ARTICLE IN PRESS Respiratory Medicine (2006) 100, 1886–1895
REVIEW
Respiratory muscle training in persons with spinal cord injury: A systematic review Siska Van Houttea, Yves Vanlandewijcka, Rik Gosselinka,b, a
Faculty of Kinesiology and Rehabilitation Sciences, Katholieke Universiteit Leuven, Tervuursevest 101, 3001 Leuven, Belgium b Respiratory Division and Respiratory Rehabilitation Unit, Universitaire Ziekenhuizen Leuven, Herestraat 49, 3000 Leuven, Belgium Received 22 August 2005; accepted 24 February 2006
KEYWORDS Lung volumes; Paraplegia; Quadriplegia; Respiratory muscles; Respiratory strength and endurance; Training
Summary The purpose of this paper was to review the effectiveness of respiratory muscle training (RMT) on respiratory muscle strength and endurance, pulmonary function, quality of life, respiratory complications and exercise performance in persons with spinal cord injury. A MEDLINE (National Library of Medicine, Bethesda, MD, USA) database was used for selection of the literature (from 1980 to November 2004), and relevant references from peer-reviewed articles were retrieved as well. Studies investigating the effects of RMT (i.e. resistive breathing weight lifting or normocapnic hyperpnea) in persons with spinal cord injury were selected. Two independent reviewers investigated controlled studies for methodological quality by using a modification of the framework for methodological quality. Methodological quality ranged between 15 and 29 (maximal feasible score ¼ 40). Twenty-three papers were retrieved and six controlled trials were kept for further analysis. A meta-analysis and calculation of effect-size of each individual study and weighted summary effect-size was intended. However, unreported data and heterogeneity in outcome variables did not allow performing a meta-analysis. From the systematic review it is concluded that RMT tended to improve expiratory muscle strength, vital capacity and residual volume. Insufficient data was available to make conclusions concerning the effects on inspiratory muscle strength, respiratory muscle endurance, quality of life, exercise performance and respiratory complications. & 2006 Elsevier Ltd. All rights reserved.
Corresponding author. Respiratory Division and Respiratory Rehabilitation Unit, Universitaire Ziekenhuizen Leuven, Herestraat 49,
3000 Leuven, Belgium. Tel.: +32 16 346760; fax: +32 16 347126. E-mail address:
[email protected] (R. Gosselink). 0954-6111/$ - see front matter & 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.rmed.2006.02.029
ARTICLE IN PRESS Respiratory muscle training in persons with spinal cord injury
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Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Study identification and selection . . . . . . . . . . . . . . . . . . . . . . . . . Methodological quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Meta-analysis, effect-size and training effects . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Study identification and selection . . . . . . . . . . . . . . . . . . . . . . . . . Methodological quality and study characteristics . . . . . . . . . . . . . . . . Methodological quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Study characteristics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effects of RMT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory muscle strength . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory muscle endurance . . . . . . . . . . . . . . . . . . . . . . . . . Pulmonary function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory complications, quality of life, exercise performance . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methodological quality and study characteristics . . . . . . . . . . . . . . . . Effects of RMT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory muscle strength . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory muscle endurance . . . . . . . . . . . . . . . . . . . . . . . . . Pulmonary function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory complications, quality of life and exercise performance. