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Resistive Inspiratory Muscle Training in People With Spinal Cord Injury During Inpatient Rehabilitation: A Randomized Controlled Trial

Karin Postma, Janneke A. Haisma, Maria T.E. Hopman, Michael P. Bergen, Henk J. Stam, Johannes B. Bussmann
DOI: 10.2522/ptj.20140079 Published 1 December 2014

Abstract

Background People with spinal cord injury (SCI) may benefit from resistive inspiratory muscle training (RIMT). Current evidence is weak, and little is known about the effect on functional outcomes and long-term effects.

Objective The purpose of this study was to assess immediate and long-term effects of RIMT in people with SCI.

Design This was a single-blinded randomized controlled trial.

Setting The study was conducted at 4 specialized SCI units in the Netherlands.

Patients The study participants were 40 people with SCI (15 with motor complete tetraplegia, 16 with incomplete tetraplegia, 8 with motor complete paraplegia, and 1 with incomplete paraplegia) who had impaired pulmonary function and were admitted for initial inpatient rehabilitation.

Intervention Study participants were randomized to an RIMT group or a control group. All participants received usual rehabilitation care. In addition, participants in the intervention group performed RIMT with a threshold trainer.

Measurements Measurements were performed at baseline, after 8 weeks of intervention, 8 weeks later, and 1 year after discharge from inpatient rehabilitation. Primary outcome measures were: respiratory muscle function, lung volumes and flows, and perceived respiratory function. Secondary outcome measures concerned patient functioning, which included health-related quality of life, limitations in daily life due to respiratory problems, and respiratory complications.

Results During the intervention period, maximum inspiratory pressure (MIP) improved more in the RIMT group than in the control group (11.7 cm H2O, 95% confidence interval=4.3 to 19.0). At follow-up, this effect was no longer significant. No effect on other primary or secondary outcome measures was found except for an immediate effect on mental health.

Limitations The sample size was insufficient to study effects on respiratory complications.

Conclusions Resistive inspiratory muscle training has a positive short-term effect on inspiratory muscle function in people with SCI who have impaired pulmonary function during inpatient rehabilitation.

In most people with acute spinal cord injury (SCI), respiratory function is seriously impaired. Even though partial recovery takes place during the first year after onset, many people continue to have respiratory impairments (eg, weak respiratory muscle strength, low lung volumes and flows, ineffective cough) and, consequently, elevated risk of respiratory complications.1–6

Traditionally, respiratory management in people with SCI has focused on ventilation-independent breathing and the prevention of respiratory complications such as secretion retention, atelectasis, and lower respiratory tract infection.7,8 It has been postulated that improvement of inspiratory muscle strength through specific training in people with SCI may result in greater improvement of pulmonary function and cough capacity during initial recovery and may lower the risk of excessive decline in pulmonary function and respiratory complications in the chronic phase.9–11 Resistive inspiratory muscle training (RIMT) has been shown to increase inspiratory muscle function, lung volumes, and exercise capacity in people who are healthy12,13 and has been shown to be effective in several patient populations.14–18 In people with SCI, a recent meta-analysis, reported in 2 publications,19,20 showed that respiratory muscle training can improve respiratory muscle strength and possibly vital capacity. However, in this meta-analysis, only 3 studies concerned clinical trials studying the effects of RIMT. These studies were characterized by small sample sizes (N=12–20), and the results are conflicting.21–23 In addition, these studies included only people with complete tetraplegia, although it can be expected that problems with impaired respiratory function also may be present in people with incomplete tetraplegia or thoracic lesions.3 Furthermore, as in other types of respiratory muscle training, it is unknown whether effects of RIMT are sustained over time and result in long-term functional benefit.

The objective of the present study was to assess the immediate and long-term effects of RIMT in addition to usual rehabilitation care, as compared with usual care alone, on respiratory function (respiratory muscle strength, lung volumes and flows, and perceived respiratory function) in people with SCI who have impaired pulmonary function. In addition, we studied the effects of RIMT on measures of patient functioning (health-related quality of life [HRQoL], limitations in daily life, and of respiratory complications).

