Resistive inspiratory muscle training in subjects with chronic cervical spinal cord injury

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Resistive Inspiratory Muscle Training in Subjects With Chronic Cervical Spinal Cord Injury Alyssa Rutchik, MS, PT, Ann R. Weissman, MS, PT, Peter L. Almenoff, MD, Ann M. Spungen, EdD, William A. Bauman, MD, David R. Grimm, EdD ABSTRACT. Rutchik A, Weissman AR, Almenoff PL, Spungen AM, Bauman WA, Grimm DR. Resistive inspiratory muscle training in subjects with chronic cervical spinal cord injury. Arch Phys Med Rehabil 1998 ;79:293-297.

Objective: To determine whether pulmonary function, respiratory muscle strength, and dyspnea can be improved in individuals with chronic cervical spinal cord injury (SCI). Study Design: Ten subjects participated in an 8-week resistive inspiratory muscle training (IMT) program for 15 minutes twice daily. Spirometry, lung volumes, maximum inspiratory pressure (MIP), maximum expiratory pressure (MEP), and dyspnea were measured at baseline, week 4, and week 8. Six months after the study, spirometry, MIP, and MEP were re-measured in a subgroup of the original participants. Results: We found that regular IMT in subjects with cervical SCI significantly improved forced vital capacity (means +_ SE) (11% + 2.82% increase), forced inspiratory vital capacity (21% -+ 6.91%), vital capacity (8% -+ 4.36%), total lung capacity (12% -+ 3.23%), functional residual capacity (15% -+ 5.96%), and MIP (24% -- 6.98%) (p < .05). Furthermore, although no statistical differences were observed for the dyspnea scale, the fact that subjects reported decreased levels (43% + 21.30% reduction) of perceived difficulty breathing may be of greater importance. No significant differences from baseline values were found in the seven subjects whose spirometry and respiratory muscle strength were measured 6 months after the study. Conclusions: Our findings suggest that in individuals with cervical SCI regular resistive IMT may result in decreased restrictive ventilatory impairment and reported dyspnea and, thus, reduced incidence of chronic respiratory complaints, respiratory infection, and other pulmonary complications.

© 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation COMPLICATIONS remain one of the prip ULMONARY mary causes of morbidity and mortality among individuals with cervical spinal cord injury (SCI), both in the first year after injury and chronically, t-3 Paralysis of respiratory muscles is directly associated with restrictive ventilatory impairment, the

From the Medical Service, Veterans Affairs Medical Center, Bronx (Drs. Almenoff, Bauman); Departments of Medicine (Drs. Almenoff, Spungen, Bamnan, Grimm) and Rehabilitation Medicine (Drs. Spungen, Bauman), Spinal Cord Damage Research Center, Mount Sinai Medical Center; and College of Physicians & Surgeons of Columbia University (Ms. Rutchik, Ms. Weissman), New York, NY. Submitted for publication May 14, 1997. Accepted in revised form August 18, 1997. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to David R. Grimm, EdD, Veterans Affairs Medical Center, Spinal Cord Damage Research Center, Rm. IE-02, 130 West Kingsbridge Road, Bronx, NY 10468. © 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/98/7903-450653.00/0

severity of which correlates inversely with the level of spinal lesion. SCI with the neurologic level C3 through C7 generally results in a weakened diaphragm and paralysis of the external (parasternals) and internal intercostals and abdominal musculature, along with partial to complete denervation of most of the accessory muscles of breathing, all resulting in significant impairment of respiratory function. Additionally, the individual with cervical SCI is unable to generate a cough forceful enough to clear mucus secretions and infection. 4 Moreover, reduced lung volumes and the associated inadequate stretch of airway smooth muscle with deep breathing may contribute to dyspnea, further limiting an individual from progressing in vocational and avocational independent activities. 5,6 Previous investigators have found that the strength and endurance of respiratory muscles in individuals with acute and chronic SCI may be further increased with specific resistive inspiratory muscle training (IMT), 7:~° suggesting this may help to protect against respiratory infections, which in severe instances can evolve into respiratory failure. In addition, IMT has been shown to be beneficial in weaning individuals with high cervical spinal injuries from mechanical ventilation. 11,12 Although Gross and coworkers 8 reported evidence of symptomatic improvement in dyspnea in subjects with tetraplegia during an IMT study, this respiratory complaint has not been adequately examined after IMT. The purpose of the study herein was to assess the effects of regular daily use of a resistive IMT on respiratory muscle strength, pulmonary function, and levels of perceived difficulty breathing in stable subjects with chronic cervical SCI.