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Competing interests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction A spinal cord injury is a central neurological disorder with reported incidence of 49.1 per million habitants in Oklahoma, USA.1 Besides paralysis of lower and/or upper limbs, spinal cord injury may also affect respiratory function and may result in chronic respiratory insufficiency.2 Respiratory insufficiency is due to paresis or paralysis of the respiratory muscles and is dependent on the level and completeness of the lesion.3,4 More in particular for the quadriplegic patient, alterations in mechanical properties of the lung and of the chest wall occur and result in paradoxical movement of the chest wall and reduced lung and chest wall compliance.5–7 This results in a decreased efficiency of breathing, a reduction in maximal static respiratory pressures and in reduced pulmonary volumes.3,4,8–11 Moreover, decreased ability to sigh, ineffective coughing and development of mucus hypersecretion will result in inadequate clearance of mucus.12 All of the foregoing factors contribute to high prevalence of mucus retention, atelectasis, pneumonia and respiratory failure.13,14 Indeed, respiratory complications in general and pneumonia in particular, still are the most common causes of death in persons with spinal cord injury, both in acute and chronic stages of injury.2,13–15
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1887 1888 1888 1888 1888 1888 1888 1888 1888 1889 1889 1889 1890 1890 1893 1893 1893 1894 1894 1894 1894 1894 1895 1895 1895
Impaired respiratory muscle function and increased risk of respiratory complications have been frequently mentioned as indication for respiratory muscle training (RMT) in persons with spinal cord injury.16–19 In addition, it is well established that persons with quadriplegia have a reduced physical capacity20 due to the loss of motor function in lower and/or upper limbs and the relatively inactive lifestyle associated with the injury.21 In addition, respiratory muscles might partake in non-ventilatory function during exercise.22 Therefore, it is assumable that exercise performance might benefit from RMT in persons with spinal cord injury. Stiller and Huff23 concluded in their review on RMT in subjects with quadriplegia that espiratory muscle strength and/or endurance improved. However, the lack of controlled studies did not exclude spontaneous recovery as the explanation for the improvements observed in the reviewed papers. Up to now, no meta-analysis of randomized controlled studies published in the last years was performed on the effectiveness of RMT in persons with spinal cord injury. The purpose of this paper was to systematically review findings of controlled studies of RMT in persons with spinal cord injury by means of a metaanalysis.
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Methods Study identification and selection A MEDLINE (National Library of Medicine, Bethesda, MD, USA) database was used for selection of the literature (from 1980 to November 2004), and relevant references from peer-reviewed articles were retrieved as well. The keywords used in the literature search were: (1) respiratory muscles and synonyms; (2) RMT or exercise and synonyms; (3) spinal cord injury (SCI), paraplegia or quadriplegia and synonyms. Reference lists of all articles obtained were considered and additional possible relevant studies were retrieved. Studies investigating the effects of RMT [weight resistive, flow resistive, flow independent (threshold pressure) or normocapnic hyperpnea] in persons with SCI were selected based on abstract. Further exclusion criteria were: (1) not written and available in English; (2) animal studies; (3) review papers; (4) studies with training programs that used glossopharyngeal breathing, abdominal binding, electrostimulation or functional electrostimulation, phrenic nerve pacing or general exercise training (e.g. arm cranking exercise). These criteria were applied by one reviewer (S.V.H.).
Methodological quality Non-controlled studies were excluded for analysis. Since results may be related to study methodological quality, a score for methodological quality was assigned to each study. Two independent reviewers (R.G. and S.V.H.) investigated controlled studies for methodological quality using a modification of the framework for methodological quality developed by Smith et al.24 and Lo ¨tters et al.25 (Table 1). Based on this review, a total score for methodological quality was calculated for each study, allowing to weight study results differentially. Disagreement between reviewers was resolved through re-analysis and discussion between the two reviewers.
Meta-analysis, effect-size and training effects A meta-analysis of studies evaluating the effects of RMT in subjects with SCI on respiratory muscle strength, endurance and pulmonary function was intended. Vital capacity and respiratory muscle strength and endurance were analyzed as primary outcome variables. Furthermore, the influence of RMT on the incidence of respiratory complications
S. Van Houtte et al. and/or exercise capacity and quality of life was investigated. In order to calculate the effect-size of each individual study and the weighted summary effectsize which could be obtained after weighting for sample size, authors of controlled papers were contacted to provide not-reported data.
