Purpose: The aim of this study was to assess the usefulness of a specific inspiratory muscle training in Duchenne muscular dystrophy (DMD).
Patients and methods: Fifteen patients with DMD started 6 months of training the inspiratory muscles and 15 patients served as a control group. Pulmonary and inspiratory muscle function parameters were assessed 3 months before and at the beginning of training, in the first and third month of training, at the end, and 6 months after its cessation. Maximal sniff assessed esophageal and transdiaphragmatic pressure values served as indices for global inspiratory muscle strength and diaphragmatic strength, respectively. Inspiratory muscle endurance was assessed by the length of time a certain inspiratory task could be maintained.
Results: In 10 of the 15 patients, respiratory muscle function parameters improved significantly after 1 month of training. Further improvements were to be seen after 3 and after 6 months. Even 6 months after the end of traning, those effects remained to a large extent. In the other five patients, there was no such improvement after 1 month of training, which was therefore discontinued. All these five patients had vital capacity values of less than 25 percent predicted and/or [PaCO.sub.2] values of more than 45 mm Hg. The 15 control patients had no significant change in their respiratory muscle function parameters.
Conclusion: We conclude that a specific inspiratory muscle traning is useful in the early stage of DMD.
One of the main problems in the treatment of patients with neuromuscular diseases is the progressive impairment of inspiratory muscle function. Since chest wall and pulmonary compliance are reduced in neuromuscular diseases, the mechanical load on the weakened respiratory muscles is increased. Imbalance between load and capacity of the respiratory muscles may lead to fatigue and respiratory failure, which is the most important cause of death in these patients. Therefore, the treatment of diseased respiratory muscles to improve their strength and endurance presents a great challenge in the treatment of patients with neuromuscular diseases. Pharmacologic theraphy was reported to possibly strengthen the respiratory muscles and make them less susceptible to fatigue. Also, periodic respiratory muscle rest and training were used to prevent the decline in respiratory muscle function.
Previous studies have shown that strength and endurance of the respiratory muscles can be improved through specific training programs in normal subjects, patients with COPD, patients with cystic fibrosis, and quadriplegics. However, the role of inspiratory muscle training remains controversial in patients with neuromuscular diseases. On the one hand, it is alleged that inspiratory muscle training is potentially hazardous, since it may accelerate fatigue in the already very weak respiratory muscles by overwork and therefore cannot be recommended. On the other hand, improvement of inspiratory muscle function by specific training programs has been reported, but these studies were uncontrolled.[6,12] The question of whether the use of inspiratory muscle training is sensible remains unanswered. And if the answer is yes, when should we intervene in the course of the patient's disease?
The goal of our study is to answer the following questions: (1) Does respiratory muscle training in patients with Duchenne muscular dystrophy (DMD) improve inspiratory muscle function or does it do more harm? (2) Does the severity of the existing pulmonary function impairment affect the obtainable training effects?
Thirty patients with DMD participated in our study. Before entering the study, they were randomly assigned to receive or not receive inspiratory muscle training. The age in the training group ranged from 10 to 24 years (mean, 13.6 [+ or -] 4.5 years), in the control group from 9 to 20 years (mean, 14.5 [+ or -] 3.8 years); all had the onset of their disease between 3 and 5 years of age. In the training group, 12 patients, and in the control group, 11 patients were wheelchair bound, corresponding to functional capacity stage 9, according to the criteria of Inkley et al. All patients were free from respiratory tract infections. None of them had symptoms or signs of inspiratory muscle fatigue, such as exertional dyspnea, orthopnea, or paradoxic breathing, which are obligatory indications for rest. No patient described sleep disturbance, daytime hypersomnolence, or morning headache, and none had an episode of acute respiratory failure requiring endotracheal ventilation. The diagnosis of DMD had been made on clinical, enzymatic, electromyographic, and muscle biopsy specimen criteria. Informed consent was obtained from all subjects and the study was approved by the Human Subject Committee of the hospital.
