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Respiratory muscle training for cervical spinal cord injury

  1. David J Berlowitz*,
  2. Jeanette Tamplin

Editorial Group: Cochrane Injuries Group

Published Online: 23 JUL 2013

Assessed as up-to-date: 28 JUN 2013

DOI: 10.1002/14651858.CD008507.pub2

How to Cite

Berlowitz DJ, 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.

Author Information

  1. Austin Health, Institute for Breathing and Sleep, Heidelberg, 3084, Australia

*David J Berlowitz, Institute for Breathing and Sleep, Austin Health, 145 Studley Road, Heidelberg, 3084, Australia. david.berlowitz@austin.org.au.

Publication History

  1. Publication Status: Edited (no change to conclusions)
  2. Published Online: 23 JUL 2013

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Summary of findings    [Explanations]

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

 
Summary of findings for the main comparison. Respiratory muscle training compared with control for cervical spinal cord injury

Respiratory muscle training compared with control for cervical spinal cord injury

Patient or population: cervical spinal cord injury
Settings: hospital and community
Intervention: RMT
Comparison: control

OutcomesIllustrative comparative risks* (95% CI)Relative effect
(95% CI)
No of Participants
(studies)
Quality of the evidence
(GRADE)
Comments

Assumed riskCorresponding risk

ControlRMT

Dyspnoea
Borg scale, modified Borg scale, and visual analogue scale
Follow-up: 6-8 weeks
The mean dyspnoea in the intervention groups was
0.10 standard deviations lower
(1.65 lower to 1.44 higher)
58
(3 studies)
⊕⊕⊝⊝
low1,2
SMD -0.10 (-1.65 to 1.44))

Vital capacity
Follow-up: 6-12 weeks
The mean vital capacity ranged across control groups from
1.4 to 2.7 L
The mean vital capacity in the intervention groups was
0.40 higher
(0.12 to 0.69 higher)
108
(4 studies)
⊕⊕⊝⊝
low1,2,3
SMD 0.50 (0.11 to 0.89)

Maximum inspiratory pressure
Follow-up: 6-12 weeks
The mean maximum inspiratory pressure ranged across control groups from
43 to 102 cm/H2O
The mean maximum inspiratory pressure in the intervention groups was
10.66 higher
(3.59 to 17.72 higher)
147
(8 studies)
⊕⊕⊝⊝
low1,2
SMD 0.44 (0.10 to 0.78)

Maximum expiratory pressure
Follow-up: 6-12 weeks
The mean maximum expiratory pressure ranged across control groups from
41 to 91 cm/H2O
The mean maximum expiratory pressure in the intervention groups was
10.31 higher
(2.80 to 17.82 higher)
151
(6 studies)
⊕⊕⊝⊝
low1,2,3
SMD 0.36 (0.03 to 0.69)

Forced expiratory volume in 1 second
Follow-up: 6-12 weeks
The mean forced expiratory volume in 1 second ranged across control groups from
1.7 to 2.4 L
The mean forced expiratory volume in 1 second in the intervention groups was
0.05 higher
(0.23 lower to 0.34 higher)
97
(4 studies)
⊕⊕⊝⊝
low1,2,3
SMD 0.08 (-0.33 to 0.49)

Quality of life
Follow-up: 6-12 weeks
See commentSee commentNot estimable78
(4 studies)
⊕⊕⊝⊝
low1,2,3

Respiratory complications
Follow-up: 8 weeks
See commentSee commentNot estimable14
(1 study)
⊕⊕⊕⊕
high

*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 the assumed 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.

GRADE Working Group grades of evidence
High 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.

 1 High risk of attrition bias.
2 Inconsistency of results + small number of studies with small sample sizes.
3 Blinding and allocation concealment unclear.

 

Background

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

Spinal cord injury (SCI) is damage to the spinal cord that results in a loss or impairment of function resulting in reduced mobility or sensation. When the spinal cord is injured, muscles below the level 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 both the 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.

Respiratory dysfunction resulting from SCI remains a major cause of morbidity, mortality, and economic burden (van den Berg 2010). It is the most common cause of death following SCI and contributes to higher mortality rates for people with SCI than the general 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) movement of 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 lung volumes. 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). Total lung 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 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 of great benefit to people with SCI.