Method

Design Overview

This study was a single-blinded multi-center randomized controlled trial, in which the effects of an added intervention (RIMT group) were compared with usual care (control group). The study was prospectively registered at the Dutch trial register (NTR1921).

Setting and Participants

This trial was carried out at 4 rehabilitation centers with specialized SCI units in the Netherlands. Recruitment started in October 2009 in 3 centers, and as the inclusion rate was slow, a fourth center was added in June 2011. Inclusion criteria were: people with SCI admitted for initial inpatient rehabilitation; motor level T12 or higher; American Spinal Injury Association Impairment Scale (AIS) grade A, B, C, or D24; age 18 to 70 years; and impaired pulmonary function. Impaired pulmonary function was defined as forced expiratory volume in 1 second (FEV1) below 80% of the predicted value. Exclusion criteria were: progressive diseases, a psychiatric condition that interfered with constructive participation, insufficient comprehension of the Dutch language, medical instability, ventilator dependency, and the presence of tracheostomy. All participants gave written informed consent.

Randomization and Interventions

For each center, a randomization schedule for 2 separate arms (arm A for people with FEV1 below 60.0% of the predicted value and arm B for people with FEV1 between 60.0% and 79.9% of the predicted value) was computer generated. The randomization schedules were constructed with blocks of 2 to ensure equal distribution across the RIMT group and the control group. The allocation sequence was concealed by using consecutively numbered, sealed envelopes. After the baseline measurement, a physical therapist working at the SCI unit opened the first numbered envelope of the corresponding arm containing the group allocation. None of the individuals involved in the allocation were aware of which method was used to construct the randomization schedules. This blinding, together with the separate randomization schedules for 2 separate arms, ensured that the allocation sequence was concealed until opening the envelope.

The study was set up as a pragmatic trial. The intervention started 5 weeks after the start of active inpatient rehabilitation (defined as out of bed for at least 3 consecutive hours). All participants received usual care (including passive range of motion, muscle strength exercises, and functional training) and 2 standardized educational lessons on general aspects of respiratory function and respiratory complications. People allocated to the RIMT group trained 8 weeks with an IMT Threshold trainer (Threshold IMT, Respironics Inc, Parsippany, New Jersey), 5 times a week, according to an interval-based, high-intensity protocol. This protocol was found to be feasible25 and effective26 in people with chronic obstructive pulmonary disease (COPD). The intended load at the start of the training was 60% of maximum inspiratory pressure (MIP) at baseline. Each training session consisted of 7 sets of 2 minutes of breathing through the Threshold trainer followed by 1 minute of unresisted breathing. To get acquainted with the training, sets were increased from 3 to 7 in the first week. At each center, one physical therapist employed at the SCI unit and instructed verbally and in writing was responsible for the execution of the protocol. This therapist evaluated the training and increased the threshold load once a week. Other training sessions were planned as part of the overall rehabilitation program and supervised (throughout each training session) by an assistant. For all training sessions during the intervention period, duration and intensity were recorded in a logbook. In addition, the intervention was subjectively evaluated with a written questionnaire at the end of the intervention period. After completion of the intervention period, participants in the RIMT group were advised by the therapist to continue RIMT. Whether participants continued training was determined retrospectively by written questionnaires at set time points: 8 weeks after the intervention period and 3, 6, 9, and 12 months after discharge from inpatient rehabilitation.

