512215
2013
CRE28610.1177/0269215513512215Clinical RehabilitationAslan et al.
CLINICAL REHABILITATION
Article
Effects of respiratory muscle training on pulmonary functions in patients with slowly progressive neuromuscular disease: a randomized controlled trial
Clinical Rehabilitation 2014, Vol. 28(6) 573–581 © The Author(s) 2013 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0269215513512215 cre.sagepub.com
Goksen Kuran Aslan1, H Nilgun Gurses2, Halim Issever3 and Esen Kiyan4
Abstract Objective: To investigate the effects of inspiratory and expiratory muscle training on pulmonary functions in patients with slowly progressive neuromuscular disease. Design: Prospective randomized controlled double-blinded study. Setting: Chest diseases clinic of university hospital. Subjects: Twenty-six patients with slowly progressive neuromuscular disease followed for respiratory problems were included in the study. Patients were randomly divided into two groups; experimental (n = 14; age 31.6 ±12.3 years) and sham (n = 12; age 26.5 ±8.6 years) groups. Methods: Spirometry, peak cough flow, maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal inspiratory pressure were measured before the eighth week of study, and subsequently at end of it. Respiratory muscle training was performed by inspiratory (Threshold Inspiratory Muscle Trainer) and expiratory (Threshold Positive Expiratory Pressure) threshold loading methods. Training intensities were increased according to maximal inspiratory and expiratory pressures in the experimental group, while the lowest loads were used for training in the sham group. Patients performed 15 minutes inspiratory muscle training and 15 minutes expiratory muscle training, twice a day, five days/week, for a total of eight weeks at home. Training intensity was adjusted in the training group once a week. Results: Maximal inspiratory and expiratory pressures (cmH2O, % predicted) (respectively p = 0.002, p = 0.003, p = 0.04, p = 0.03) and sniff nasal inspiratory pressure (p = 0.04) were improved in the experimental group when compared with the sham group. However, there was no improvement in spirometric measurements when groups were compared (p > 0.05). Conclusions: As a conclusion of our study, we found that respiratory muscle strength improved by inspiratory and expiratory muscle training in patients with slowly progressive neuromuscular disease. 1Department of Physical Therapy and Rehabilitation, Istanbul University, Istanbul, Turkey 2Department of Physiotherapy and Rehabilitation, BezmialemVakif University, Istanbul, Turkey 3Department of Public Health, Istanbul University, Istanbul, Turkey 4Department of Chest Disease, Istanbul University, Istanbul, Turkey
Corresponding author: H Nilgun Gurses, Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, BezmialemVakif University, Ortaklar Cad. Pehlivan Sok. S. Aksoy Ap. No: 42/13B, Fulya Mah. 34394 Sisli/Istanbul, Turkey. Email: [email protected]
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
574
Clinical Rehabilitation 28(6)
Keywords Neuromuscular diseases, respiratory muscle training, maximal inspiratory pressure, maximal expiratory pressure, hospital-supported home rehabilitation Received: 9 June 2013; accepted: 19 October 2013
Introduction Respiratory muscle weakness is a common and a serious problem among patients with neuromuscular disease.1 Inspiratory muscle weakness can decrease vital capacity and chest wall expansion,2 while expiratory muscle weakness can decrease coughing strength, causing atelectasis and infections.3–5 Therefore, it is generally accepted that respiratory muscle weakness causes increased morbidity and mortality1,6 owing to inadequate ventilation, nocturnal hypoventilation and ineffective coughing.1,3 Respiratory muscle weakness-related symptoms are not always typical in patients with neuromuscular diseases. These patients may have clinically significant respiratory muscle weakness in the absence of typical symptoms, such as dyspnea, orthopnea, rapid shallow breathing, daytime hypersomnolence, morning headaches, and insomnia.7 Some nocturnal hypoventilation-related symptoms, such as fatigue and exhaustion, may be misinterpreted as one of the symptoms of the deterioration of the underlying neuromuscular disease.8 Furthermore, symptoms of respiratory muscle weakness, especially dyspnea, may be absent or latent owing to reduced mobility related to peripheral muscle weakness.7 In any case, early recognition and treatment of respiratory muscle weakness is very important in neuromuscular diseases.8 It has been shown that inspiratory muscle training aids treatment and increases inspiratory muscle strength in patients with neuromuscular disease, especially in those with muscular dystrophies.9–11 Therefore, the American Thoracic Society/European Respiratory Society pulmonary rehabilitation guidelines recommends inspiratory muscle training for suspected or confirmed respiratory muscle weakness.12 Unlike other diseases, neuromuscular diseases are also associated with weakness of the expiratory muscles,13 which increases the risk of
respiratory complications.3–5 The use of expiratory muscle training may prevent expiratory muscle strength from decreasing. However, the effect of inspiratory muscle training and expiratory muscle training on respiratory functions in patients with slowly progressive neuromuscular diseases is understudied in the literature. Therefore, the purpose of this study was to determine if inspiratory and expiratory muscle training would improve pulmonary function and respiratory muscle strength of patients with slowly progressive neuromuscular disease.
Methods This study was prospective, randomized, controlled, and double-blinded and approved by the University Ethics Committee. Patients with neuromuscular diseases from Neuromuscular Diseases outpatient clinic of a university hospital’s chest diseases department were screened for the study. The inclusion criteria were; neurologist-confirmed diagnosis of neuromuscular diseases that have a slow disease progression rate, such as Myotonic dystrophy, oculopharnygodistal myopathy, Limb-Girdle muscular dystrophy, multiminicore disease, congenital myopathy, facioscapulohumeral dystrophy, etc. In addition, the ability to walk independently, ability to do daily living activities independently, and to comprehend commands, having no contractures and language disorders were also further inclusion criteria. Patients diagnosed with Duchenne muscular dystrophy, amyotrophic lateral sclerosis, and patients who have moderate or severe scoliosis, acute lower respiratory tract infection, and major cardiac problems (heart failure, arrhythmia, cardiomyopathy, etc.) were excluded.