 

Description of the condition

Respiratory dysfunction post SCI is characterised by weak or paralysed respiratory muscles, resulting in reduced lung volume, ineffective cough, increased respiratory tract infections, reduced chest wall compliance, and an increased oxygen cost of breathing (Brown 2006; Chen 1990). In particular, paralysis of intercostal and abdominal muscles causes a decrease in inspiratory volume during resting breathing, and the loss of expiratory force during cough (Alvarez 1981). This respiratory inefficiency also increases the risk of respiratory muscle fatigue, particularly when load is imposed on the muscles, as with pneumonia or obstruction of the airways (Fugl-Meyer 1984).

 

Description of the intervention

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 be trained in a similar way to the limb muscles with devices that increase the load on the muscles. A training session typically consists of a certain number of exercise repetitions, or a particular length of time spent exercising. Training intensity is individually set at a percentage 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 one-way 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 consists of a re-breathing bag (at 30% to 40% of the participant's forced VC) 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 minute ventilation 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, and recruitment of accessory respiratory muscles. Therapeutic singing training was thus considered to constitute a form of RMT in this review.

 

How the intervention might work

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 major and latissimus dorsi for expiration) to improve performance during maximal effort tasks (Fujiwara 1999), and that the strength of 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, such as 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.

 

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 these muscles could be trained to increase in strength or endurance, or both. This review is needed to determine whether such training of the respiratory muscles is effective for people with cervical SCI, and if so, what are the best training techniques and methods to achieve improvements in respiratory function.

Previously, Brooks 2005, Sheel 2008, and Van Houtte 2006 attempted to review research systematically to evaluate the effect of RMT in people with SCI on respiratory muscle strength, endurance, and pulmonary function. These reviews focused on particular types of training, that is, inspiratory muscle training (Brooks 2005; Sheel 2008) and exercise training (Sheel 2008), and used different inclusion criteria, that is, randomised versus non-randomised designs (Brooks 2005). The three reviews reported that the included studies were too variable in terms of research design, participant characteristics, training techniques used, and outcomes measured, thus results could not be pooled for meta-analysis. 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 needed in order to synthesise these disparate findings for people living with 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, and second, it will aim to provide methodological recommendations for future clinical research in this area.

 

Objectives

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

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

 

Methods

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms
 

Criteria for considering studies for this review

 

Types of studies

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

 

Types of participants

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 not caused by SCI (such as chronic obstructive pulmonary disease and asthma).

 

Types of interventions

We considered trials for inclusion if the trial author(s) described an intervention as RMT and compared it with a control group using 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 respiratory complications, dyspnoea, and VC. Respiratory complications are defined 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

  1. Respiratory complications
  2. Dyspnoea
  3. VC

 

Secondary outcomes

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

 

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 March 2013);
  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 March 2013);
  6. CINAHL Plus (EBSCO) (1937 to 6 March 2013);
  7. ISI Web of Science: Science Citation Index Expanded (SCI-EXPANDED) (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 of trials 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 and literature 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. 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 the trial's eligibility for inclusion. Review authors reported and resolved disagreements by discussion. We noted the reasons for excluding studies.

 

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) and assessed 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 of the 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 of bias (Higgins 2011). This tool assesses the following domains: sequence generation, allocation concealment, blinding, incomplete outcome data, selective outcome reporting, and other sources of bias. On each domain, the review authors made a judgement of low risk of bias ('Yes'), high risk of bias ('No'), or unclear risk of bias ('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 the randomisation 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 not allow either investigators or participants to know or influence treatment group assignment at the time of study entry. Acceptable methods included central allocation or sequentially numbered, opaque, sealed envelopes.
  • No: the method of allocation was not concealed (e.g. alternating participants, odd-even day) or one in which the investigators 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 not clearly adequate.

Blinding of outcome assessors

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

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 uncertain from the report whether this was fully carried out.

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 to true outcome, with either imbalance in numbers or reasons for missing data across intervention groups, or potentially inappropriate application of simple imputation.
  • Unclear: insufficient reporting of attrition/exclusions to permit judgement of 'Yes' or 'No' (e.g. number randomised not stated, no reasons for missing data provided).

Selectiveness of outcome reporting

  • Yes: the study protocol was available and all of the study's prespecified (primary and secondary) outcomes that are of interest 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 not prespecified, 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.

 

Measures of treatment effect

We anticipated that all outcomes measured in this review would be continuous variables. Thus, we calculated standardised mean differences (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.