Outcome Measures and Follow-up

Measurements were performed in the week before the start of the intervention period (baseline: T0), within 1 week after the intervention period (T1), 8 weeks after T1 (T2), and 1 year after discharge of inpatient rehabilitation (T3). All measurements, with the exception of respiratory complications, were performed by a research assistant who was not involved in treatment of the participant and not aware of the group allocation. Lesion characteristics, secondary complications, and comorbidity were recorded by the attending physician at all measurement occasions. Motor loss and sensory loss were scored according to the Dutch translation of the International Standards for Neurological Classification of Spinal Injury developed by the American Spinal Injury Association (ASIA).24

Primary outcome measures of this study were objective and subjective measurements of respiratory function. Respiratory muscle strength was determined by MIP (also known as PImax) and maximum expiratory pressure (MEP, also known as PEmax), both measured at the mouth with the MicroRPM (CareFusion, Basingstoke, United Kingdom) using a flanged mouthpiece and expressed in cm H2O.27,28 Maximum inspiratory pressure was measured after full expiration, and MEP was measured after full inspiration. Maximum pressure had to be maintained for at least 1 second. The highest value of 8 maneuvers that varied less than 5% from the next value was recorded and used for analysis. Lung volumes and flows were measured with a spirometer (Oxycon Delta, CareFusion, Hoechberg, Germany). Forced vital capacity (FVC), FEV1, and peak expiratory flow (PEF) were measured according to the American Thoracic Society standards modified for people with SCI.29,30 Three to 5 repeated flow volume curves were performed. Outcomes of the best trial (the trial with the highest sum of FVC and FEV1) were used for analysis. Maximum ventilation volume (MVV), a measure of respiratory muscle endurance, was measured during 12 seconds of maximal deep inspiration and expiration at a set pace of 60 breaths per minute.27 The pace was controlled using a metronome, and the highest value of 3 maneuvers was used for analysis. To establish cough capacity, participants were asked to cough as forcefully as possible after full inspiration.31 The highest value of 8 maneuvers that varied less than 5% from the next value was recorded as peak cough flow (PCF) and used for analysis.

All measures of objective respiratory function were determined with participants seated in their own wheelchair, using a noseclip, and with abdominal binders (if present) removed. Perceived respiratory functioning was assessed with a questionnaire. Participants were asked to what extent they experienced limitations with breathing (when sitting quietly, positioned supine, or during exercise), talking (when speaking loudly, in long sentences, or more than a few minutes), and coughing and clearing one's nose on a numeric visual analog scale (0=no effort, 10=not possible). A mean score (0–10) for the breathing, talking, and cough/sneeze function was calculated; higher scores reflect worse functioning.

Secondary outcome measures concerned different aspects of patient functioning: HRQoL, perceived limitations in daily life, and respiratory complications. Three subdomains of HRQoL—perceived general health, mental health (psychological functioning), and vitality (energy and fatigue)—were measured with the corresponding subscales of the 36-Item Short-Form Health Survey questionnaire (SF-36).32 In each subscale, scores were added and transformed to a score of 0 (lowest) to 100 (highest). High scores reflect better HRQoL. The SF-36 has been proven to be reliable and valid in people with SCI.33,34 Furthermore, participants reported to what extent they felt limited in daily life due to respiratory problems on a 7-point scale (1=not at all, 7=completely limited). The incidence of respiratory complications within the first year after discharge of inpatient rehabilitation was assessed in 2 ways. One year after discharge (at T3), the physician registered whether the person had received treatment for respiratory complications during the previous year (physician-reported respiratory complications). In addition, participants were asked by written questionnaire, every 3 months after discharge, whether they had had any increased breathlessness, increased phlegm, fever due to respiratory infection, or other respiratory problems (patient-reported respiratory complications).

Data Analysis

The sample size was determined with a power analysis based on FVC. Given this outcome measure, an expected additional treatment effect of 10%, a standard deviation of 12%, a power of 80%, a significance level of .05, and a 10% dropout rate, we calculated that 20 patients in each group were needed.