For this study, a special training apparatus was constructed to enable the patient to actually adhere to the prescribed training intensity. In addition, the number of correctly and incorrectly performed exercises was stored by the apparatus to give the physician the possibility to control the training of the patient.
The training apparatus enabled the patient to do resistive breathing maneuvers against a variable inspiratory resistance or maximal static inspiratory efforts against the almost occluded resistance. Room air was breathed through a mouthpiece, a two-way non-rebreathing valve of low resistance, a 3-cm-long plastic tube, a pneumotachograph, and a variable alinear inspiratory resistance. Inspiratory flow was measured with the pneumotachograph connected to a differential pressure transducer (Honeywell 163 PC, Freeport, Ill). The training equipment was kept in a small collapsible case. In the bottom half of the case, the mouthpiece, the two-way valve, and the short plastic tube were kept. The pneumotachograph and the alinear resistor were fixed in this part of the case. In addition, there was a slot for a videogame cassette that could be opened if the training was successful. The possibility to play a videogame as a reward could motivate the patients not to interrupt the training prematurely. To provide a visual control of the performance, there were two vertical LED displays fixed to the inside of the upper half of the case. One one display, the patient was shown breath by breath the inspiratory airflow (in arbitrarily chosen units). During the loaded breathing runs, each breath had to reach an exact minimal value. On the other display, the patient would be shown by the indicator if he had achieved the preset minute volume (VE) while breathing against the inspiratory resistance. Two lights beside the displays served as visible cues for maintaining breathing frequency (fb). During the maximal static inspiratory effort maneuvers against the almost completely occluded resistance, the generated negative pressure was displayed in arbirary units in place of inspiratory airflow. A small leak prevented the patients from using the buccal muscles for generating negative pressures. Pressures were measured with a [+ or -] 300 cm [H.sup.2]O differential pressure transducer (model 142 PC, Honeywell, Freeport, Ill). On a side wall of the case, there was a switch with which one could select one of the two training programs. The resistance was automatically set at the desired level when the switch was in the "program I" position. In the "program 2" position, the resistance was almost completely closed.
Inspiratory Muscle Training at Home
At home, patients had to perform both resistive breathing maneuvers and maximal static inspiratory efforts against the almost occluded resistance. Training was done in the sitting position and a noseclip was used. The inspiratory resistive breathing training consisted of ten loaded breathing cycles of 1-min duration each, with 20-s intervals between them, twice daily. The level of the inspiratory resistance was adjusted in the hospital. During the 1-min resistive breathing cycle, if the minimal airflow value was not achieved more than two times, a warning signal on the training apparatus would be shown to the patient and the cycle had to be repeated. The same happened if the desired VE was not achieved. Thus, each patient had to correctly complete ten resistive breathing cycles twice a day. The number of correctly and incorrectly performed exercises was stored in the apparatus. Fifteen minutes after the resistive breathing training, the patients had to perform ten maximal static inspiratory efforts and reach a certain minimal pressure value, which was determined in the hospital. A 20-s interval between the maneuvers was allowed. When the minimal pressure value was not achieved, this maneuver had to be repeated, until a total of ten maneuvers were performed correctly. The number of correctly and incorrectly performed efforts was stored in the apparatus.
Pulmonary Function Tests: Pulmonary function measurements and blood gas analysis were performed 3 months before and at the beginning of training, in the first and third month of training, at the end, and 6 months after its cessation. All mesurements were done in the sitting position. The vital capacity (VC), the forced expiratory volume in 1 s ([FEV.sub.1]), and the 12-s maximum voluntary ventilation test (12s-MVV) were measured three times on a computerized spirometer (Jaeger, Wurzburg, Germany). The best trial was used for further analysis. In patients with scoliosis, armspan was used for determining percent predicted values according to the method of Johnson and Westgate. The expected normal values were those reported by Forche. Capillary blood collected from an earlobe was used for estimating oxygen and carbon dioxide tension in the arterial blood.
