract] ORbreath*[title/abstract])) AND (endurance[title/abstract] OR train*[title/abstract] OR exercis*[title/abstract] OR resist*[title/abstract]
OR strength*[title/abstract]))))
CINAHL (EBSCO)S21 S9 and S20 (Limiters - Exclude MEDLINE records)
S20 S11 or S12 or S16 or S17 or S18 or S19
S19 TX RMTS18 TX (inspiratory or respiratory or breath*) and (endurance or train* or exercis* or resist* or strength*)
S17 TX normocapnic hyperpnoea training
S16 S10 and S15
S15 S11 or S12 or S13 or S14
S14 TX train* or exercis* or endurance or strength* or resistive
S13 (MH “Therapeutic Exercise+”)S12 (MH “Buteyko Method”)
S11 (MH “Breathing Exercises+”)
S10 (MH “Respiratory Muscles+”)
S9 S1 or S2 or S3 or S4 or S5 or S6 or S7 or S8S8 TX paraplegi* or quadriplegi* or tetraplegi* or SCI
S7 (MH “Cervical Vertebrae/IN”)
S6 TI spinal cord and (contusion or laceration or transaction or trauma or ischemia)
S5 TI (spine or spinal) AND (fracture* or wound* or trauma* or injur* or damage)
S4 TX myelopathy N5 post-traumatic
S3 TX myelopathy N5 traumatic
S2 (MH “Spinal Cord Injury Nursing”)
S1 (MH “Spinal Cord Injuries+”)
ISI Web of Science: Science Citation Index Expanded (SCI-EXPANDED)
ISI Web of Science: Conference Proceedings Citation Index-Science (CPCI-S)
1. TS=(myelopathy and (traumatic or post-traumatic)) OR TS=((spine or spinal) same (fracture* or wound* or trauma* or injur* or
damage*)) OR TS=(“spinal cord” same (contusion or laceration or transaction or trauma or ischemia or syndrome)) OR TS=(SCI)
Respiratory muscle training for cervical spinal cord injury (Review)
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2. TS=(Respiratory Muscle* same (train* or exercis* or endurance or strength* or resistive or Therap*)) OR TS=(normocapnic hyperpnoea training) OR TS=((inspiratory or respiratory or breath*) same (endurance or train* or exercis* or resist* or strength*)) OR TS=(RMT)
3. 1 and 2
Australian New Zealand Clinical Trials Registryspinal injury
ClinicalTrials.gov
spinal injury AND respiratory
Current Controlled Trials
spinal injury AND respiratory

CONTRIBUTIONS OF AUTHORS
Jeanette Tamplin drafted the protocol and replied to comment of the peer reviewer. David Berlowitz reviewed the draft and approved
the final version.
For the review:
Jeanette Tamplin:• Assisting with design of search strategies, undertaking and screening searches, organising retrieval of papers;• Screening retrieved papers against eligibility criteria, appraising quality of papers, developing a data collection form, andextracting data from papers;• Inter-rater reliability (trial selection);• Writing to authors of papers for additional information;• Providing additional data about papers, obtaining and screening data on unpublished studies;• Entering data into RevMan;• Analysis and interpretation of data;• Writing the review.
David Berlowitz:• Screening retrieved papers against eligibility criteria, appraising quality of papers, and extracting data from papers;• Providing additional data about papers, obtaining and screening data on unpublished studies;• Analysis and interpretation of data;• Assisting with writing the review.

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

40

DECLARATIONS OF INTEREST
The review authors are currently involved in a research study, which, on completion, may be eligible for inclusion in this review.

SOURCES OF SUPPORTInternal sources• No sources of support supplied

External sources• Victorian Neurotrauma Initiative, Australia.

DIFFERENCES BETWEEN PROTOCOL AND REVIEW
None.

Respiratory muscle training for cervical spinal cord injury (Review)
Copyright © 2013 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.

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