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
575
Aslan et al. Twenty-eight patients with neuromuscular diseases met the criteria. All patients and/or families gave their written informed consent to participation, except two patients who declined to participate because of their transportation problems. After consent and initial assessment, data were collected (pulmonary function measurements, age, gender, body mass index, diagnosis and duration of illness, comorbidities, and the use of home oxygen or noninvasive mechanical ventilation), participants were randomized by the study coordinator. Subjects were allocated to an experimental group or a sham group using a numbered series of 30 prefilled envelopes specifying group assignment created by a computerbased random number generator.14 Patients were unaware of which group they were included and were referred to a physiotherapist who was blinded to the assessments for inspiratory and expiratory muscle training. When patients finished eight weeks of training they were referred to a pulmonary function laboratory for final assessments by the coordinator of the study (Figure 1). During the eight weeks, all patients were asked to perform both inspiratory and expiratory muscle training at home for at least five days a week, twice a day for 15 minutes at each session (15 minutes inspiratory muscle training + 15 minutes expiratory muscle training). A diary was given to each patient to record their sessions and their compliance. A physiotherapist educated the patients and their families for the use and maintenance of the devices. Patients were called to the clinic once a week to measure mouth pressures, to control diaries, to find out whether they have any complaints or not, and to perform one session training with our physiotherapist. In experimental group, after measurement of maximal inspiratory and expiratory pressures, the intensity of the training was determined as 30% of the maximal inspiratory pressure level for inspiratory muscle training and 30% of the maximal expiratory pressure level for expiratory muscle training. The intensity was adjusted weekly after mouth pressure measurements. In the sham group the intensity of training was kept at minimum for both inspiratory and expiratory muscle training (9 cm H2O for inspiratory muscle training and 5 cm H2O for expiratory muscle training). Mouth pressures were measured
every week, but the intensity was not changed for the eight weeks. “Threshold Inspiratory Muscle Trainer (Threshold IMT)” was used for inspiratory muscle training (measurement range 9–41 cm H2O) (Respironics, New Jersey, Inc. NJ, USA). Threshold IMT incorporates a flow-independent one-way valve to ensure consistent resistance and features an adjustable specific pressure setting (in cm H2O) to be set by a healthcare professional. “Threshold Positive Expiratory Pressure (Threshold PEP)” was used for expiratory muscle training (measurement range 5–20 cm H2O) (Respironics, New Jersey, Inc. NJ, USA). Threshold PEP incorporates a flow-independent oneway valve to ensure consistent resistance and features an adjustable specific pressure setting (in cm H2O) to be set by a healthcare professional. For outcome measures; spirometry (forced expiratory volume in one second (FEV1), forced vital capacity (FVC) and FEV1/FVC ratio), peak cough flow, maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal-inspiratory pressure measurements were performed at the beginning of the study and subsequently at the eighth week. Spirometric parameters were measured using a ZAN-GPI 3.00 (Nspire Health GmbH, Germany). Maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal-inspiratory pressure were measured by a Micro Medical MicroRPM® (Carefusion Micromedical, Micro RPM, USA). For peak cough flow, three measurements by peak expiratory flow meter were performed and the highest level was recorded.15,16 All measurements were taken by a technician who was blinded to the study. The acceptance criteria of the American Thoracic Society/ European Respiratory Society was used for spirometric measurements.17 Maximal inspiratory and expiratory pressures measurements were performed using the Black and Hyatt technique.18 The minimum sample size (Type I error = 0.05, Type II error = 0.20, and power = 0.80) was found to be 10 for each group, by aiming for an average increase of 7 units and an estimated standard deviation of 7 units in pretreatment and posttreatment maximal inspiratory pressure, maximal expiratory pressure, sniff nasal inspiratory pressure, and peak cough flow values for each group. Our sample size
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
576
Clinical Rehabilitation 28(6)
Total patients screened (n=283)
Excluded (n=257) • Did not match inclusion criteria (n=255) • Refused to participate (n=2)
Accept to participate (n=26)
Assessment (PFT Laboratory technician) MIP, MEP, SNIP, PCF, PFT Blind to group allocation
Randomization: computer-based random number generator
Allocated to experimental group ( n=14)
Allocated to sham group ( n=12)
Discontinued intervention (n=2) Due to personal reason
Training 8 weeks (physiotherapist) Blind to initial and final assesments
Assessment (PFT Laboratory technician) MIP, MEP, SNIP, PCF, PFT Blind to group allocation
Figure 1. Design of the study (CONSORT flow diagram). PFT, pulmonary function test; MIP, maximal inspiratory pressure; MEP, maximal expiratory pressure; SNIP, sniff nasal inspiratory pressure; PCF, peak cough flow.
was arranged according to just mentioned power analysis.
Statistical analysis The homogeneity tests between two groups were performed by independent samples; t-test and covariance analysis for quantitative variables and chisquare test for categorical variables. Normal distribution was analyzed by the Kolmogorov– Smirnow Z test for all group variables. Differences after the training between the two groups were analyzed by covariance analysis. Data were analyzed
by using SPSS (Statistical Package for Social Science, Version 15). Statistical significance was set as p < 0.05.
Results Two patients in the control group (one spinal muscular atrophy Type 3, one oculopharyngodistal myopathy) discontinued the study owing to personal reasons after the first week. There were 14 patients in the experimental group (five myotonic dystrophy, three myopathy, two oculopharyngodistal myopathy, one desminopathy, one multiminicore disease, one
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
577
Aslan et al. Table 1. Patients’ characteristics.
Age (years) Gender (M/F) Body mass index (kg/m²) Disease duration (month) FVC (L) FVC (pred %) FEV1 (L) FEV1 (pred %) FEV1/FVC ratio MIP (cmH2O) MIP (pred %) MEP (cmH2O) MEP (pred %) SNIP (cmH2O) PCF (L/min)
Experimental (n = 14)
Sham (n = 10)
p value
31.6 (12.3) 8M 6F 19.5 (4.9) 110.4 (57.8) 2.1 (0.6) 55.0 (16.0) 1.9 (0.6) 57.4 (19.4) 87.8 (11.9) 50.2 (9.7) 50.9 (16.0) 45.7 (18.6) 26.3 (17.6) 44.7 (12.2) 254.2 (76.4)
26.5 (8.6) 2M 8F 18.8 (2.2) 123.4 (77.5) 2.7 (0.6) 80.1 (15.0) 2.3 (0.6) 81.7 (16.9) 88.8 (5.5) 48.3 (13.5) 55.7 (24.9) 39.8 (15.9) 28.5 (19.0) 39.5 (12.7) 292.0 (65.1)
0.2 0.07 0.6 0.6 0.5 0.4 0.2 0.1 0.8 0.5 0.02 0.03 0.0001 0.9 0.6
Data are presented as mean (SD). FEV1, forced expiratory volume in one second; FVC, forced vital capacity; MEP, maximal expiratory pressure; MIP, maximal inspiratory pressure; PCF, peak cough flow; SD, standard deviation; SNIP, sniff nasal inspiratory pressure.