Results Study identification and selection A total of 106 references were identified. Eightythree studies did not satisfy one or more of the specified inclusion criteria (Table 2). As shown in Fig. 1, 23 of those 106 references applied RMT. Fifteen studies were uncontrolled trials. In two of the 23 studies RMT was combined with a general exercise program (e.g. arm cranking exercise) which did not allow assessing the specific effects of RMT. Although Huldtgren et al.26 reported a control group; they did not provide follow-up data of the control group. Finally, six controlled trials were left for further analysis. After Stiller and Huff23 reviewed the literature in 1999, five additional studies investigated the effects of RMT in patients with spinal cord injury. Only two studies19,27 were controlled trials and consequently were kept for further analysis.
Methodological quality and study characteristics Four corresponding authors were contacted to provide additional data, but only one author27 was able to provide data on respiratory muscle strength, endurance and pulmonary function. Consequently, in three studies28–30 mean scores without associated standard deviation or only values expressed as percentage predicted were available. For that reason as well as the heterogeneity in outcome variables, the current data set was considered insufficient to perform an adequate meta-analysis and subsequently, a systematic review was performed. Methodological quality Table 3 presents the methodological quality as well as a summary of the six controlled papers. The methodological quality score varied between 15 and 29 (median 23) with a maximal feasible score of 40. The major methodological shortcomings were lack of adequate description of randomization procedure (median 0), lack of similarity of the
ARTICLE IN PRESS Respiratory muscle training in persons with spinal cord injury Table 1
1889
Criteria for methodological quality.24,25 Score
Randomization Randomization procedure described Randomization procedure not described
5 0
Similarity of groups Age, sex, lung function, PImax, lesion level
0/5y
Co-intervention Comparable frequency of visits Comparable number of intercurrent illnesses Comparable medication changes
0–5z
Masking Patients Therapist Researcher
0–5z
Compliance Training was supervised Home programme with reporting diary and periodic control visit Home programme with either diary or periodic control visit Compliance not measured
5 4 3 0
Outcome measures Validity and/or reliability mentioned or referred to Validity and/or reliability not mentioned or referred to
5 0
Exercise regime Adequate description of intensity, duration and frequency in both exercise and control group No adequate description of intensity, duration and frequency
5 0
Follow-up 90–100% follow-up 80–89% follow-up o 80% subjects accounted for Cannot tell
5 3 1 0
PImax: maximum static inspiratory pressure. Total score ¼ 40 points y 0 or 5. z 5 for 3 out of 3, 4 for 2 out of 3, 3 for 1 out of 3 and 0 for 0 out of 3.
co-intervention with the experimental intervention (median 0) and absence of (double) blinding procedures (median 0). Compliance, description of exercise regime and follow-up reached the highest scores (median 5, for all). In addition, all studies presented pre and post results, but only three out of six studies17,19,28 performed between groups statistical analysis. Study characteristics Table 3 presents a summary of six controlled studies on RMT in persons with spinal cord injury. Estenne et al.29 and Gounden17 performed resistive expiratory muscle training, whereas the four other studies19,27,28,30 applied resistive inspiratory muscle training. The total number of subjects (n ¼ 128)
in the six controlled trials were equally divided over the control and experimental group. There were 110 men and 18 women with a mean age of 32 years. All studies included persons with a quadriplegia (lesion level C3–C8) who were more than 3 months after injury. Only in the study of Liaw et al.19 subjects between 1 and 3.5 months after injury were included.
Effects of RMT Respiratory muscle strength In five out of six studies respiratory muscle strength was measured as inspiratory or expiratory mouth pressure or as pectorals muscle strength.29 Two
ARTICLE IN PRESS 1890 Table 2
S. Van Houtte et al. Reasons of exclusion for 83 papers with corresponding number of citations.
Reason exclusion
Number of papers
No spinal cord injury Not in English Animal studies Reviewy Glossopharyngeal breathing/neck breathing or training of accessory muscles (Functional) electrostimulation Phrenic nerve pacing General exercise training (e.g. arm cranking exercise, handbike exercise, etc.) Respiratory intervention, no training (e.g. effects of abdominal binder, abdominal loads, etc.)