Inspiratory Muscle Strength: Maximal sniff assessed esophageal (Pesmax) and transdiaphragmatic pressure (Pdimax) values served as parameters for global inspiratory muscle stength and diaphragmatic strength respectively. Sniffs were carried out at resting end-expiration. Transdiaphragmatic pressure (Pdi) was measured with flexible double-lumen catheters. The catheters were specially adapted for the height of the patients so that it was possible to place the distal lumen slightly below the cardia (about 50 to 60 cm from the nostrils) and the proximal lumen in the middle third of the esophagus (about 30 to 40 cm from the nostrils). The catheters were perfused with distilled water at a constant flow of 25 ml/h. The proximal ends were coupled to pressure transducers (Gould-Statham, P23ID, Cleveland). The catheter-pressure transducer system was described in detail previously. The Pdi was calculated by subtracting esophageal pressure (Pes) from the gastric pressure (Pga) by an electronic subtraction circuit. The Pes, Pga, and Pdi were displayed on-line on a four-channel paper recorder (Beckman 511 A, Fullerton. Calif). The Pes, Pga, and Pdi were arbitrarily assigned zero at the start of each sniff trial. Thus, only the change in pressure from the initial position was determined for each sniff. An interval of 30 to 40 s was allowed between each sniff and the best of a total of ten maneuvers was used for analysis.
Inspiratory Muscle Endurance: The patients were instructed to breathe continuously in cycles at a certain level of inspiratory resistance for 1 min, followed by 20 s of rest. The test was terminated when the Pdi could not be sustained at the target level for three consecutive breaths or when a total of 20 resistive breathing cycles were completed by the patient. The cumulative time of these maneuvers (TE) served as a parameter for inspiratory muscle endurance. A single-lead ECG was monitored throughout the maneuvers. The blood gas values assessed immediately after the resistive breathing cycles showed no worsening in oxygen tension or increase in [CO.sub.2] tension in any patient.
Three months before and at the beginning of training, in the first and third month of training, at the end, and 6 months after its cessation, inspiratory muscle strength and endurance were assessed in both groups. Additionally, serum creatine kinase measurements were done to detect possible muscular damage caused by training. To analyze inspiratory muscle endurance, the initial resistance was adjusted in such a way that 70 percent of the Pdimax value had to be generated with each breath at normal resting flow rates. The VE and fb had to correspond to the resting VE and fb, which were assessed earlier over a 10-min time span, during which the patients breathed quietly through the unloaded circuit. The Pes, Pga, and Pdi were recorded online on the paper-recorder to ensure that 70 percent of the Pdimax was generated breath by breath. When the given resistance could be tolerated for more than 15 cycles, the level of resistance was increased to 80 percent of the Pdimax. When it was tolerated for less than 12 cycles, the level was decreased to 60 percent of the Pdimax. For the training patients, the level of resistance was adjusted each month anew, if the patients could meanwhile achieve higher Pdimax values or sustain more than 15 resistive breathing cycles. The hospital-adjusted level of resistance was used for training at home. The mean of the five highest pressure values during ten maximal static inspiratory efforts against the almost occluded airway was used as the minimal pressure value which had to be reached during such efforts at home. This value had to be adjusted each month anew, if the patients could meanwhile achieve higher mean pressure values. If a training patient showed no improvement in the inspiratory muscle function parameters after 1 month of training, he met our discontinuation criterion and was excluded from the study, since significant improvement should have occurred within 1 month.
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The baseline parameters of the two groups were compared by means of the Mann-Whitney test. The changes during the training period within one group were compared by the Wilcoxon test. The Spearman rank correlation coefficient was used to test the relationship between improvement in respiratory muscle strength and endurance and baseline levels of VC.
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Table 1 lists the pulmonary and blood gas values 3 months before and at the beginning of training, and 6 months after cessation of training in the study patients and control groups. The mean values of VC and [FEV.sub.1], either expressed as absolute values or in percent predicted, were not significantly different in the two groups. The same was true for 12s-MVV, [PaO.sub.2] and [PaCo.sub.2]. None of the patients showed a significant change in the VC and 12s-MVV values within the observation period (Table 1).