Table 2. Effects of respiratory muscle training on spirometric measurements. Experimental (n = 14)
FVC (L) FVC (% pred) FEV1 (L) FEV1 (% pred) FEV1/FVC (%)
Sham (n = 10)
Between groups p value
Initial
8th week
Δ
Initial
8th week
Δ
2.1 (0.6) 55.0 (16.0) 1.9 (0.6) 57.4 (19.5) 87.9 (11.9)
2.2 (0.6) 56.7 (17.1) 2.0 (0.6) 59.5 (18.1) 87.4 (12.0)
0.09 (0.2) 1.6 (5.3) 0.1 (0.2) 2.1 (6.8) –0.4 (2.8)
2.7 (0.7) 80.1 (15.1) 2.3 (0.6) 81.7 (17.0) 88.8 (5.6)
2.5 (0.8) 71.5 (23.9) 2.2 (0.7) 74.2 (24.1) 88.7 (10.0)
–0.2 (0.7) –8.6 (24.4) –0.1 (0.7) –7.5 (26.7) –0.1 (9.1)
0.2 0.6 0.7 0.9 0.9
Data are presented as mean (SD). FEV1, forced expiratory volume in one second; FVC, forced vital capacity; SD, standard deviation; Δ, initial–final test differences.
facioscapulohumeral dystrophy, one congenital myopathy), and 10 patients in sham group (two myotonic dystrophy, three myopathy, two oculopharyngodistal myopathy, two Limb-Girdle muscular dystrophy, one spinal muscular atrophy Type 3). Patients’ characteristics are listed in Table 1. Two patients from the experimental group and one from the sham group were receiving non-invasive mechanical ventilation. No patient was on oxygen therapy and no one had comorbidities or hospitalization during the last year for respiratory problems.
The patients did not miss any hospital sessions and they were compliant at home according to their diaries. No side-effects were reported during the study. When the two groups were compared, there was no statistically significant change in initial–final test differences of spirometric measurements between the two groups (p > 0.05) (Table 2). The increase in initial–final test differences of maximum inspiratory pressure (cm H2O and % predicted), maximum expiratory pressure (cm H2O and % predicted), and sniff nasal inspiratory pressure
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
578
Clinical Rehabilitation 28(6)
Table 3. Effects of respiratory muscle training on respiratory mouth pressures, sniff nasal pressure, and peak cough flow. Experimental (n = 14) Initial 50.3 (9.7) MIP (cm H20) MIP (% pred) 50.8 (16.0) 45.8 (18.6) MEP (cm H20) MEP (% pred) 26.3 (17.6) SNIP (cm H20) 44.8 (12.3) PCF (L/min) 254.3 (76.4)
Sham (n = 10)
8th week
Δ
Initial
8th week
Δ
74.5 (16.6) 74.7 (23.7) 60.4 (25.3) 35.1 (23.3) 60.5 (17.3) 296.4 (90.3)
24.2 (13.7) 23.8 (14.7) 14.6 (11.1) 8.8 (7.6) 17.3 (15.6) 42.1 (38.7)
48.3 (13.5) 55.7 (25.0) 39.8 (15.9) 28.5 (19.0) 39.5 (12.7) 292.0 (65.1)
53.9 (20.4) 5.6 (10.8) 62.6 (37.5) 6.9 (14.7) 44.9 (20.5) 5.1 (6.8) 32.8 (26.2) 4.3 (7.9) 45.2 (14.1) 5.7 (5.1) 309.0 (69.5) 17.0 (20.0)
Between groups p value 0.002 0.003 0.04 0.03 0.04 0.07
Data are presented as mean (SD). MEP, maximal expiratory pressure; MIP, maximal inspiratory pressure; PCF, peak cough flow; SNIP, sniff nasal inspiratory pressure; SD, standard deviation; Δ, initial–final test differences.
were significantly higher in the experimental group (p < 0.05). The increase in initial–final test differences of peak cough flow was higher in the experimental group when compared with the sham group, but it was not found significant (p = 0.7) (Table 3).
Discussion In our study, we found significant increases in maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal inspiratory pressure after eight weeks of inspiratory and expiratory muscle training in the experimental group when compared with the sham group. After training, there was no significant change in spirometric measurements (FVC, FEV1, FEV1/ FVC) between the two groups. The experimental group had a minimal increase in FEV1 and FVC % predicted, while the sham group had a decrease in eight weeks, which shows that training may have a role in stabilizing of pulmonary function test, or at least in delaying its decline. Koessler et al.10 investigated this fact in their study by giving 24 months of inspiratory muscle training to their patients with spinal muscular atrophy (nine patients) and Duchenne muscular dystrophy (18 patients). They stated that there was no significant decline in vital capacity after training and concluded that they have shown the effect of long-term training of inspiratory
muscle training on stabilization of vital capacity. Since it is regarded as a predictor of the need for mechanical ventilation, delaying its decline is an important conclusion. Many researchers studying inspiratory muscle training in neuromuscular disease have found that despite a significant increase in respiratory muscle strength, the same improvement was not observed for spirometric measurements.9–11 Wanke et al.9 found improvement only in respiratory muscle strength with six months of a inspiratory resistive device in patients with Duchenne muscular dystrophy. Koessler et al.10 used a similar training method to Wanke et al. and found improvement in maximum inspiratory pressure and 12 second maximum voluntary ventilation. Although the methods, patient diagnosis, and training periods of above studies were different from ours, the results were similar in showing the significant effect of training in strength of inspiratory muscles. Yeldan et al.11, compared the effects of threemonth inspiratory muscle training in patients with Limb Girdle and Becker muscular dystrophy. At the end of three months, the authors found an increase in maximal inspiratory pressure by using similar equipment and inspiratory muscle training protocol like our study and an increase in maximal inspiratory and expiratory pressure with respiratory exercises. The improvement in maximum inspiratory pressure was more significant in the inspiratory
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
579
Aslan et al. muscle training group, whereas there were no changes in spirometric data in both groups. The authors commented that there could have been a significant increase in maximal expiratory pressure if expiratory muscle training had been added to the inspiratory muscle training group. Our study confirms their findings. Although our training time was shorter than the studies mentioned, we still found a similar increase in maximum inspiratory pressure. There are only two publications about the effectiveness of using both inspiratory and expiratory muscle training at the same time in neuromuscular disease.19–20 One of these publications is a case report of myotonic dystrophy19 and the other one is a controlled study.20 Gozal et al.20 found significant improvement in respiratory muscles by inspiratory and expiratory muscle training in their controlled study on patients with Duchenne muscular dystrophy and spinal muscular atrophy. However, they reported that there was no change in pulmonary functions. They did not find any increase in respiratory muscle strength (inspiratory and expiratory) in their control group, which did not receive training. Our study differs from the above study with respect to training time, training intensity, and the control time. For instance, their training time was six months, whereas ours was eight weeks. In addition, they had used control group, whereas we used sham group trained with the lowest training load. We believe that our program of training, performed at home with support from hospital, supervised by a physiotherapist, and also the weekly control of the diaries, was effective in increasing the compliance of the patients to the training. This conclusion is confirmed by the data of the previously mentioned studies, which showed effective results with hospitalsupported home-based programs.9–11,19–20 We were unable to find a study in the literature investigating the effect of inspiratory and expiratory muscle training on peak cough flow in patients with muscular diseases. However, there is one study, in which the effect of expiratory muscle training on respiratory functions, including peak cough flow levels in healthy individuals, were investigated. In this study, Sasaki21 divided 33 patients into three groups; one group received training at the normal expiratory flow rate, one
group at the fast expiratory flow speed, and the third control group received no training. At the end of training there was a significant increase in maximum expiratory pressure levels in the two training groups when compared with the control group, while there was no difference between the two training groups. There was no improvement in respiratory functions and peak cough flow levels with expiratory muscle training. Our study is the first one to evaluate the effect of inspiratory and expiratory muscle training on peak cough flow in neuromuscular diseases, and we found that peak cough flow was higher in the experimental group when compared with the sham group, but there was no statistical significance (p = 0.07). Our study has some limitations. Designing a training study with neuromuscular diseases has many problems. Patients may differ with respect to diagnosis, involvement of muscle weakness, and rate of progression. It is difficult to obtain a reasonable number of patients having the same diagnosis and distribution of weakness. For this reason, although we know that it is a limitation for this study, we included patients with different diagnosis of neuromuscular disorders. However, we tried to homogenize our study sample by choosing neuromuscular diseases that have a slow progression rate. Our patient groups were small because we only included ambulatory patients to the study. Besides, some patients did not accept participation because they had transportation problems. Another limitation was that the “Threshold PEP” device used was limited to a maximum resistance of 20 cm H2O. This meant that some patients’ training intensity was below 30% of maximum expiratory pressure. Despite this handicap, we found a significant increase in maximum expiratory pressure in both groups. Literature reports that training intensity for inspiratory muscle training should be a minimum of 30% of maximum inspiratory pressure in order to reveal the effects of training,22 however, we were unable to find similar data for expiratory muscle training. This data is supported by our finding of no change in maximum inspiratory pressure, but improvement in maximum expiratory pressure with this level of intensity in the sham group. We investigated training effects of
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
580
Clinical Rehabilitation 28(6)
inspiratory and expiratory muscle training on pulmonary functions. We do not know whether these approaches have an effect on mobility or they prevent development of respiratory complications in these patient groups. This may also be a limitation of our study. We need more studies further investigating these topics. Our study demonstrates that an improvement of maximal inspiratory pressure (cm H2O and % predicted), maximal expiratory pressure (cm H2O and % predicted), and sniff nasal inspiratory pressure can be achieved in patients with slowly progressive muscular diseases after eight weeks of inspiratory and expiratory muscle training. However, there is a need for longer follow-up studies to evaluate how long this effect lasts.