To test the potential effect when performing RIMT, a per-protocol analysis was used. Per-protocol analysis was chosen above intention-to-treat analysis to allow clinicians to offer this intervention based on the estimated actual effect (effect of people who follow the training) as opposed to the estimated effect in a group of people who were offered the treatment. Only participants who adhered to the protocol and performed at least one follow-up measurement were included in the analysis. Center-specific effects were not of interest for this trial; therefore, the data of participants from each center were pooled. Generalized estimating equation analysis was used to determine the between-group differences. The measurement occasion (as the factor time), group (RIMT or control), and time × group interaction were added to the model as independent variables. The group variable represents the between-group differences and thus the intervention effect. Baseline values were added to the model as covariates to control the intervention effect for baseline differences. By changing the sequence of the factor time, effects at different follow-up periods were calculated: short term (T0–T1), medium term (T0–T2), and long term (T0–T3). Limitations in daily life and respiratory complications were described in numbers and percentages. All statistical analyses were performed with IBM SPSS version 20 (IBM Corp, Armonk, New York), and level of significance was set at P<.05.

Role of the Funding Source

This study was supported by the Kinderrevalidatie Fonds Adriaanstichting (grant no. 2007/0179-063).

Results

Study Population

The first person enrolled in the trial on October 1, 2009, and the last person enrolled on July 7, 2012. Figure 1 is a flow diagram of study participation from enrollment to analysis. After randomization, 2 people were excluded because of psychiatric conditions, 1 person discontinued the training due to decline in overall function, and 1 person was not available for the follow-up measurements.

Figure 1.
Figure 1.

CONSORT flow diagram of study participation from enrollment to analysis. RIMT=resistive inspiratory muscle training. Asterisk indicates data missing for 2 participants.

The study group (n=40) consisted of 35 men (87.5%) and 5 women (12.5%), and the mean age at baseline was 46.8 years (SD=14.3). Fifteen participants had motor complete tetraplegia, 15 had incomplete tetraplegia, 9 had motor complete paraplegia (lowest level [T9]), and 1 had incomplete paraplegia (T7). Table 1 presents the personal and lesion characteristics for the RIMT group and control group at baseline. By chance, all participants with concomitant respiratory diseases (2 had asthma, and 4 had COPD) were allocated to the control group.

View this table:
Table 1.

Characteristics at Baseline for the RIMT Group and Control Groupa

Training

On average, 39 training sessions (SD=4, range=30–47) were performed by the RIMT group during the intervention period. The mean training load increased from 50% (SD=15%) to 77% (SD=33%) of baseline MIP. Six participants achieved the maximum possible resistance of the Threshold trainer (41 cm H2O) before the end of the intervention period and continued to increase the training dose by lengthening the time breathing against resistance and shortening the time without resistance. Eight participants continued training at a regular base (2–3 times a week) at least until 8 weeks after the intervention period, and some continued several months after discharge from inpatient rehabilitation. Nobody continued training during the full follow-up time.

Effects of RIMT

Table 2 presents the respiratory function and HRQoL at all measurement occasions. Generalized estimating equation analysis showed significant improvement over time in all parameters except for the subdomains of HRQoL for the entire study group. During the intervention period, the RIMT group showed greater improvement in MIP compared with the control group (Tab. 3). This between-group difference was partially sustained but was no longer statistically significant at follow-up. The change in MIP over time for the RIMT group and the control group is graphically presented in Figure 2. Additional exploratory analyses indicated that MIP improved over a longer period in participants who continued RIMT after the intervention period compared with those who discontinued RIMT (Fig. 3). In none of the other measures of respiratory function were between-group differences found.

View this table:
Table 2.

Descriptive Results for the RIMT Group and Control Groupa

View this table:
Table 3.

Mean Differences in Change Between the RIMT Group and Control Group at Short-Term, Medium-Term, and Long-Term Follow-upa

Figure 2.
Figure 2.