Five of the 15 training patients discontinued the training after 1 month because the inspiratory muscle function parameters had not improved. All these five patients had VC values less than 25 percent of predicted and/or a [PaCO.sub.2] of more than 45 mm Hg, indicating severe pulmonary function impairment. We analyzed the effects of training on inspiratory muscle function in these five patients separately from the remaining ten training patients. In the control group, 3 of the 15 patients showed VC values less than 25 percent of predicted and/or a [PaCO.sub.2] of more than 45 mm Hg. Inspiratory muscle function parameters of these three were therefore analyzed separately from the other 12 control patients. Two months before the end of the observation period, one of those three control subjects received nighttime positive pressure ventilation via nose mask because of rising [CO.sub.2] retention. Two weeks before the end of the study, one of the five training patients with severe pulmonary function impairment developed acute respiratory failure due to pneumonia so that ventilation had to be supported via tracheostomy. These two patients were excluded from the study from the moment they received assisted ventilation.
At the beginning of the study the Pesmax and Pdimax values were not significantly different in the two groups (Fig 1, Table 2). After the 6-month training period, however, the ten patients who completed the training had significantly higher Pesmax and Pdimax values than the 12 control subjects without severe functional impairment (p [less than] 0.001) (Fig 1, Table 2). At the end of training the mean Pesmax and Pdimax values were 5.59 [+ or -] 0.98 kPa and 6.61 [+ or -] 1.16 kPa, respectively, for the 10 training patients; 3.38 [+ or -] 1.18 kPa and 4.12 [+ or -] 1.11 kPa, respectively, for the 12 controls. The 12 controls without severe pulmonary function impairment, the 5 training, and the 3 control patients with severe impairment showed no significant change of Pesmax and Pdimax values during the observation period (Fig 1, Table 2). The effects of training on inspiratory muscle endurance are shown in Table 3. In the ten patients who completed the training, the endurance time increased significantly (Table 3). The reasons for terminating the test are also listed in Table 3. It should be noted that in the ten patients who completed the training, the target pressure during the resistive breathing tests increased during the training period. This means that the inspiratory task which could be sustained increased. In these ten patients, a pressure/endurance-time product was calculated by multiplying the created Pdi by TE to compare the work capacity of the inspiratory muscles before and at the end of training. The mean pressure-time product increased from 2678 kPa[multiplied by]s to 5500 kPa[multiplied by]s (p [less than] 0.001) (Fig 2).
In the ten patients who completed the training, no relationship existed between the degree of improvement in respiratory muscle strength and endurance following training and the baseline levels of VC. The number of incorrect exercises did not significantly differ in the five training patients with severe pulmonary function impairment from that of the remaining ten training patients. Within the 1-month training period, the number of incorrect resistive breathing trials and static inspiratory effort maneuvers were 38.3 [+ or -] 21.6 and 40.1 [+ or -] 18.5, respectively, for the five training patients with severe pulmonary function impairment; 32.9 [+ or -] 11.7 and 35.2 [+ or -] 12.5, respectively, for the remaining ten training patients. None of the patients finished the training prematurely so that the prescribed number of correctly performed exercises was reached by all patients.
The sniff maneuvers were performed by all patients without difficulties. In all patients, a plateau of peak sniff Pdi was reached within four to six sniffs. No further increase in Pdimax was observed during the remaining four to six sniff maneuvers.
The individual maximal variation was not more than 2.0 kPa for Pdi performed during all ten sniff maneuvers and less than 0.4 kPa for Pdi performed during the last four to six of the ten sniff maneuvers. The contribution of esophageal and gastric pressure to sniff Pdi varied among patients, though none had a negative Pga at peak Pdi. A trend toward higher blood creatine kinase levels could not be detected in any patient during the observation period.