Acknowledgements The authors give thanks gratefully to the technician of the pulmonary function test laboratory at the University Chest Diseases Clinic for spirometry and respiratory muscle strength measurements of patients. We also highly appreciate the editing support we received from Dr David Terence Thomas MD and Dr Kerem Gurses PhD in the first and second submissions, respectively.
Conflict of interest The author declares that there is no conflict of interest.
Funding This work was supported by the Istanbul University Research Fund (grant number 5561).
References Clinical messages • Inspiratory and expiratory muscle strength can be improved in patients with slowly progressive neuromuscular disease by eight weeks of inspiratory and expiratory muscle training. • The increased respiratory muscle strength did not improve lung function as measured by spirometry. • The program can be delivered at home with support from hospital.
Contributors GKA designed the study, implemented training of patients, drafted the manuscript and was involved in the final approval of the version to be published. HNG designed and coordinated the study, monitored its progress, analyzed and interpreted data, critically reviewed the manuscript and was involved in the final approval of this version to be published. HI was involved in designing the study and running the statistical analysis of the study and approved the final version of the manuscript to be published. EK was involved in designing the study, recruitment of the subjects, interpretation of data, critically reviewing the manuscript and the final approval of the version to be published.
1. Perrin C, Unterborn JN, Ambrosio CD and Hill NS. Pulmonary complications of chronic neuromuscular diseases and their management. Muscle Nerve 2004; 29: 5–27. 2. McCool FD and Tzelepis GE. Inspiratory muscle training in the patient with neuromuscular diseases. Phys Ther 1995; 75: 1006–1014. 3. Lynn DJ, Woda RP and Mendell JR. Respiratory dysfunction in neuromuscular dystrophy and other myopathies. Clin Chest Med 1994; 15: 661–674. 4. Benditt JO and Boitano LJ. Pulmonary issues in patients with chronic neuromuscular disease. Am J Respir Crit Care Med 2013; 10: 1046–1055. 5. Danov Z and Schroth MK. Pediatric management of pediatric patients with neuromuscular disease. Pediatr Ann 2010; 12: 769–776. 6. Ambrosino N, Carpene N and Gherardi M. Chronic respiratory care for neuromuscular diseases in adults. Eur Respir J 2009; 34: 444–451. 7. Polkey M, Lyall RA, Moxham J and Leigh PN. Respiratory aspects of neurological disease. J Neurol Neurosurg Psychiatry 1999; 66: 5–15. 8. Hull J, Aniapravan R, Chan E, et al. British Thoracic Society guideline for respiratory management of children with neuromuscular weakness. Thorax 2012; 67: i1–i40. 9. Wanke T, Toifle K, Merkle M, et al. Inspiratory muscle training in patients with Duchenne muscular dystrophy. Chest 1994; 105: 475–482. 10. Koessler W, Wanke T, Winkler G, et al. Two years experience with inspiratory muscle training in patients with neuromuscular disorders. Chest 2001; 120: 765–769. 11. Yeldan I, Gurses HN and Yuksel H. Comparison study of chest physiotherapy home training programmes on respiratory
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
581
Aslan et al. functions in patients with muscular dystrophy. Clin Rehabil 2008; 22: 741–748. 12. Nici L, Donner C, Wouters E, et al. American Thoracic Society; European Respiratory Society. ATS/ERS statement on pulmonary rehabilitation. Am J Respir Crit Care Med 2006; 173: 1390–1413. 13. Araújo TL, Resqueti VR, Bruno S, et al. Respiratory muscle strength and quality of life in myotonic dystrophy patients. Rev Port Pneumol 2010; 6: 892–898. 14. Graph Pad Software. Quick Calcs. http://graphpad.com/ quickcalcs/randomize2.cfm (October 2009). 15. Gauld LM and Boynton A. Relationship between peak cough flow and spirometry in Duchenne muscular dystrophy. Pediatr Pulmonol 2005; 39: 457–460. 16. Bianchi C and Baiardi P. Cough peak flows: Standard values for children and adolescents. Am J Phys Med Rehabil 2008; 87: 461–467.
17. Miller MR, Hankinson J, Brusasco V, et al. ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J 2005; 26: 319–338. 18. Black LF and Hyatt RE. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis 1969; 99: 696–702. 19. Fregonozi GAF, Resqueti VR and Casan P. Domiciliary respiratory muscle training in myotonic dystrophy. Arch Bronconeumol 2006; 42: 605–607. 20. Gozal D and Thiriet P. Respiratory muscle training in neuromuscular disease: long-term effects on strengt hand load perception. Med Sci in Sports Exerc 1999; 31: 1522–1527. 21. Sasaki M. The effect of expiratory muscle training on pulmonary function in normal subjects. J Phys Ther Sci 2007; 19: 197–203. 22. Gosselink R. Physiotherapy in respiratory disease. Breathe 2006; 3: 31–39.
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
2013
CRE28610.1177/0269215513512215Clinical RehabilitationAslan et al.