Change of maximum inspiratory pressure (in cm H2O) over time in the resistive inspiratory muscle training (RIMT) group and control group, based on (A) generalized estimating equation analysis and (B) raw data (mean and standard error of the mean). T0=baseline (measurements performed in the week before the start of the intervention period), T1=1 week after the intervention period, T2=8 weeks after T1, T3=1 year after discharge from inpatient rehabilitation.

Figure 3.
Figure 3.

Change of maximum inspiratory pressure (in cm H2O) over time in 2 subgroups within the resistive inspiratory muscle training (RIMT) group, based on (A) generalized estimating equation analysis and (B) raw data (mean and standard error of the mean). T0=baseline (measurements performed in the week before the start of the intervention period), T1=1 week after the intervention period, T2=8 weeks after T1, T3=1 year after discharge from inpatient rehabilitation.

With the exception of mental health, no between-group differences were found for secondary outcome measures. The RIMT group showed greater improvement in mental health compared with the control group after the intervention period. In both groups, the number of participants who perceived limitations in daily life (“very little” to “fully”) decreased similarly over time (in the RIMT group, the incidence was 68% at T0, 32% at T1, 44% at T2, and 36% at T3; in the control group, the incidence was 62% at T0, 33% at T1, 50% at T2, and 33% at T3). Physicians reported respiratory complications in 3 participants in the RIMT group (upper respiratory tract infection, pneumonia, and nocturnal dyspnea) and in 2 participants in the control group (upper respiratory tract infection and nocturnal dyspnea) during the year after inpatient rehabilitation. In addition, 6 participants in the RIMT group and 7 participants in control group reported increased breathlessness, increased phlegm, fever due to respiratory infection, or other respiratory problems.

Discussion

In the present randomized clinical trial, we studied the effect of an added RIMT program, as compared with the usual inpatient rehabilitation care alone, in people with SCI who have impaired pulmonary function. In addition to the effect on respiratory function, we also studied the effect on several aspects of patient functioning. To our knowledge, this is the first study concerning RIMT in which long-term effects and the effect on respiratory complications were studied. Resistive inspiratory muscle training had an immediate positive effect on MIP, but this effect was no longer significant after long-term follow-up. No effects on other parameters of respiratory function were found. With exception for an immediate effect on mental health, we found no effect on other measures of patient functioning (HRQoL, limitations in daily life due to respiratory problems, or the incidence of respiratory complications).

We found positive effects of RIMT on MIP. These effects were found after per-protocol analysis; therefore, the results are only for participants who actually performed RIMT. These results strengthen the conclusion of a recently published randomized clinical trial on RIMT23 and a meta-analysis on respiratory muscle training in general.19,20 The short-term additional effect of RIMT on MIP found in our study (11.7 cm H2O) was comparable to the pooled effect of the previously mentioned meta-analysis (10.7 cm H2O)20 but lower than the effect found by Mueller et al (26.5 cm H2O).23 However, in that study, a different control intervention was applied. When considering the relative improvements in the RIMT groups, the results were quite similar (46.6% in our study versus 53.6% in the study by Mueller et al23), despite lower training intensities in our study (50%–70% of baseline MIP versus 80% of actual MIP). Improvement of MIP during the first months after onset of SCI may be of great importance in this population. After all, in acute SCI, respiratory muscle function is often severely impaired, and medical complications lurk.2 Well-preserved inspiratory muscle function is essential in maintaining adequate gas exchange during quiet breathing and in situations of increased respiratory demand (during exercise, strenuous work such as wheelchair propelling or making transfers, and during periods of illness or respiratory complications).35,36 The positive short-term effect on MIP found in our study was partly sustained at follow-up but was no longer statistically significant. A large part of the sustained effect 8 weeks after the intervention appeared to be due to the 8 participants who continued RIMT after the intervention period. This finding suggests that a longer training period may prolong the effect of RIMT on MIP. Perhaps for long-term effects, maintenance training may be needed, as previously reported in people with COPD.37