5 6 3 11 11 10 15 7 21
Totality of reasons for exclusion
89
For each paper all relevant criteria were registered. Therefore the total number of exclusions exceeded the total number of papers. In case a paper was not available in English, this was the only criterion which was registered. y In case of a review, it was the only registered criterion.
106 papers were identified Excluded for one or more reasons: n = 83 See Table 2. Respiratory muscle training n = 23 Combination with general exercise program: n=2 Respiratory muscle training n = 21
Non- controlled studies: n = 15
Controlled studies: n=6
Figure 1 Flowchart with identified and excluded papers after literature search.
studies,19,28 both providing inspiratory muscle training, found a change for inspiratory mouth pressure which varied between 2% and 44% (median 29%) after RMT, whereas the change in the control group varied between 0% and 30% (median 24%). No statistically significant differences between groups were found. In addition, Uijl et al.27 did not observe any changes in inspiratory mouth pressure in treatment or control group. Two studies, one providing expiratory muscle training17 and another providing inspiratory muscle training,19 found an increase in expiratory mouth
pressure of 43% and 56%, respectively, whereas the change in the control group was 0% and 44%, respectively. Only Gounden17 showed a significant improvement for expiratory mouth pressure in the experimental compared to the control group. In addition, Estenne et al.29 found an increase of 55% in pectorals strength whereas the control group did not show any change. Respiratory muscle endurance Two studies,27,28 both providing inspiratory muscle endurance training, investigated the effects of RMT on respiratory muscle endurance. Although endurance performance improved in both studies in the experimental groups, between groups comparison revealed no statistical differences. Pulmonary function Vital capacity was measured before and after RMT in five studies (Fig. 2). Between groups comparisons only showed a significantly improved vital capacity for the experimental group in the Gounden17 study. Although Liaw et al.19 found a significant change (67%) for vital capacity in the experimental group, also the control group significantly improved (27%). No between groups differences were observed. Zupan et al.30 showed a significant improvement of 19% for vital capacity in the experimental and no improvement (0%) in the control group. No between groups comparisons were reported. Loveridge et al.28 and Uijl et al.27 did not observe any improvement in experimental and control group after RMT. Three studies investigated the effects of RMT on residual volume. Liaw et al.19 and Loveridge
MQ
15
25
16
Estenne et al.29
Gounden17
Liaw et al.19 E: n ¼ 10 C: n ¼ 10 C4–C7
E: n ¼ 20 C: n ¼ 20 C5–C8
E: n ¼ 6 C: n ¼ 6 C5–C8
# subjects, level of lesion E: pectoralis muscle training, 10 repetitive, submaximal, isometric contractions, initial load at 80% MVC, 5 days a week, 6 weeks C: no training, general rehabilitation measures E: progressive expiratory resistive loading on accessory muscles by means of Pflex muscle trainer, initial resistance was approximately 60% PEmax; 5–8 min at least 5 times a day, 6 days per week, 8 weeks C: no training, conventional therapy E: resistive inspiratory muscle training, 6 different levels of resistance, 15-20 min, twice a day, 7 days a week, 6 weeks C: no training, general rehabilitation program
Description of training program
VC, FVC, FEV1, PEF, TLC, RV, FRC, PImax, PEmax, Borgscale, VE, chest circumference measurements
VC, PEmax
Pectoralis muscle strength, ERV, RV
Outcome variables
Scores for methodological quality (MQ, max ¼ 40) and summary of controlled studies.
