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

MethodsRCT

Randomisation method: table of random numbers


Participants11 acute inpatients with C4-C7 complete quadriplegia (9 males, 2 females), aged 16-41 years, USA


InterventionsInspiratory resistance muscle training (continuous for 15 min/day) vs. abdominal weights training (10 breaths x 4). The inspiratory resistance group initially trained with least amount of resistance. Resistance increased when participant was able to complete 3 consecutive sessions of continuous breathing for 15 min. Abdominal weights training used the maximum weight that did not alter IC and required 4 x 10 maximal inspirations, holding each breath for several seconds.

Training intensity: 2 x daily (5 days/week) for 7 weeks


OutcomesFVC, MVV, PEFR, PImax (also known as MIP), and IC were measured pre and post intervention


NotesNo 'control' group, likely post randomisation withdrawal not reported


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskTable of random numbers used

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
High risk40 participants met admission criteria, but only 11 full sets of data reported (dropout rate of 73%)

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Gounden 1990

MethodsRCT

Randomisation method: not specified


Participants40 inpatients and outpatients with C5-C7 quadriplegia (32 males, 8 females), aged 16-64 years, South Africa


InterventionsExpiratory muscle training (progressive resistive loading) vs. no training. Experimental group trained using the PFLEX Inspiratory Muscle Trainer® and expired against a resistance set at 60% of maximal expiratory mouth pressure

Training intensity: 5-8 min x 5 daily (6 days/week) for 8 weeks


OutcomesMEP, VC


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
Low riskNo dropouts reported

Selective reporting (reporting bias)Low risk

Liaw 2000

MethodsRCT

Randomisation method: not specified


Participants20 inpatients with C4-C7 complete quadriplegia at least 6 months post injury (16 males, 4 females), aged 16-52 years, Taiwan


InterventionsResistive inspiratory muscle training vs. usual care. Initially trained with at lowest resistance setting. Resistance level increased when participant able to complete 3 consecutive sessions of continuous breathing

Training intensity: 15-20 min x 2 daily (12-16 breaths/min) for 6 weeks


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
High risk30 participants recruited, but 10 dropped out. Outcome data only presented for the 20 participants who completed the study (dropout rate of 33%)

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Litchke 2008

MethodsRCT with block randomisation (matched by lesion level or track rating, or both)

Randomisation method: not specified


Participants9 wheelchair athletes with C5-T12 SCI (1 neuro disorder, 1 postpolio). All males aged 21-49 years, USA


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

Training intensity: (set of 10) 3 x daily for 10 weeks


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


NotesOnly 5 of 9 subjects fit inclusion criteria for this review


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
High riskData not reported for 1 participant who withdrew from the study (dropout rate of 11%)

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Litchke 2010

MethodsRCT

Randomisation method: not specified


Participants16 wheelchair athletes with C5-C7 quadriplegia (11 complete, 11 incomplete, 1 spastic cerebral palsy, 1 congenital deformities). All male, aged 18-50 years, USA


InterventionsConcurrent flow resistance (1 set of 10 breaths) vs. concurrent pressure threshold resistance (3 sets of 10 breaths) vs. no training. The flow resistance training consisted of inhaling slowly and deeply through the concurrent flow resistance device, holding breath for 2-5 seconds, exhaling until almost out of air, then forcefully blowing out as much of the remaining residual air as possible. This sequence was repeated up to 10 times with 10-20 seconds of rest between each sequence

The pressure resistance training consisted of inhaling fully and forcefully through the concurrent pressure resistance device for 3 seconds (completely filling the lungs), holding breath for 1-2 seconds, exhaling fully and forcefully through the device (completely emptying the lungs), and pausing for 1-2 seconds. For both conditions, respiratory resistance was increased by 1 level when able to complete 1 set of 10 without experiencing respiratory fatigue, dizziness, or light-headedness

Training intensity: 3 times daily for 9 weeks


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
High riskData reported only for 16 participants who completed the study (24 were initially recruited) - dropout rate of 33%

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Loveridge 1989

MethodsRCT

Randomisation method: not specified


Participants12 outpatients with C6-C7 complete quadriplegia, aged 22-49 years, Canada


InterventionsInspiratory resistance training vs. no treatment. Participants trained with an inspiratory resistance device at 85% of their SIP at normal resting flow rates

Training intensity: 15 min twice daily (5 days/week) for 8 weeks


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
Low riskNo dropouts reported

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Mueller 2013

MethodsRCT


Participants24 participants with C5-C8 complete quadriplegia, aged 22-58 years, Switzerland


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

Training intensity: 4 x 10 min/week for 8 weeks


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

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

Incomplete outcome data (attrition bias)
All outcomes
High risk2 dropouts reported

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Roth 2010

MethodsRCT

Randomisation method: based on medical record number


Participants29 acute inpatients with C4-T1 complete SCI < 6 months post injury (22 males, 7 females), aged 16-60 years, USA


InterventionsExpiratory muscle resistance training vs. sham. The training group exhaled quickly and forcefully through a high-pressure gauge providing resistance to expiration. The sham group exhaled forcefully through the same device but with no pressure gauge and thus no resistance. Each participant performed 10 repetitions without resting between breaths

Training intensity: 2 x 10 repetitions daily (5 days/week) for 6 weeks


OutcomesFVC, FEV1, MEP, MIP, IC, ERV, TLC, FRC, and RV were measured pre and post intervention