 

Dealing with missing data

We considered an ITT analysis adequate when the numbers of people who dropped out and the reasons why they dropped out 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).

 

Assessment of heterogeneity

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 of heterogeneity 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 random-effects 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.

 

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 each study. 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 to determine any relationship between treatment intensity or duration and an intervention effect.

 

Sensitivity analysis

We performed sensitivity analyses based on the methodological quality of the included studies. The analyses examined the effect of 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.

 

Results

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms
 

Description of studies

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

 

Results of the search

The database searches identified 843 citations. After duplicates and animal studies were removed, 747 citations remained. We screened the abstracts of these 747 citations and retrieved 40 full-text 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 the reference lists of these 40 papers for possible additional studies to include. This generated a further six studies. Three of the 40 studies were not written in English. A native speaker of the language that 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.

 FigureFigure 1. Flow diagram.

 

Included studies

We included 11 studies with 212 participants in this review. These studies 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 the data analysis. Completed details of all included studies are provided in the Characteristics of included studies table. Below is a brief summary of the 11 included studies.

 

Design

All 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 and seven comparisons between RMT and a control condition (three sham 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 (Loveridge 1989) (see  Table 1). Testing with an abdominal binder has been reported 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 confirmed that 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) used normocapnic or isocapnic hyperpnoea and Tamplin 2013 used singing 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 two studies that could enable comparison of percentage of predicted scores. We were unable to contact the authors of these studies to obtain 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 in the risk of bias tables included with the Characteristics of included studies table.

 FigureFigure 2. Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
 FigureFigure 3. Risk of bias summary: review authors' judgements about each risk of bias item for each included study.

 

Allocation

Only two studies (18%) described adequate allocation concealment (Tamplin 2013; Van Houtte 2008).

 

Blinding

Only four studies (36%) described blinding of participants and assessors (Mueller 2013; Roth 2010; Tamplin 2013; Van Houtte 2008).

 

Incomplete outcome data

We classified six of the included studies (55%) as having a high risk 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 the remaining six trials.

 

Selective reporting

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.

 

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 injury

See:  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 measures or scales, most studies did not provide change score standard deviations. Thus, we conducted the meta-analysis using mean post-test scores for control and intervention groups. Although this meant that we could not account for baseline scores between groups and between studies, random allocation should account for any baseline differences.

 

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.

 

Dyspnoea

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 the modified has only 10 points) (Liaw 2000; Van Houtte 2008), and one study used a 10-point visual analogue scale (Mueller 2013). 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 was applied due to the high level of heterogeneity between the three studies (I2 = 81%) ( Analysis 1.1).

 

Vital capacity

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.

 

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 the meta-analysis indicated a significant effect of RMT on MIP (MD mean end point 10.66 cm/H2O, 95% CI 3.59 to 17.72, P value = 0.003; I2 = 0%) ( Analysis 1.3). In the included studies, the mean control MIP ranged from 43 to -102 cm/H2O. As such, an improvement of 10 cm/H2O represents approximately a 10% to 25% improvement. The Derrickson 1992 study used another form 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 the data from this study did not significantly alter the result (MD mean end point 9.47 cm/H2O, 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/H2O, 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/H2O. As such, an improvement of 10 cm/H2O represents approximately a 10% to 25% improvement.

 

Forced expiratory volume in one second

The pooled estimate of four studies examining FEV1 indicated no strong 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 health-related 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 compared with 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 found no 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 the diversity of instruments and subscales used between studies.

 

Sensitivity analyses

We conducted sensitivity analyses based on the methodological quality of the included studies. The analyses examined the effect of 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 meant that we removed all but one study from the analysis and, therefore, meta-analysis was impossible. After removing the two studies with a high risk of attrition bias (Liaw 2000; Roth 2010), a stronger effect was found for both MIP (MD mean end point 14.17 cm/H2O, 95% CI 5.85 to 22.49, P value = 0.0008) and MEP (MD mean end point 17.35 cm/H2O, 95% CI 7.42 to 27.27, P value = 0.0006).