Our study shows the following results:
(1) In patients with DMD, respiratory muscles and in particular the diaphragm, are trainable in terms of strength and endurance, provided that their ventilatory function is not severely restricted.
(2) In patients with VC values less than 25 percent predicted and/or a [PaCO.sub.2] of more than 45 mm Hg, a specific training of the inspiratory muscles does not produce any benefit. On the other hand, a damaging effect could be excluded, at least for a training period of 1 month.
The significance of skeletal muscle training in patients with neuromuscular disease is controversial. There is a scarcity of data regarding whether or not diseased muscles can be strengthened by specific training programs at all, much less the exact extent and stage of the disease at which skeletal muscles can be strengthened. In one patient with Duchenne dystrophy, histologic examination showed that those muscles assuming the least degree of sustained physical activity had the least degeneration, implying that physical activity hastened muscle fiber degeneration. It was therefore suspected that overwork or heavy exercise may accelerate skeletal muscle weakness in neuromuscular disease.
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Our study, however, shows that strength and endurance of the inspiratory muscles can be improved by selective training, provided that the patient's ventilatory function is not severely impaired. The results of our study therefore differ substantially from other earlier studies. It may be that none of these published studies has examined how training actually stresses the inspiratory muscles and the diaphragm.[6,12,21-24] In patients where the pressures generated by the inspiratory musculature have been measured, these were only obtained at the beginning and at the end of the training.[6,21-23] It has to be stated that measurement of maximal inspiratory mouth pressure, though it is widely used, cannot be recommended in all cases. Especially patients with weak mouth and cheek muscles tend to have difficulties with this method and, besides, the normal range is quite wide. To our knowledge, ours is the first controlled study that evaluates the global inspiratory muscle function and the diaphragmatic function selectively using maximal sniff assessed esophageal and transdiaphragmatic pressure values, respectively. For the measurement of global inspiratory muscle strength and the strength of the diaphragm, the sniff maneuver without a noseclip has turned out to be a reliable and reproducible technique.[16,17] Another advantage is that most patients, even those with weakness of the cheek muscles, can easily perform the maneuvers.
Many previous authors have failed to document improvement in strength and endurance of the respiratory muscles by training because they could not make sure that the subjects truly performed the prescribed work.[6,11,22,23] Since airflow and minute ventilation were not controlled during the training, the patients could minimize the work of breathing through resistive orifices by reducing inspiratory flow and breathing frequency. The stimulus for training in these studies could have been too weak. In our study, inspiratory airflow and VE were measured continuously to ensure that the work of breathing remained constantly high.
Although the strength and endurance of the inspiratory muscles improved with training, the pulmonary function parameters, especially VC and 12s-MVV, did not change. Similar effects were reported by Chen and coworkers and by Flynn and associates in patients with COPD during respiratory muscle training. Pulmonary function testing is known to be an insensitive parameter of inspiratory muscle function. The 12s-MVV test is influenced by many factors and it may therefore fail to distinguish inspiratory muscle dysfunction from other causes for its impairment.
In our study, training not only improved diaphragmatic and global inspiratory muscle function, but nearly all of the adaptation gained from training was also retained 6 months after the cessation of the training. Healthy young subjects who had 4 or 5 weeks of training lost at least 50 percent of the gain after 8 to 15 weeks of no training. Belman and Gaesser have shown in normal elderly subjects that almost all the adaptations gained from 8 weeks of training were retained 2 months after its cessation. It is therefore very likely that the adaptations in ventilatory muscles become greater with increased training period.
In patients with severely impaired ventilatory function (VC values less than 25 percent predicted and/or a [PaCO.sub.2] [greater than] 45 mm Hg), inspiratory muscle training proved to be ineffective. Many factors can account for this.
(1) The intensity of our training program could be too low. This program proved to be effective, however, in the remaining ten training patients. Besides, Larson and coworkers showed that even breathing with a pressure threshold device at inspiratory pressure loads 30 percent of the maximum led to improvement of inspiratory muscle function.