CLINICAL REHABILITATION
Article
Effects of respiratory muscle training on pulmonary functions in patients with slowly progressive neuromuscular disease: a randomized controlled trial
Clinical Rehabilitation 2014, Vol. 28(6) 573–581 © The Author(s) 2013 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0269215513512215 cre.sagepub.com
Goksen Kuran Aslan1, H Nilgun Gurses2, Halim Issever3 and Esen Kiyan4
Abstract Objective: To investigate the effects of inspiratory and expiratory muscle training on pulmonary functions in patients with slowly progressive neuromuscular disease. Design: Prospective randomized controlled double-blinded study. Setting: Chest diseases clinic of university hospital. Subjects: Twenty-six patients with slowly progressive neuromuscular disease followed for respiratory problems were included in the study. Patients were randomly divided into two groups; experimental (n = 14; age 31.6 ±12.3 years) and sham (n = 12; age 26.5 ±8.6 years) groups. Methods: Spirometry, peak cough flow, maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal inspiratory pressure were measured before the eighth week of study, and subsequently at end of it. Respiratory muscle training was performed by inspiratory (Threshold Inspiratory Muscle Trainer) and expiratory (Threshold Positive Expiratory Pressure) threshold loading methods. Training intensities were increased according to maximal inspiratory and expiratory pressures in the experimental group, while the lowest loads were used for training in the sham group. Patients performed 15 minutes inspiratory muscle training and 15 minutes expiratory muscle training, twice a day, five days/week, for a total of eight weeks at home. Training intensity was adjusted in the training group once a week. Results: Maximal inspiratory and expiratory pressures (cmH2O, % predicted) (respectively p = 0.002, p = 0.003, p = 0.04, p = 0.03) and sniff nasal inspiratory pressure (p = 0.04) were improved in the experimental group when compared with the sham group. However, there was no improvement in spirometric measurements when groups were compared (p > 0.05). Conclusions: As a conclusion of our study, we found that respiratory muscle strength improved by inspiratory and expiratory muscle training in patients with slowly progressive neuromuscular disease. 1Department of Physical Therapy and Rehabilitation, Istanbul University, Istanbul, Turkey 2Department of Physiotherapy and Rehabilitation, BezmialemVakif University, Istanbul, Turkey 3Department of Public Health, Istanbul University, Istanbul, Turkey 4Department of Chest Disease, Istanbul University, Istanbul, Turkey
Corresponding author: H Nilgun Gurses, Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, BezmialemVakif University, Ortaklar Cad. Pehlivan Sok. S. Aksoy Ap. No: 42/13B, Fulya Mah. 34394 Sisli/Istanbul, Turkey. Email: [email protected]
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
574
Clinical Rehabilitation 28(6)
Keywords Neuromuscular diseases, respiratory muscle training, maximal inspiratory pressure, maximal expiratory pressure, hospital-supported home rehabilitation Received: 9 June 2013; accepted: 19 October 2013
Introduction Respiratory muscle weakness is a common and a serious problem among patients with neuromuscular disease.1 Inspiratory muscle weakness can decrease vital capacity and chest wall expansion,2 while expiratory muscle weakness can decrease coughing strength, causing atelectasis and infections.3–5 Therefore, it is generally accepted that respiratory muscle weakness causes increased morbidity and mortality1,6 owing to inadequate ventilation, nocturnal hypoventilation and ineffective coughing.1,3 Respiratory muscle weakness-related symptoms are not always typical in patients with neuromuscular diseases. These patients may have clinically significant respiratory muscle weakness in the absence of typical symptoms, such as dyspnea, orthopnea, rapid shallow breathing, daytime hypersomnolence, morning headaches, and insomnia.7 Some nocturnal hypoventilation-related symptoms, such as fatigue and exhaustion, may be misinterpreted as one of the symptoms of the deterioration of the underlying neuromuscular disease.8 Furthermore, symptoms of respiratory muscle weakness, especially dyspnea, may be absent or latent owing to reduced mobility related to peripheral muscle weakness.7 In any case, early recognition and treatment of respiratory muscle weakness is very important in neuromuscular diseases.8 It has been shown that inspiratory muscle training aids treatment and increases inspiratory muscle strength in patients with neuromuscular disease, especially in those with muscular dystrophies.9–11 Therefore, the American Thoracic Society/European Respiratory Society pulmonary rehabilitation guidelines recommends inspiratory muscle training for suspected or confirmed respiratory muscle weakness.12 Unlike other diseases, neuromuscular diseases are also associated with weakness of the expiratory muscles,13 which increases the risk of
respiratory complications.3–5 The use of expiratory muscle training may prevent expiratory muscle strength from decreasing. However, the effect of inspiratory muscle training and expiratory muscle training on respiratory functions in patients with slowly progressive neuromuscular diseases is understudied in the literature. Therefore, the purpose of this study was to determine if inspiratory and expiratory muscle training would improve pulmonary function and respiratory muscle strength of patients with slowly progressive neuromuscular disease.
Methods This study was prospective, randomized, controlled, and double-blinded and approved by the University Ethics Committee. Patients with neuromuscular diseases from Neuromuscular Diseases outpatient clinic of a university hospital’s chest diseases department were screened for the study. The inclusion criteria were; neurologist-confirmed diagnosis of neuromuscular diseases that have a slow disease progression rate, such as Myotonic dystrophy, oculopharnygodistal myopathy, Limb-Girdle muscular dystrophy, multiminicore disease, congenital myopathy, facioscapulohumeral dystrophy, etc. In addition, the ability to walk independently, ability to do daily living activities independently, and to comprehend commands, having no contractures and language disorders were also further inclusion criteria. Patients diagnosed with Duchenne muscular dystrophy, amyotrophic lateral sclerosis, and patients who have moderate or severe scoliosis, acute lower respiratory tract infection, and major cardiac problems (heart failure, arrhythmia, cardiomyopathy, etc.) were excluded.