Study
Table 3
Respiratory muscle training in persons with spinal cord injury
C: VC 27% (S), FVC 27% (S), FEV1 31% (S) PEF 30% (NS), TLC 0% (NS), PImax 24% (S), PEmax 44% (S), Borgscale 10% (S), VE 29% (S) Between groups: TLC (S), Borgscale (S), VE (S)
E: VC 67% (S), FVC 50% (S), FEV1 31% (S), PEF 40% (S), TLC 21% (S), PImax 29% (S), PEmax 43% (S), Borgscale 22% (S), VE 18% (NS)
Between groups: no statistics to compare groups E: VC 34% (S), PEmax 56% (S) C: VC 0.1% (NS), PEmax 0.05% (NS) Between groups: VC (S), PEmax (S)
E: pect 55% (S), ERV 47% (S), RV 14% (S) C: pect 0% (NS), ERV 9% (NS), RV 0% (NS)
Effects of RMT
ARTICLE IN PRESS 1891
24
29
23
Loveridge et al.28
Uijl et al.27
Zupan et al.30
C4–C7
E: n ¼ 13 C: n ¼ 13
C3–C7
C: n ¼ 9
E: n ¼ 9
E: n ¼ 6 C: n ¼ 6 C6–C7
# subjects, level of lesion
E: maximal sustained inspirations, 20–30 min, twice a day, 6 days a week, 4 weeks Cy: no training, usual physiotherapy program
E: resistive inspiratory muscle training, initial resistance at 85% sustainable inspiratory pressure, 15 min, twice a day, 5 days a week, 8 weeks C: not mentioned E: target flow training, incentive flow meter with resistance, initial load 70% endurance pressure, 15 min, twice a day, 6 weeks Cy: sham training, no appreciable resistance
Description of training program
FVCz, FEV1
IVC, FEV1, FIV1, PImax, Pendu, RPendu, PO2 peak, VO2 peak, VEpeak
IC, FVC, TLC, RV, FRC, PImax, SIP, VT, Ti, Te
Outcome variables
Between groups: no statistics to compare groups
C: Pendu 18% (NS), RPendu 0% (NS), VO2 peak 0.03% (NS) Between groups: no statistics to compare groups E1: FVC 19% (S), FEV1 21% (S) C: FVC 0%, FEV1 0%
E: Pendu 31% (S), RPendu 19% (S), VO2 peak 11% (S)
E: PImax 44% (S), SIP 59% (S) C: PImax 30% (S), SIP 31% (S) Between groups: NS differences
Effects of RMT
Studies investigated the effects of respiratory muscle training (RMT) in subjects with spinal cord injury. Only variables with significant changes in experimental group and associated changes in control group were presented as effects of RMT. Values which were reported as % predicted, as ratio and chest circumference measurements were not presented here. y An experimental cross-sectional design. z Only non-assisted respiratory tests in sitting position were presented. Number of subjects (#), maximal score (max), experimental group (E), control group (C), maximal voluntary contraction (MVC), sustainable inspiratory pressure (SIP), vital capacity (VC), expiratory reserve volume (ERV), residual volume (RV), forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), forced inspiratory volume in 1 s (FIV1), peak expiratory volume (PEF), total lung capacity (TLC), functional residual capacity (FRC), inspiratory mouth pressure (PImax), expiratory mouth pressure (PEmax), Borgscale for resting dyspnea, ventilation (VE), inspiratory capacity (IC), tidal volume (VT), inspiratory time (Ti), expiratory time (Te), endurance pressure (Pendu), ratio between Pendu and PImax (RPendu), peak power output (POpeak), peak oxygen consumption (VO2 peak), peak expiratory minute ventilation (VEpeak), Pflex ventilatory muscle trainer (Health Scan Medical Apparatus), significant difference (S), no significant difference (NS).