Based on previously found associations between inspiratory muscle function on the one hand and lung volumes38 and cough flows9 on the other, it could be expected that RIMT would indirectly (through improved MIP) improve lung volumes and flows. Nevertheless, the present study showed no effect on lung volumes and flows. The lack of an immediate effect on FVC is in agreement with the results of Mueller et al23 but does not coincide with the positive effect on vital capacity found in the study on RIMT by Liaw et al22 and the meta-analysis on respiratory muscle training in general.19,20 As pointed out by the authors of that meta-analysis, the effect they found was not strong (small effect size and small number of studies) and may have been overestimated due to uncontrolled differences at baseline. The aforementioned associations among inspiratory muscle function, lung volumes, and cough flows may be complex and cumulative in nature. Factors such as concomitant trauma of lung tissue and thorax, spasticity of the trunk muscles, and the degree of preservation of expiratory muscle may play an important role. In addition, over time, the inability to inspire deeply (due to weak inspiratory muscle strength) may lead to a cascade of reduced compliance of lung and thorax, lowered reserve capacity of the respiratory pump, increased susceptibility for medical complications,35 recurrent respiratory infections, and gradual deterioration of lung tissue. The latter may explain the associations between low MIP and excessive decline in FVC in people with chronic SCI found in previous studies.10,11

With the exception of a short-term effect of RIMT on mental health, no effects were found on measures of patient functioning. The specific short-term effect of RIMT on mental health may be explained by the extra attention participants in the RIMT group received and their trust in a positive effect. However, this explanation does not have a strong basis; therefore, especially in combination with the possible effect of multiple testing for which we did not correct in our analyses, we have to be careful in drawing firm conclusions. Another important aim of this trial was to study the effects on respiratory complications. The results did not indicate a positive effect of RIMT on respiratory complications. However, the power analysis was based on respiratory function measures and not on respiratory complications; therefore, interpretation of these results should be done with caution. To attain better insight into the effect of respiratory muscle training on long-term respiratory complications, large-scale studies with a long (several years) follow-up time are necessary. In addition, research is needed to study whether respiratory complications during the acute phase can be prevented when RIMT is started shortly after injury. In the present study, for methodological reasons, the intervention started relatively late. Nevertheless, RIMT also can be performed by patients still immobilized in bed, with a tracheostomy or even in combination with mechanical ventilation.

In this trial, RIMT was successfully conducted in 3 different SCI units without large changes in care or organization. The positive effect of RIMT on MIP did not differ among these units. In general, administration of the training delivered no problems. A short instruction, face-to-face and on paper, was sufficient to instruct the therapists. Additionally, the training sessions fitted within the regular structure of half-hour treatment schedules, and the majority of training sessions were performed with little supervision. Participants with restricted hand function needed personal assistance to start and finish the training and a simple homemade stand to position the device. Furthermore, most participants were able to handle the training device independently, and some used the device at home. The majority of participants in the RIMT group were satisfied (13 of 19 participants) or somewhat satisfied (4 participants) about the training. In contrast to previous studies, we included not only people with complete tetraplegia but also those with incomplete tetraplegia or paraplegia who had impaired pulmonary function. Therefore, the results of this study may be generalized to all people with SCI who have impaired pulmonary function, regardless of lesion level. However, the results of the present study (eg, a positive immediate effect on MIP) suggest that RIMT may be especially beneficial in people with weakness of the inspiratory muscles. Therefore, MIP may be a better indicator for RIMT than impaired pulmonary function.

A limitation of the present study may have been the uneven distribution of people with premorbid respiratory diseases between groups (all were allocated to the control group). However, post hoc analysis showed that conclusions concerning the effect of RIMT on MIP did not change when the data of these individuals were excluded. Nevertheless, because of the uneven distribution, the present study does not answer the question whether the proven positive effects of RIMT in people with COPD or asthma also apply after SCI.15,39 Another limitation was that the questionnaires on perceived respiratory function, limitations in daily life, and respiratory complications were not validated and may not have been sensitive enough to detect differences between groups. In addition, the relatively large number of dropouts 1 year after inpatient rehabilitation caused a loss of power, which may have influenced the results concerning long-term follow-up. Finally, due to the low incidence rates, the sample size may have been too small to show long-term effects on respiratory complications. Altogether, interpretation of the long-term effects on patient functioning has to be done with caution.