(2) The intensity of our training program could be too high. The diseased muscles work against noncompliant structures, and they may already approach the threshold of fatigue. The weakened muscle may be more susceptible to damage and fiber splitting; this could be even furthered by training, but the sniff-assessed Pes and Pdi values obtained after 1 month of training did not give evidence of inspiratory muscle exhaustion. No changes in blood creatine kinase levels further suggest no deleterious effects of training on inspiratory muscles.
(3) There may not be enough functional muscle mass remaining in severely ill patients to allow measurable improvement in muscle function by specific training programs. Aldrich and Uhrlass, however, have shown that even in severe respiratory failure, respiratory muscles can be trained successfully in a patient with muscular dystrophy. In this report, muscle resistive training was combined with respiratory muscle rest in the form of intermittent mandatory ventilation. Most likely our training program has been proved ineffective in the five patients with severe functional impairment since
(4) No alternating training and rest of respiratory muscles took place. Alternating rest and exercise might improve respiratory muscle function in this group of patients.
Improved inspiratory muscle function may have important clinical implications. If higher respiratory loads can be sustained without the development of respiratory muscle exhaustion, ventilatory failure may be delayed or prevented. Although the advantages of improved inspiratory muscle function are obvious, it is certainly not easy to motivate especially young patients for the training. Respiratory muscle training is considered cumbersome, boring, and without immediate awards, so that it is very unlikely that many patients will use it long enough to reap the benefits. As a reward, our training equipment provided a video game. Incorrect exercises were easily identified so that they could be repeated without much waste of time, and patients could complete their exercises quickly. A further advantage was that training could be done at home, without abandoning an exact monitoring of the training. This complies with the ideal that patients with DMD be treated on an outpatient basis, with admissions to the hospital kept to a minimum.
The results of our study justify a specific inspiratory muscle training program for patients with DMD, provided that it is instituted early in the course of the disease.
 Smith PEM, Calverley PMA, Edwards RHT, Evans GA, Campbell EJM. Practical problems in the respiratory care of patients with muscular dystrophy. N Engl J Med 1987; 316:1197-1205
 Rochester DF, Arora NS. Respiratory muscle failure. Med Clin North Am 1983; 67:573-97
 Inkley SR, Oldenburg FC, Vignos RJ. Pulmonary function in Duchenne's muscular dystrophy related to stage of disease. Am J Med 1974; 56:297-306
 Schiffman PL, Belsh JM. Effect of inspiratory resistance and theophylline on respiratory muscle strength in patients with amyotrophic lateral sclerosis. Am Rev Respir Dis 1989; 139:1418-23
 Baydur A, Gilgaff I, Prentice W, Carlson M, Fischer DA. Decline in respiratory function and experience with long-term assisted ventilation in advanced Duchenne's muscular dystrophy. Chest 1990; 97:284-89
 DiMarco AF, Kelling JS, Dimarco MS, Jakobs I, Shields R, Altose MD. The effects of inspiratory resistive training on respiratory muscle function in patients with muscular dystrophy. Muscle Nerve 1985; 8:284-90
 Leith DE, Bradley M. Ventilatory muscle strength and endurance training. J Appl Physiol 1976; 41:508-16
 Harver A, Mahler DA, Daubenspeck JA. Targeted inspiratory muscle training improves respiratory muscle function and reduces dyspnea in patients with chronic obstructive pulmonary disease. Ann Intern Med 1989; 111:117-24