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
575
Aslan et al. Twenty-eight patients with neuromuscular diseases met the criteria. All patients and/or families gave their written informed consent to participation, except two patients who declined to participate because of their transportation problems. After consent and initial assessment, data were collected (pulmonary function measurements, age, gender, body mass index, diagnosis and duration of illness, comorbidities, and the use of home oxygen or noninvasive mechanical ventilation), participants were randomized by the study coordinator. Subjects were allocated to an experimental group or a sham group using a numbered series of 30 prefilled envelopes specifying group assignment created by a computerbased random number generator.14 Patients were unaware of which group they were included and were referred to a physiotherapist who was blinded to the assessments for inspiratory and expiratory muscle training. When patients finished eight weeks of training they were referred to a pulmonary function laboratory for final assessments by the coordinator of the study (Figure 1). During the eight weeks, all patients were asked to perform both inspiratory and expiratory muscle training at home for at least five days a week, twice a day for 15 minutes at each session (15 minutes inspiratory muscle training + 15 minutes expiratory muscle training). A diary was given to each patient to record their sessions and their compliance. A physiotherapist educated the patients and their families for the use and maintenance of the devices. Patients were called to the clinic once a week to measure mouth pressures, to control diaries, to find out whether they have any complaints or not, and to perform one session training with our physiotherapist. In experimental group, after measurement of maximal inspiratory and expiratory pressures, the intensity of the training was determined as 30% of the maximal inspiratory pressure level for inspiratory muscle training and 30% of the maximal expiratory pressure level for expiratory muscle training. The intensity was adjusted weekly after mouth pressure measurements. In the sham group the intensity of training was kept at minimum for both inspiratory and expiratory muscle training (9 cm H2O for inspiratory muscle training and 5 cm H2O for expiratory muscle training). Mouth pressures were measured
every week, but the intensity was not changed for the eight weeks. “Threshold Inspiratory Muscle Trainer (Threshold IMT)” was used for inspiratory muscle training (measurement range 9–41 cm H2O) (Respironics, New Jersey, Inc. NJ, USA). Threshold IMT incorporates a flow-independent one-way valve to ensure consistent resistance and features an adjustable specific pressure setting (in cm H2O) to be set by a healthcare professional. “Threshold Positive Expiratory Pressure (Threshold PEP)” was used for expiratory muscle training (measurement range 5–20 cm H2O) (Respironics, New Jersey, Inc. NJ, USA). Threshold PEP incorporates a flow-independent oneway valve to ensure consistent resistance and features an adjustable specific pressure setting (in cm H2O) to be set by a healthcare professional. For outcome measures; spirometry (forced expiratory volume in one second (FEV1), forced vital capacity (FVC) and FEV1/FVC ratio), peak cough flow, maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal-inspiratory pressure measurements were performed at the beginning of the study and subsequently at the eighth week. Spirometric parameters were measured using a ZAN-GPI 3.00 (Nspire Health GmbH, Germany). Maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal-inspiratory pressure were measured by a Micro Medical MicroRPM® (Carefusion Micromedical, Micro RPM, USA). For peak cough flow, three measurements by peak expiratory flow meter were performed and the highest level was recorded.15,16 All measurements were taken by a technician who was blinded to the study. The acceptance criteria of the American Thoracic Society/ European Respiratory Society was used for spirometric measurements.17 Maximal inspiratory and expiratory pressures measurements were performed using the Black and Hyatt technique.18 The minimum sample size (Type I error = 0.05, Type II error = 0.20, and power = 0.80) was found to be 10 for each group, by aiming for an average increase of 7 units and an estimated standard deviation of 7 units in pretreatment and posttreatment maximal inspiratory pressure, maximal expiratory pressure, sniff nasal inspiratory pressure, and peak cough flow values for each group. Our sample size
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
576
Clinical Rehabilitation 28(6)
Total patients screened (n=283)
Excluded (n=257) • Did not match inclusion criteria (n=255) • Refused to participate (n=2)
Accept to participate (n=26)
Assessment (PFT Laboratory technician) MIP, MEP, SNIP, PCF, PFT Blind to group allocation
Randomization: computer-based random number generator
Allocated to experimental group ( n=14)
Allocated to sham group ( n=12)
Discontinued intervention (n=2) Due to personal reason
Training 8 weeks (physiotherapist) Blind to initial and final assesments
Assessment (PFT Laboratory technician) MIP, MEP, SNIP, PCF, PFT Blind to group allocation
Figure 1. Design of the study (CONSORT flow diagram). PFT, pulmonary function test; MIP, maximal inspiratory pressure; MEP, maximal expiratory pressure; SNIP, sniff nasal inspiratory pressure; PCF, peak cough flow.
was arranged according to just mentioned power analysis.
Statistical analysis The homogeneity tests between two groups were performed by independent samples; t-test and covariance analysis for quantitative variables and chisquare test for categorical variables. Normal distribution was analyzed by the Kolmogorov– Smirnow Z test for all group variables. Differences after the training between the two groups were analyzed by covariance analysis. Data were analyzed
by using SPSS (Statistical Package for Social Science, Version 15). Statistical significance was set as p < 0.05.
Results Two patients in the control group (one spinal muscular atrophy Type 3, one oculopharyngodistal myopathy) discontinued the study owing to personal reasons after the first week. There were 14 patients in the experimental group (five myotonic dystrophy, three myopathy, two oculopharyngodistal myopathy, one desminopathy, one multiminicore disease, one
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
577
Aslan et al. Table 1. Patients’ characteristics.
Age (years) Gender (M/F) Body mass index (kg/m²) Disease duration (month) FVC (L) FVC (pred %) FEV1 (L) FEV1 (pred %) FEV1/FVC ratio MIP (cmH2O) MIP (pred %) MEP (cmH2O) MEP (pred %) SNIP (cmH2O) PCF (L/min)
Experimental (n = 14)
Sham (n = 10)
p value
31.6 (12.3) 8M 6F 19.5 (4.9) 110.4 (57.8) 2.1 (0.6) 55.0 (16.0) 1.9 (0.6) 57.4 (19.4) 87.8 (11.9) 50.2 (9.7) 50.9 (16.0) 45.7 (18.6) 26.3 (17.6) 44.7 (12.2) 254.2 (76.4)
26.5 (8.6) 2M 8F 18.8 (2.2) 123.4 (77.5) 2.7 (0.6) 80.1 (15.0) 2.3 (0.6) 81.7 (16.9) 88.8 (5.5) 48.3 (13.5) 55.7 (24.9) 39.8 (15.9) 28.5 (19.0) 39.5 (12.7) 292.0 (65.1)
0.2 0.07 0.6 0.6 0.5 0.4 0.2 0.1 0.8 0.5 0.02 0.03 0.0001 0.9 0.6
Data are presented as mean (SD). FEV1, forced expiratory volume in one second; FVC, forced vital capacity; MEP, maximal expiratory pressure; MIP, maximal inspiratory pressure; PCF, peak cough flow; SD, standard deviation; SNIP, sniff nasal inspiratory pressure.
Table 2. Effects of respiratory muscle training on spirometric measurements. Experimental (n = 14)
FVC (L) FVC (% pred) FEV1 (L) FEV1 (% pred) FEV1/FVC (%)
Sham (n = 10)
Between groups p value
Initial
8th week
Δ
Initial
8th week
Δ
2.1 (0.6) 55.0 (16.0) 1.9 (0.6) 57.4 (19.5) 87.9 (11.9)
2.2 (0.6) 56.7 (17.1) 2.0 (0.6) 59.5 (18.1) 87.4 (12.0)
0.09 (0.2) 1.6 (5.3) 0.1 (0.2) 2.1 (6.8) –0.4 (2.8)
2.7 (0.7) 80.1 (15.1) 2.3 (0.6) 81.7 (17.0) 88.8 (5.6)
2.5 (0.8) 71.5 (23.9) 2.2 (0.7) 74.2 (24.1) 88.7 (10.0)
–0.2 (0.7) –8.6 (24.4) –0.1 (0.7) –7.5 (26.7) –0.1 (9.1)
0.2 0.6 0.7 0.9 0.9
Data are presented as mean (SD). FEV1, forced expiratory volume in one second; FVC, forced vital capacity; SD, standard deviation; Δ, initial–final test differences.
facioscapulohumeral dystrophy, one congenital myopathy), and 10 patients in sham group (two myotonic dystrophy, three myopathy, two oculopharyngodistal myopathy, two Limb-Girdle muscular dystrophy, one spinal muscular atrophy Type 3). Patients’ characteristics are listed in Table 1. Two patients from the experimental group and one from the sham group were receiving non-invasive mechanical ventilation. No patient was on oxygen therapy and no one had comorbidities or hospitalization during the last year for respiratory problems.