MQ
Study
Table 3 (continued )
ARTICLE IN PRESS
1892 S. Van Houtte et al.
ARTICLE IN PRESS Respiratory muscle training in persons with spinal cord injury Experimental group 4 3.5
120 *
VC (liter)
3
100
2.5 80 2 1.5
# 60
* *
40
1
20
0.5 0
VC (%predicted or % initial value)
140
0 before
in favor of the experimental group. Although Liaw et al.19 mentioned cough evaluation in their method section, no further data were provided. Furthermore, Zupan et al.30 reported that seven patients found breathing easier during training periods. Two patients experienced more spasms and had increased sputum production. Finally, only one study27 investigated the effects of RMT on exercise performance. Uijl et al.27 found that peak oxygen consumption during an incremental maximal arm-cranking exercise test significantly improved with 11% after RMT, whereas sham training showed no difference (0%). Between groups comparison was not performed.
after
Gounden
Liaw
Loveridge°
Uijl Zupan°
Discussion
4
140
3.5
120
3
100
2.5 80 2 *
60
1.5 40
1
20
0.5 0
VC (%predicted or % initial value)
Control group
VC (liter)
1893
0 before Gounden Loveridge°
after Liaw
Uijl Zupan°
Figure 2 Vital capacity in experimental and control group before and after respiratory muscle training.
et al.28 provided inspiratory muscle training and found no changes in residual volume. The experimental groups changed with 0% and 15%, respectively, whereas the control groups changed with—17% and 0.5%, respectively. Only Estenne et al.29 providing expiratory muscle training, showed a significant decrease of 14%, whereas the control group did not change (0%). However, between groups comparisons were not performed. Respiratory complications, quality of life, exercise performance Only Liaw et al.19 objectively measured the effect on dyspnea. Borg score for resting dyspnea decreased with 22% and 10% in experimental and control group, respectively. Between groups statistical comparison revealed a significant difference
This is the first systematic review based on controlled trials and a methodological framework to analyze the efficacy of RMT in persons with spinal cord injury. A MEDLINE search revealed only six controlled studies with moderate methodological quality. Unfortunately, a limited number of randomized controlled trials, unreported data and heterogeneity in outcome variables hampered interpretation of findings. Consequently, it was impossible to calculate effect sizes and to perform a meta-analysis. Nevertheless, based on the current findings, tendencies for improved expiratory muscle strength, vital capacity and decreased residual volume after RMT were observed. Insufficient data were available to provide conclusions on the effects of RMT on quality of life, exercise performance and respiratory complications.
Methodological quality and study characteristics Methodological quality scores of the six studies in the present review were in line with scores reported by Lo ¨tters et al.25 in patients with chronic obstructive pulmonary disease. Although previous reviews already have proven the validity and value of this methodological framework,24,25 it is obvious that other parameters such as the duration of the training, the training modality as well as an adequate selection of outcome variables will also determine the quality of a study. Moreover, between group statistical analysis and power analysis were not included as criteria for methodological quality. We consider the lack of between group statistical analysis in three27,29,30 of the six studies and absence of power analysis in all studies as methodological weaknesses. Finally, the
ARTICLE IN PRESS 1894 relatively low incidence, the severity of the injury and the distribution across different rehabilitation centers of persons with an acute spinal cord injury might explain the small sample size of the studies.