In conclusion, RIMT has a positive short-term effect on inspiratory muscle function and is a feasible and important addition to the usual inpatient rehabilitation of people with SCI who have impaired pulmonary function, regardless of lesion level. To sustain the effect over a longer time period, the training periods may have to be extended. Based on the results of this study, it is not possible to make conclusions regarding the long-term effects of RIMT on respiratory complications. Future research is needed to attain better insight into the underlying mechanisms of respiratory muscle training and the effect on respiratory complications.

The Bottom Line

What do we already know about this topic?

Respiratory function is seriously impaired in many people with spinal cord injury. Specific inspiratory muscle training may result in greater improvement in pulmonary function and cough capacity during initial recovery and may lower the risk of excessive decline in pulmonary function and respiratory complications in the chronic phase.

What new information does this study offer?

Resistive inspiratory muscle training, added to the usual inpatient rehabilitation care, had an immediate positive effect on inspiratory muscle strength in people with spinal cord injury and impaired pulmonary function. This effect was no longer significant after long-term follow-up. No effects on other parameters of respiratory function or measures of patient functioning were found except for an immediate effect on mental health.

If you're a patient, what might these findings mean for you?

Eight weeks of resistive inspiratory muscle training with a threshold trainer improves inspiratory muscle strength.

Footnotes

  • All authors provided concept/idea/research design. Ms Postma, Dr Haisma, and Dr Bussmann provided writing. Ms Postma provided data collection. Ms Postma and Dr Haisma provided data analysis. Ms Postma, Dr Stam, and Dr Bussmann provided project management and fund procurement. Ms Postma and Dr Stam provided facilities/equipment. Ms Postma and Dr Bussmann provided institutional liaisons. Dr Haisma, Dr Hopman, Dr Bergen, Dr Stam, and Dr Bussmann provided consultation (including review of the manuscript before submission). The authors thank all participants, the participating rehabilitation centers and their research assistants and physicians who collected data, and the physical therapists who were involved in the training: Rijndam Rehabilitation Center (Rotterdam) and Rehabilitation Center De Hoogstraat (Utrecht), Reade (Amsterdam), and Heliomare (Wijk aan Zee).

  • Part of the manuscript was presented as a poster at the International Spinal Cord Society (ISCOS); October 28–30, 2013; Istanbul, Turkey.

  • The study was approved by the Medical Ethics Committee of Erasmus University Medical Centre, Rotterdam, the Netherlands.

  • This study was supported by the Kinderrevalidatie Fonds Adriaanstichting (grant no. 2007/0179-063).

  • The trial was registered at the Dutch trial register (NTR1921) in July 2009.

  • Received February 26, 2014.
  • Accepted July 19, 2014.

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Resistive Inspiratory Muscle Training in People With Spinal Cord Injury During Inpatient Rehabilitation: A Randomized Controlled Trial
Karin Postma, Janneke A. Haisma, Maria T.E. Hopman, Michael P. Bergen, Henk J. Stam, Johannes B. Bussmann
Physical Therapy Dec 2014, 94 (12) 1709-1719; DOI: 10.2522/ptj.20140079

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Resistive Inspiratory Muscle Training in People With Spinal Cord Injury During Inpatient Rehabilitation: A Randomized Controlled Trial
Karin Postma, Janneke A. Haisma, Maria T.E. Hopman, Michael P. Bergen, Henk J. Stam, Johannes B. Bussmann
Physical Therapy Dec 2014, 94 (12) 1709-1719; DOI: 10.2522/ptj.20140079
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