 

Subgroup analyses

We conducted subgroup analyses only on outcomes that had data from more than three trials (MIP and MEP). When we included studies with only acute (less than one year) participants in the analysis (Derrickson 1992; Liaw 2000; Mueller 2013 (A); Mueller 2013(B); Roth 2010; Van Houtte 2008), the effect on MIP was minimal but the studies were more heterogeneous (MD mean end point 9.99 cm/H2O, 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/H2O, 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 an intervention 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 eight weeks in the meta-analysis of MIP and MEP, there was no longer a significant 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

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

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 the small 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 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 the cervical SCI population with a range of injury levels and severity (ATS/ERS 2002; ATS/ERS 2005). This increased 'measure-specific' variability and the consequent larger standard deviation of 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 and further research is needed. The respiratory muscle strength (MIP and MEP) results are more reliable due to the greater number of included 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 from the Van Houtte 2008 study indicated minimal change in dyspnoea scores over time for either group, whereas the data from the Liaw 2000 study indicated a significant difference between groups in improvement on dyspnoea scores. Mueller 2013 found a high effect 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 quality of 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 RMT on these more functional outcomes (dyspnoea, quality of life, and respiratory complications).

 

Overall completeness and applicability of evidence

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 and study information where necessary. Overall, the quality of reporting risk of bias was poor. Only four studies reported the method of 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 of different types of RMT in this review. These included: inspiratory muscle training, expiratory muscle training, and techniques that trained 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 is needed 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-risk studies 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. This may have altered the estimate of the overall effect size for the intervention.

In cervical SCI, respiratory function measures may be substantially affected by both the position in which the tests are performed and the presence or not of an abdominal binder. For example, an increase in VC is observed in cervical SCI when changing from the seated to the supine posture. This is the opposite to that which is observed 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 position in which respiratory function and strength was measured varied across the 11 studies and while likely, it was uncertain whether testing position and abdominal binder use was standardised within each 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.

 

Agreements and disagreements with other studies 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 this review. Furthermore, the small number of studies that were included were heterogeneous in terms of research design, participant characteristics, training techniques, and comparison conditions used. The systematic review by Van Houtte 2006 found trends towards improvement following RMT on VC and MEP (which were 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

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

 

Implications for practice

The results of this review suggest that respiratory muscle training (RMT) can improve vital capacity and respiratory muscle strength (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, respiratory complications, hospital admissions, or quality of life.

 
Implications for research

More large-scale studies are needed to examine the effect of RMT on 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 a dosage 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 of life, respiratory morbidity, and mortality.

 

Acknowledgements

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

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;
  • Prof Ian Roberts, Professor of Epidemiology & Public Health, Cochrane Injuries Group;
  • Dr Vasiliy V. Vlassov, President, Society for Evidence Based Medicine, Russia.

 

Data and analyses

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms
Download statistical data

 
Comparison 1. Respiratory muscle training versus control

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Dyspnoea358Std. Mean Difference (IV, Random, 95% CI)-0.10 [-1.65, 1.44]

 2 Vital capacity (L)4108Mean Difference (IV, Fixed, 95% CI)0.40 [0.12, 0.69]

 3 Maximal inspiratory pressure (cmH2O)8147Mean Difference (IV, Fixed, 95% CI)10.66 [3.59, 17.72]

 4 Maximal expiratory pressure (cmH2O)6151Mean Difference (IV, Fixed, 95% CI)10.31 [2.80, 17.82]

 5 Forced expiratory volume in 1 second (L)497Mean Difference (IV, Fixed, 95% CI)0.05 [-0.23, 0.34]

 

Appendices

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms
 

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 RMT

Cochrane 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
#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 have been 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
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] OR breath*[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 RMT

S18 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 S8

S8 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)

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 Registry

spinal injury

ClinicalTrials.gov

spinal injury AND respiratory

Current Controlled Trials

spinal injury AND respiratory

 

What's new

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

Last assessed as up-to-date: 28 June 2013.


DateEventDescription

16 January 2014AmendedReference to another version of this review has been added (Tamplin 2014).



 

History

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

Protocol first published: Issue 5, 2010
Review first published: Issue 7, 2013


DateEventDescription

6 August 2013AmendedUpdated SoF table



 

Contributions of authors

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

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, and extracting 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.

 

Declarations of interest

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

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

 

Sources of support

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms
 

Internal sources

  • No sources of support supplied

 

External sources

  • Victorian Neurotrauma Initiative, Australia.

 

Differences between protocol and review

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

None.

 

Notes

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Notes
  19. Index terms

Additional study outcomes which were not pre-specified in the protocol for this review have been published elsewhere Tamplin 2014.