 Keens TG, Krastin IRB, Wannamaker EM, Levison H, Crozier DN, Bryan AC. Ventilatory muscle endurance training in normal subjects and patients with cystic fibrosis. Am Rev Respir Dis 1977; 116:853-60
 Gross D, Ladd HW, Riley EJ, Macklem PT, Grassino A. The effect of training on strength and endurance of the diaphragm in quadriplegics. Am J Med 1980; 68:27-33
 Smith PEM, Coakley JM, Edwards RHT. Respiratory muscle training in Duchenne muscular dystrophy. Muscle Nerve 1988; 11:784-85
 Siegel IM. Pulmonary problems in Duchenne muscular dystrophy: diagnosis, prophylaxis and treatment. Phys Ther 1975; 55:160-62
 Rochester DF, Martin LL. Respiratory muscle rest. In: Roussos CH, Macklem PT, eds. The thorax, part B. New York: Marcel Dekker Inc, 1985; 1303-28
 Johnson BE, Westgate HD. Methods of predicting vital capacity in patients with thoracic scoliosis. J Bone Joint Surg 1970; 52A:1433-39
 Forche G. Austrian reference values for spirometry. Wien Klin Wochenschr 1986; 99:136s
 Laroche CH, Mier AK, Moxham J, Green M. The value of sniff esophageal pressures in the assessment of global inspiratory muscle strength. Am Rev Respir Dis 1988; 138:598-603
 Mier-Jedrzejowicz A, Brophy C, Moxham J, Green M. Assessment of diaphragm weakness. Am Rev Respir Dis 1988; 137:877-83
 Wanke T, Schenz G, Zwick H, Popp W, Ritschka L, Flicker M. Dependence of maximal sniff generated mouth and transdiaphragmatic pressures on lung volume. Thorax 1990; 45:352-55
 Bonsett CA. Pseudohypertrophic muscular dystrophy: distribution of degenerative features as revealed by anatomical study. Neurology 1963; 13:728-38
 Johnson EW, Braddom R. Over-work weakness in facioscapulohumeral muscular dystrophy. Arch Phys Med Rehabil 1971;52:333-36
 Stern LM, Martin AJ, Jones N, Garret R, Yeates J. Training inspiratory resistance in Duchenne dystrophy using adapted computer games. Dev Med Child Neurol 1989; 31:494-500
 Rodillo E, Noble-Jamieson CM, Aber V, Heckmatt JZ, Muntani F, Dubowitz V. Respiratory muscle training in Duchenne muscular dystrophy. Arch Dis Child 1989; 64:736-38
 Martin AJ, Stern L, Yeates J, Lepp D, Little J. Respiratory muscle training in Duchenne muscular dystrophy. Dev Med Child Neurol 1986; 28:314-18
 Houser CR, Johnson DM. Breathing exercises for children with pseudohypertrophic muscular dystrophy. Phys Ther 1971; 51:751-59
 Belman MJ, Thomas SG, Lewis MI. Resistive breathing training in patients with chronic obstructive pulmonary disease. Chest 1986; 90:662-69
 Chen HI, Dukes R, Martin BJ. Inspiratory muscle training in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1985; 131:251-55
 Flynn MG, Barter CE, Nosworthy JC, Pretto JJ, Rochford PD, Pierce RJ. Threshold pressure training, breathing pattern and exercise performance in chronic airflow obstruction. Chest 1989; 95:535-40
 Smeltzer SC, Skurnick JH, Traiano R, Cook SD, Duran W, Lavietes MM. Respiratory function in multiple sclerosis: utility of clinical assessment of respiratory muscle function. Chest 1992; 101:479-84
 Baydur A. Respiratory muscle strength and control of ventilation in patients with neuromuscular disease. Chest 1991; 99:30-8
 Belman MJ, Gaesser GA. Ventilatory muscle training in the elderly. J Appl Physiol 1988; 64:899-905
 Larson JI, Kim MJ, Sharp JT, Larson DA. Inspiratory muscle training with a pressure threshold breathing device in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1988; 138:689-95
 Aldrich TK, Uhrlass RM. Weaning from mechanical ventilation: successful use of modified inspiratory resistive training in muscular dystrophy. Crit Care Med 1987; 247-49
 Braum NMT, Faulkner J, Hughes RL, Roussos CH, Sahgal V. When should respiratory muscles be exercised? Chest 1983; 84:75-84
 Aldrich TK. The application of muscle endurance training techniques to the respiratory muscles in COPD (review). Lung 1985; 163:15-22
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