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Low riskThe randomisation allocations were made by an investigator who had no contact with any of the subjects and who had no knowledge of the any of the subjects' demographic or injury characteristics

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

Incomplete outcome data (attrition bias)
All outcomes
High riskData reported only for 29 participants who completed the study (52 were initially recruited) - dropout rate of 42%

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Tamplin 2013

MethodsRCT with block randomisation (matched by history of tracheostomy)

Randomisation method: computer-generated table of random numbers


Participants24 participants with C4-C8 quadriplegia (ASIA A or B), aged 27-70 years, Australia


InterventionsSinging training vs. music appreciation. Singing training included oral motor and respiratory exercises, vocal warm-ups, and singing familiar songs. Music appreciation included song sharing and discussion, musical games, and music-assisted relaxation

Training intensity: 1 hour daily (3 days/week) for 12 weeks


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskComputer-generated randomisation sequence

Allocation concealment (selection bias)Low riskRandomised sequence concealed in sealed, opaque envelopes

Blinding (performance bias and detection bias)
All outcomes
Low riskParticipants blinded to which intervention was the experimental condition. Assessors blinded to group allocation

Incomplete outcome data (attrition bias)
All outcomes
Low riskNo dropouts reported

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Van Houtte 2008

MethodsRCT with block randomisation (match by lesion level)

Randomisation method: not specified


Participants14 acute inpatients with C4-T1 SCI (ASIA A, B, or C) at least 6 weeks, but < 6 months post injury (12 males, 2 females), aged 17-66 years, Belgium


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

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


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


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Low riskBoth participants and assessors blinded to group allocation

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

Incomplete outcome data (attrition bias)
All outcomes
Low riskNo dropouts reported

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

Zupan 1997

MethodsRCT (cross-over design)

Randomisation method: not specified


Participants13 inpatients with C4-C7 quadriplegia (10 complete, 3 incomplete) (11 males, 2 females), aged 17-46 years, Slovenia


InterventionsInspiratory muscle training (incentive spirometry) vs. expiratory muscle training + electrical stimulation vs. control (no training). For inspiratory muscle training the participants were instructed to inhale slowly to maximum value on the incentive spirometer and attempt to hold the breath at 75% of this value for as long as possible. For expiratory muscle training the participants were instructed to inhale slowly, hold the breath, and then attempt to achieve maximal expiration on a peak flow meter (twice without electrical stimulation of the abdominal muscles and 8 times with electrical stimulation) and blow bubbles through a thin straw for 3 min

Training intensity: 7 exercises x 10 sets twice daily (6 days/week) for 4 weeks


OutcomesFVC and FEV1 (sitting and lying) were measured at baseline and monthly for 3 months. FVC and FEV1 were measured under 4 conditions: unassisted, manual assistance, electrical simulation (patient), and electrical stimulation (therapist)


Notes


Risk of bias

BiasAuthors' judgementSupport for judgement

Random sequence generation (selection bias)Low riskRandom group assignment

Allocation concealment (selection bias)Unclear riskNot reported

Blinding (performance bias and detection bias)
All outcomes
Unclear riskNot reported

Incomplete outcome data (attrition bias)
All outcomes
Low riskNo dropouts reported

Selective reporting (reporting bias)Low riskResults presented for all original variables recorded

 
Characteristics of excluded studies [ordered by study ID]

StudyReason for exclusion

Alvarez 1981Not an RCT, no RMT intervention

Biering-Sorensen 1991Not an RCT, no control group, pre-post study

Crane 1994Not an RCT, exercise training with retrospective sample

Ehrlich 1999Not an RCT, case study

Epifanov 1987Not an RCT, not quadriplegia

Estrup 1986Not an RCT

Fugl-Meyer 1972Not an RCT

Gallego 1993Not an RCT

Goosey-Tolfrey 2010Not an RCT, not quadriplegia

Gross 1980Not an RCT

Hornstein 1986Not an RCT

Imamura 1967Not an RCT

Lee 2012Poor description of the expiratory muscle training makes it is difficult to understand if it would have added to the effect of the mechanical in-exsufflation (which would be expected to be large). Randomisation order was determined by hospital admission, therefore, no allocation concealment and high potential for bias. Also, no indication of when the lung volume measures were made

Lerman 1987Not an RCT

Lin 1999Not an RMT, no training intervention

Lin 2001Not an RCT

Metcalf 1966Not an RCT

Moreno 2012Not an RCT

Moreno 2013Not an RCT

Nygren-Bonnier 2009Not an RCT

Rutchik 1998Not an RCT

Sapienza 2006Not an RCT

Sutbeyaz 2005Not an RCT, not quadriplegia

Uijl 1999Not an RCT, cross-over design, but not randomised

Valent 2009Not an RCT, no control group, pre-post study, not RMT intervention

Walker 1987Not an RCT

Wang 2002Not an RCT

 
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]

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

StudyTest positionBinderVital capacityMIPMEPFEV1

Derrickson 1992Supinen/aX

Gounden 1990Supine and sitting?XX

Liaw 2000Supinen/aXXXX

Litchke 2008Sitting?X

Litchke 2010Sitting?X

Loveridge 1989Sitting?X

Mueller 2013SittingnoXXXX

Roth 2010Sitting?XXX

Tamplin 2013SittingnoXXXX

Van Houtte 2008Sitting?XX

Zupan 1997Supine and sitting?X

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