* Indicates the major publication for the study

References

References to studies included in this review

  1. Top of page
  2. AbstractRésumé
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Notes
  20. Characteristics of studies
  21. References to studies included in this review
  22. References to studies excluded from this review
  23. Additional references
  24. References to other published versions of this review
Derrickson 1992 {published data only}
  • Derrickson J, Ciesla N, Simpson N, Imle PC. A comparison of two breathing exercise programs for patients with quadriplegia. Physical Therapy 1992;72(11):763-9.
Gounden 1990 {published data only}
  • Gounden P. Progressive resistive loading on accessory expiratory muscles in tetraplegia. South African Journal of Physiotherapy 1990;46(4):4-12.
Liaw 2000 {published data only}
  • Liaw MY, Lin MC, Cheng PT, Wong MK, Tang FT. Resistive inspiratory muscle training: its effectiveness in patients with acute complete cervical cord injury. Archives of Physical Medicine and Rehabilitation 2000;81(6):752-6.
Litchke 2008 {published data only}
  • Litchke LG, Russian CJ, Lloyd LK, Schmidt EA, Price L, Walker JL. Effects of respiratory resistance training with a concurrent flow device on wheelchair athletes. Journal of Spinal Cord Medicine 2008;31(1):65-71.
Litchke 2010 {published data only}
  • Litchke L, Lloyd L, Schmidt E, Russian C, Reardon R. Comparison of two concurrent respiratory resistance devices on pulmonary function and time trial performance of wheel chair athletes. Therapeutic Recreation Journal 2010;44(1):51-62.
  • Litchke L, Lloyd L, Schmidt E, Russian C, Reardon R. Effects of concurrent respiratory resistance training on health-related quality of life in wheelchair rugby athletes: a pilot study. Topics in Spinal Cord Injury Rehabilitation 2012;18(3):264-72.
Loveridge 1989 {published data only}
  • Loveridge B, Badour M, Dubo H. Ventilatory muscle endurance training in quadriplegia: effects on breathing pattern. Paraplegia 1989;27(5):329-39.
Mueller 2013 {published data only}
  • Mueller G, Hopman MTE, Perret C. Comparison of respiratory muscle training methods in individuals with motor and sensory complete tetraplegia - a randomized controlled trial. Journal of Rehabilitation Medicine 2013;45(3):248-53.
Roth 2010 {published data only}
  • Roth EJ, Stenson KW, Powley S, Oken J, Primack S, Nussbaum SB, et al. Expiratory muscle training in spinal cord injury: a randomized controlled trial. Archives of Physical Medicine and Rehabilitation 2010;91(6):857-61.
Tamplin 2013 {published data only}
  • Tamplin J, Baker F, Grocke D, Brazzale D, Pretto JJ, Ruehland WR, et al. The effect of singing on respiratory function, voice, and mood following quadriplegia: a randomized controlled trial. Archives of Physical Medicine and Rehabilitation 2013;94(3):426-34.
Van Houtte 2008 {published data only}
  • Van Houtte S, Vanlandewijck Y, Kiekens C, Spengler CM, Gosselink R. Patients with acute spinal cord injury benefit from normocapnic hyperpnoea training. Journal of Rehabilitation Medicine 2008;40(2):119-25.
Zupan 1997 {published data only}
  • Zupan A, Savrin R, Erjavec T, Kralj A, Karcnik T, Skorjanc T, et al. Effects of respiratory muscle training and electrical stimulation of abdominal muscles on respiratory capabilities in tetraplegic patients. Spinal Cord 1997;35(8):540-5.