Effects of RMT The main training effects of the reviewed papers will be discussed in perspective of differences in training modality, intensity and methodological quality. Respiratory muscle strength Across the three controlled trials which investigated inspiratory muscle strength (see Table 3), surprisingly, no consistent effect of RMT was found. One study27 with the highest score for methodological quality (29) did not observe any effect, whereas two studies19,28 of lower methodological quality (score 22 and 16, respectively) found similar significant changes for experimental and control group. These findings are in contrast with the significant improvements for inspiratory muscle strength following overall analysis of 15 studies in the meta-analysis by Lo ¨tters et al.25 on inspiratory muscle training in patients with chronic obstructive pulmonary disease. The review of Smith et al.24 concerning RMT in patients with chronic airflow limitation strongly suggested that specific training effects were related to the type (inspiratory or expiratory resistive breathing) of muscle training. Indeed, Uijl et al.27 used a target flow endurance training of the inspiratory muscles at an initial load of 70% endurance pressure, explaining that respiratory muscle strength in that study was not affected. Gounden17 (methodological quality of 25) showed a significant improvement for expiratory muscle strength in the experimental group (expiratory muscle training) compared to the control group, also underlining the specificity of the training response. Similarly, pectorals muscle strength significantly improved in the experimental group of the study of Estenne et al.29 Changes in inspiratory or expiratory lung volumes might have contributed to improved expiratory or inspiratory mouth pressures, respectively, none of the studies controlled for this. Respiratory muscle endurance Only two controlled studies27,28 (methodological quality of 24 and 29, respectively), included a measure of respiratory endurance (see Table 3), but did not observe between group differences. An explanation for the lack of significant differences might be the small sample sizes and therefore lack
S. Van Houtte et al. of power of the studies. Alternatively, adequate training intensity controlled with diaphragm electromyography assured induction of respiratory fatigue during each training session of resistive breathing in the uncontrolled trial of Gross et al.18 They found significant improved respiratory muscle endurance in a sample of six patients with a cervical spinal cord injury. Lo ¨tters et al.25 reported significantly improved respiratory muscle endurance after overall analysis of seven studies in patients with COPD. Pulmonary function Five studies17,19,27,28,30 with a methodological quality ranging between 16 and 29 (see Table 3), reported effects of RMT on vital capacity. Only, Gounden17 found an improved vital capacity in favor of the experimental group. This is in contrast with the results of the meta-analysis of Lo ¨tters et al.25 who did not find any significant change of pulmonary function in patients with chronic obstructive pulmonary disease. Differences in population characteristics may explain this contradiction. Pulmonary function in SCI is mainly limited by the weakness of respiratory muscles, whereas in patients with chronic obstructive pulmonary disease airway obstruction is the main reason for impaired pulmonary function. Therefore, training of the remaining respiratory muscles in SCI and the use of compensatory respiratory mechanisms, such as m. pectorals function for expiration29 may improve pulmonary function. Consequently, the improved expiratory muscle strength in the study of Gounden17 could have lowered end-expiratory lung volume and thus increased vital capacity. However, end-expiratory lung volume was not measured in the study. Estenne et al.29 providing expiratory muscle training, showed an improved residual volume (i.e. decrease) in the experimental group (see Table 3) as well as improved pectorals muscle strength. This observation underlines the specificity of training as well. Respiratory complications, quality of life and exercise performance Although subjects with SCI have an impaired pulmonary function3,4,8–10 and are at higher risk for respiratory complications2,13–15 and mortality,2,15 only one study19 reported changes in resting dyspnea. Also in patients with chronic obstructive pulmonary disease RMT already resulted in relieve of dyspnea and improved quality of life.25 Since respiratory complications are important events in patients with spinal cord injury, efficacy of cough should be an important target for RMT. Increased expiratory pressure will increase driving pressure
ARTICLE IN PRESS Respiratory muscle training in persons with spinal cord injury for forced expiration, while improved inspiratory muscle strength will enhance inspiratory volume and thus will also contribute to driving pressure for expiration. In their meta-analysis, Lo ¨tters et al.25 did not find a significant additional effect on functional exercise capacity. To which extent improved respiratory strength and endurance in persons with SCI can be transferred to an improved exercise performance and quality of life remains to be elucidated.
10. 11.
12.
13.
14.
Conclusion 15.
Trends for improvement following respiratory muscle training were observed for expiratory muscle strength, vital capacity and residual volume, whereas not sufficient support is available for improved inspiratory muscle strength and endurance. Insufficient data was available to provide conclusions on the effects on quality of life, respiratory complications and exercise performance. Further randomized controlled trials should clarify these issues.
Competing interests
16.
17.
18.
19.
20.
The authors declare that they have no competing interests.
21.
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