The patients did not miss any hospital sessions and they were compliant at home according to their diaries. No side-effects were reported during the study. When the two groups were compared, there was no statistically significant change in initial–final test differences of spirometric measurements between the two groups (p > 0.05) (Table 2). The increase in initial–final test differences of maximum inspiratory pressure (cm H2O and % predicted), maximum expiratory pressure (cm H2O and % predicted), and sniff nasal inspiratory pressure
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
578
Clinical Rehabilitation 28(6)
Table 3. Effects of respiratory muscle training on respiratory mouth pressures, sniff nasal pressure, and peak cough flow. Experimental (n = 14) Initial 50.3 (9.7) MIP (cm H20) MIP (% pred) 50.8 (16.0) 45.8 (18.6) MEP (cm H20) MEP (% pred) 26.3 (17.6) SNIP (cm H20) 44.8 (12.3) PCF (L/min) 254.3 (76.4)
Sham (n = 10)
8th week
Δ
Initial
8th week
Δ
74.5 (16.6) 74.7 (23.7) 60.4 (25.3) 35.1 (23.3) 60.5 (17.3) 296.4 (90.3)
24.2 (13.7) 23.8 (14.7) 14.6 (11.1) 8.8 (7.6) 17.3 (15.6) 42.1 (38.7)
48.3 (13.5) 55.7 (25.0) 39.8 (15.9) 28.5 (19.0) 39.5 (12.7) 292.0 (65.1)
53.9 (20.4) 5.6 (10.8) 62.6 (37.5) 6.9 (14.7) 44.9 (20.5) 5.1 (6.8) 32.8 (26.2) 4.3 (7.9) 45.2 (14.1) 5.7 (5.1) 309.0 (69.5) 17.0 (20.0)
Between groups p value 0.002 0.003 0.04 0.03 0.04 0.07
Data are presented as mean (SD). MEP, maximal expiratory pressure; MIP, maximal inspiratory pressure; PCF, peak cough flow; SNIP, sniff nasal inspiratory pressure; SD, standard deviation; Δ, initial–final test differences.
were significantly higher in the experimental group (p < 0.05). The increase in initial–final test differences of peak cough flow was higher in the experimental group when compared with the sham group, but it was not found significant (p = 0.7) (Table 3).
Discussion In our study, we found significant increases in maximal inspiratory pressure, maximal expiratory pressure, and sniff nasal inspiratory pressure after eight weeks of inspiratory and expiratory muscle training in the experimental group when compared with the sham group. After training, there was no significant change in spirometric measurements (FVC, FEV1, FEV1/ FVC) between the two groups. The experimental group had a minimal increase in FEV1 and FVC % predicted, while the sham group had a decrease in eight weeks, which shows that training may have a role in stabilizing of pulmonary function test, or at least in delaying its decline. Koessler et al.10 investigated this fact in their study by giving 24 months of inspiratory muscle training to their patients with spinal muscular atrophy (nine patients) and Duchenne muscular dystrophy (18 patients). They stated that there was no significant decline in vital capacity after training and concluded that they have shown the effect of long-term training of inspiratory
muscle training on stabilization of vital capacity. Since it is regarded as a predictor of the need for mechanical ventilation, delaying its decline is an important conclusion. Many researchers studying inspiratory muscle training in neuromuscular disease have found that despite a significant increase in respiratory muscle strength, the same improvement was not observed for spirometric measurements.9–11 Wanke et al.9 found improvement only in respiratory muscle strength with six months of a inspiratory resistive device in patients with Duchenne muscular dystrophy. Koessler et al.10 used a similar training method to Wanke et al. and found improvement in maximum inspiratory pressure and 12 second maximum voluntary ventilation. Although the methods, patient diagnosis, and training periods of above studies were different from ours, the results were similar in showing the significant effect of training in strength of inspiratory muscles. Yeldan et al.11, compared the effects of threemonth inspiratory muscle training in patients with Limb Girdle and Becker muscular dystrophy. At the end of three months, the authors found an increase in maximal inspiratory pressure by using similar equipment and inspiratory muscle training protocol like our study and an increase in maximal inspiratory and expiratory pressure with respiratory exercises. The improvement in maximum inspiratory pressure was more significant in the inspiratory
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
579
Aslan et al. muscle training group, whereas there were no changes in spirometric data in both groups. The authors commented that there could have been a significant increase in maximal expiratory pressure if expiratory muscle training had been added to the inspiratory muscle training group. Our study confirms their findings. Although our training time was shorter than the studies mentioned, we still found a similar increase in maximum inspiratory pressure. There are only two publications about the effectiveness of using both inspiratory and expiratory muscle training at the same time in neuromuscular disease.19–20 One of these publications is a case report of myotonic dystrophy19 and the other one is a controlled study.20 Gozal et al.20 found significant improvement in respiratory muscles by inspiratory and expiratory muscle training in their controlled study on patients with Duchenne muscular dystrophy and spinal muscular atrophy. However, they reported that there was no change in pulmonary functions. They did not find any increase in respiratory muscle strength (inspiratory and expiratory) in their control group, which did not receive training. Our study differs from the above study with respect to training time, training intensity, and the control time. For instance, their training time was six months, whereas ours was eight weeks. In addition, they had used control group, whereas we used sham group trained with the lowest training load. We believe that our program of training, performed at home with support from hospital, supervised by a physiotherapist, and also the weekly control of the diaries, was effective in increasing the compliance of the patients to the training. This conclusion is confirmed by the data of the previously mentioned studies, which showed effective results with hospitalsupported home-based programs.9–11,19–20 We were unable to find a study in the literature investigating the effect of inspiratory and expiratory muscle training on peak cough flow in patients with muscular diseases. However, there is one study, in which the effect of expiratory muscle training on respiratory functions, including peak cough flow levels in healthy individuals, were investigated. In this study, Sasaki21 divided 33 patients into three groups; one group received training at the normal expiratory flow rate, one
group at the fast expiratory flow speed, and the third control group received no training. At the end of training there was a significant increase in maximum expiratory pressure levels in the two training groups when compared with the control group, while there was no difference between the two training groups. There was no improvement in respiratory functions and peak cough flow levels with expiratory muscle training. Our study is the first one to evaluate the effect of inspiratory and expiratory muscle training on peak cough flow in neuromuscular diseases, and we found that peak cough flow was higher in the experimental group when compared with the sham group, but there was no statistical significance (p = 0.07). Our study has some limitations. Designing a training study with neuromuscular diseases has many problems. Patients may differ with respect to diagnosis, involvement of muscle weakness, and rate of progression. It is difficult to obtain a reasonable number of patients having the same diagnosis and distribution of weakness. For this reason, although we know that it is a limitation for this study, we included patients with different diagnosis of neuromuscular disorders. However, we tried to homogenize our study sample by choosing neuromuscular diseases that have a slow progression rate. Our patient groups were small because we only included ambulatory patients to the study. Besides, some patients did not accept participation because they had transportation problems. Another limitation was that the “Threshold PEP” device used was limited to a maximum resistance of 20 cm H2O. This meant that some patients’ training intensity was below 30% of maximum expiratory pressure. Despite this handicap, we found a significant increase in maximum expiratory pressure in both groups. Literature reports that training intensity for inspiratory muscle training should be a minimum of 30% of maximum inspiratory pressure in order to reveal the effects of training,22 however, we were unable to find similar data for expiratory muscle training. This data is supported by our finding of no change in maximum inspiratory pressure, but improvement in maximum expiratory pressure with this level of intensity in the sham group. We investigated training effects of
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
580
Clinical Rehabilitation 28(6)
inspiratory and expiratory muscle training on pulmonary functions. We do not know whether these approaches have an effect on mobility or they prevent development of respiratory complications in these patient groups. This may also be a limitation of our study. We need more studies further investigating these topics. Our study demonstrates that an improvement of maximal inspiratory pressure (cm H2O and % predicted), maximal expiratory pressure (cm H2O and % predicted), and sniff nasal inspiratory pressure can be achieved in patients with slowly progressive muscular diseases after eight weeks of inspiratory and expiratory muscle training. However, there is a need for longer follow-up studies to evaluate how long this effect lasts.