References to studies excluded from this review

  1. Top of page
  2. AbstractRésumé
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Notes
  20. Characteristics of studies
  21. References to studies included in this review
  22. References to studies excluded from this review
  23. Additional references
  24. References to other published versions of this review
Alvarez 1981 {published data only}
Biering-Sorensen 1991 {published data only}
  • Biering-Sorensen F, Lehmann Knudsen J, Schmidt A, Bundgaard A, Christensen I. Effect of respiratory training with a mouth-nose-mask in tetraplegics. Paraplegia 1991;29(2):113-9.
Crane 1994 {published data only}
  • Crane L, Klerk K, Ruhl A, Warner P, Ruhl C, Roach KE. The effect of exercise training on pulmonary function in persons with quadriplegia. Paraplegia 1994;32(7):435-41.
Ehrlich 1999 {published data only}
  • Ehrlich M, Manns PJ, Poulin C. Respiratory training for a person with C3-C4 tetraplegia. Australian Journal of Physiotherapy 1999;45(4):301-7.
Epifanov 1987 {published data only}
  • Epifanov VA, Zverev VV. Therapeutic physical exercise in the intensive therapy of patients with injuries to the cervical spine and spinal cord. Voprosy Kurortologii, Fizioterapii i Lechebnoi Fizicheskoi Kultury 1987;Mar-Apr(2):52-4.
Estrup 1986 {published data only}
  • Estrup C, Lyager S, Noeraa N, Olsen C. Effect of respiratory muscle training in patients with neuromuscular diseases and in normals. Respiration 1986;50(1):36-43.
Fugl-Meyer 1972 {published data only}
  • Fugl-Meyer AR. Respiratory function and training in traumatic spinal cord injuries. Lakartidningen 1972;69(25):3038-40.
Gallego 1993 {published data only}
  • Gallego J, Perez de la Sota A, Vardon G, Jaeger-Denavit O. Learned activation of thoracic inspiratory muscles in tetraplegics. American Journal of Physical Medicine & Rehabilitation 1993;72(5):312-7.
Goosey-Tolfrey 2010 {published data only}
  • Goosey-Tolfrey V, Foden E, Perret C, Degens H. Effects of inspiratory muscle training on respiratory function and repetitive sprint performance in wheelchair basketball players. British Journal of Sports Medicine 2010;44(9):665-8.
Gross 1980 {published data only}
Hornstein 1986 {published data only}
  • Hornstein S, Ledsome JR. Ventilatory muscle training in acute quadriplegia. Physiotherapy Canada 1986;38(3):145-9.
Imamura 1967 {published data only}
  • Imamura T. The effect of auxiliary respiratory muscular training on breathing exercise in cervical cord injuries. Journal of the Kumamoto Medical Society 1967;41(2):130-51.
Lee 2012 {published data only}
  • Lee Y, Kim J, Jin Y. The efficacy of pulmonary rehabilitation using a mechanical in-exsufflator and feedback respiratory training for cervical cord injury patients. Journal of Physical Therapy Science 2012;24(1):89-92.
Lerman 1987 {published data only}
  • Lerman RM, Weiss MS. Progressive resistive exercise in weaning high quadriplegics from the ventilator. Paraplegia 1987;25(2):130-5.
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 maximal voluntary breathing in chronic tetraplegic patients. Archives of Physical Medicine and Rehabilitation 1999;80(7):741-5.
Lin 2001 {published data only}
  • Lin VW, Hsiao I N, Zhu E, Perkash I. Functional magnetic stimulation for conditioning of expiratory muscles in patients 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 breathing in 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 for lung 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}
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 in quadriplegics 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-disordered breathing of traumatic tetraplegia. Archives of Physical Medicine & Rehabilitation 2002;83(4):491-6.

Additional references

  1. Top of page
  2. AbstractRésumé
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Notes
  20. Characteristics of studies
  21. References to studies included in this review
  22. References to studies excluded from this review
  23. Additional references
  24. References to other published versions of this review
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
Brooks 2005
  • Brooks D, O'Brien K, Geddes EL, Crowe J, Reid D. Is inspiratory muscle training effective for individuals with cervical 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 in patients 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 with spinal cord injury. Archives of Physical Medicine and Rehabilitation 1999; Vol. 80, issue 11:1411-9. [PUBMED: 10569435]
Estenne 1987
  • Estenne M, De Troyer A. Mechanism of the postural dependence of vital capacity in tetraplegic subjects. American Review of Respiratory Disease 1987;135(2):367-71.
Estenne 1989
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Fishburn 1990
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Fugl-Meyer 1984
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Fujiwara 1999
  • Fujiwara T, Hara Y, Chino N. Expiratory function in complete 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
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Reines 1987
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RevMan 2011
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Rodriguez-Roisin 2009
  • Rodriguez-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 July 2013).
Sale 1988
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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
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Van Houtte 2006
  • Van Houtte S, Vanlandewijck Y, Gosselink R. Respiratory muscle training in persons with spinal cord injury: a systematic review. Respiratory Medicine 2006; Vol. 100, issue 11:1886-95.