Acknowledgements The authors give thanks gratefully to the technician of the pulmonary function test laboratory at the University Chest Diseases Clinic for spirometry and respiratory muscle strength measurements of patients. We also highly appreciate the editing support we received from Dr David Terence Thomas MD and Dr Kerem Gurses PhD in the first and second submissions, respectively.
Conflict of interest The author declares that there is no conflict of interest.
Funding This work was supported by the Istanbul University Research Fund (grant number 5561).
References Clinical messages • Inspiratory and expiratory muscle strength can be improved in patients with slowly progressive neuromuscular disease by eight weeks of inspiratory and expiratory muscle training. • The increased respiratory muscle strength did not improve lung function as measured by spirometry. • The program can be delivered at home with support from hospital.
Contributors GKA designed the study, implemented training of patients, drafted the manuscript and was involved in the final approval of the version to be published. HNG designed and coordinated the study, monitored its progress, analyzed and interpreted data, critically reviewed the manuscript and was involved in the final approval of this version to be published. HI was involved in designing the study and running the statistical analysis of the study and approved the final version of the manuscript to be published. EK was involved in designing the study, recruitment of the subjects, interpretation of data, critically reviewing the manuscript and the final approval of the version to be published.
1. Perrin C, Unterborn JN, Ambrosio CD and Hill NS. Pulmonary complications of chronic neuromuscular diseases and their management. Muscle Nerve 2004; 29: 5–27. 2. McCool FD and Tzelepis GE. Inspiratory muscle training in the patient with neuromuscular diseases. Phys Ther 1995; 75: 1006–1014. 3. Lynn DJ, Woda RP and Mendell JR. Respiratory dysfunction in neuromuscular dystrophy and other myopathies. Clin Chest Med 1994; 15: 661–674. 4. Benditt JO and Boitano LJ. Pulmonary issues in patients with chronic neuromuscular disease. Am J Respir Crit Care Med 2013; 10: 1046–1055. 5. Danov Z and Schroth MK. Pediatric management of pediatric patients with neuromuscular disease. Pediatr Ann 2010; 12: 769–776. 6. Ambrosino N, Carpene N and Gherardi M. Chronic respiratory care for neuromuscular diseases in adults. Eur Respir J 2009; 34: 444–451. 7. Polkey M, Lyall RA, Moxham J and Leigh PN. Respiratory aspects of neurological disease. J Neurol Neurosurg Psychiatry 1999; 66: 5–15. 8. Hull J, Aniapravan R, Chan E, et al. British Thoracic Society guideline for respiratory management of children with neuromuscular weakness. Thorax 2012; 67: i1–i40. 9. Wanke T, Toifle K, Merkle M, et al. Inspiratory muscle training in patients with Duchenne muscular dystrophy. Chest 1994; 105: 475–482. 10. Koessler W, Wanke T, Winkler G, et al. Two years experience with inspiratory muscle training in patients with neuromuscular disorders. Chest 2001; 120: 765–769. 11. Yeldan I, Gurses HN and Yuksel H. Comparison study of chest physiotherapy home training programmes on respiratory
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
581
Aslan et al. functions in patients with muscular dystrophy. Clin Rehabil 2008; 22: 741–748. 12. Nici L, Donner C, Wouters E, et al. American Thoracic Society; European Respiratory Society. ATS/ERS statement on pulmonary rehabilitation. Am J Respir Crit Care Med 2006; 173: 1390–1413. 13. Araújo TL, Resqueti VR, Bruno S, et al. Respiratory muscle strength and quality of life in myotonic dystrophy patients. Rev Port Pneumol 2010; 6: 892–898. 14. Graph Pad Software. Quick Calcs. http://graphpad.com/ quickcalcs/randomize2.cfm (October 2009). 15. Gauld LM and Boynton A. Relationship between peak cough flow and spirometry in Duchenne muscular dystrophy. Pediatr Pulmonol 2005; 39: 457–460. 16. Bianchi C and Baiardi P. Cough peak flows: Standard values for children and adolescents. Am J Phys Med Rehabil 2008; 87: 461–467.
17. Miller MR, Hankinson J, Brusasco V, et al. ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J 2005; 26: 319–338. 18. Black LF and Hyatt RE. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis 1969; 99: 696–702. 19. Fregonozi GAF, Resqueti VR and Casan P. Domiciliary respiratory muscle training in myotonic dystrophy. Arch Bronconeumol 2006; 42: 605–607. 20. Gozal D and Thiriet P. Respiratory muscle training in neuromuscular disease: long-term effects on strengt hand load perception. Med Sci in Sports Exerc 1999; 31: 1522–1527. 21. Sasaki M. The effect of expiratory muscle training on pulmonary function in normal subjects. J Phys Ther Sci 2007; 19: 197–203. 22. Gosselink R. Physiotherapy in respiratory disease. Breathe 2006; 3: 31–39.
Downloaded from cre.sagepub.com at Univ of Newcastle upon Tyne on December 5, 2016