SUBJECTS AND METHODS The study group consisted of 10 men with chronic SCI at the neurologic level of C4 through C7, with duration of injury greater than 1 year. Subjects had no preinjury history of pulmonary disease or respiratory symptoms, none reported recent or active pulmonary infection, and none were receiving medications known to alter airway tone. Our medical center's review board granted approval for the study. Informed consent of each subject was obtained before the investigation. Subjects trained with a resistive IMT. a Training consisted of subjects seated in their wheelchair breathing at normal tidal volumes, and wearing a noseclip with the IMT initially set at the lowest resistance level (the largest orifice) for two 15-minute sessions daily. Upon completion of each session, subjects entered into their diaries the time of day, training duration, resistance level (1 to 6), and perceived difficulty breathing (modified Borg scale). Each subject was instructed to increase the resistance one orifice at a time only when completion of two consecutive 15-minute sessions resulted in a modified Borg scale reading of 2 or less. Spirometry, lung volumes, maximum inspiratory pressure (MIP), and maximum expiratory pressure (MEP) were measured at the beginning of the study, then repeated at weeks 4 and 8. In seven subjects, spirometry, MIR and MEP were measured at least six months after the study. Pulmonary function measures were obtained using a model 2200 automated pulmonary Arch Phys Med Rehabil Vol 79, March 1998

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function lab, b with subjects seated in their wheelchairs. Baseline values of forced vital capacity (FVC) and forced expiratory volume in 1 second (FEVI) were obtained for each subject according to the recommendations of the American Thoracic Society, 13 Spirometry results were expressed as absolute values and percent predicted based upon the standards of Morris and colleagues. 14Lung volumes were determined using the nitrogen washout technique. 15 Respiratory muscle strength measures (MIP and MEP) were obtained using an electronic portable Mouth Pressure Meter ° from the best of three maximum efforts, each effort beginning from functional residual capacity (FRC) and total lung capacity (TLC), respectively. A standard respiratory symptoms and history questionnaire 16 modified for individuals with limited mobility was administered to each subject at baseline, and the breathlessness section of the questionnaire was re-administered at weeks 4 mad 8. The subjects' responses to activity and environmental changes throughout the study were assessed by this survey. Resting dyspnea was quantified before each testing session by use of the modified Borg scale, 17,1s in which each level includes a verbal descriptor to assist subjects in rating the intensity of their dyspnea. All data were expressed as means -+ SE. A paired student t test was performed to measure absolute and percentage change differences between baseline and week 8, in addition to change from baseline to 6-month poststudy values for all pulmonary parameters (p < .05). An unpaired t test was also used to assess differences in mean pulmonary values and respiratory strength measures for subjects whose compliance was 75% more than that of the less compliant subjects. Nonlinear regression analysis was also applied to determine the relationship in absolute values among pulmonary function, respiratory muscle strength, and dyspnea tests. RESULTS Characteristics of the subjects are shown in table 1. Subject compliance was calculated by dividing the total number of completed training sessions by the total number possible (112) and multiplying by 100. All subjects completed the entire 8-week study and none missed more than eight consecutive training sessions; compliance ranged from 48% to 100%. Individuals whose compliance exceeded 75% demonstrated slightly higher mean pulmonary values at week 8 for most parameters; however, these values were not statistically different from those of the less compliant subjects. A summary of the mean pulmonary function and respiratory strength measures for baseline, weeks 4 and 8 are presented in table 2. All pulmonary measures showed trends toward improve-

ment, although not all were significantly different from baseline. More specifically, at week 8, these respiratory strength and pulmonary function measures showed significant improvement from baseline: MIP (66.2 2 5.42 vs 78.5 2 3.62cmH20), FVC (2.81 +_ .27 vs 3.07 + .26L), forced inspiratory vital capacity (FIVC) (2.60 2 . 2 6 vs 3.00-+ .28L), TLC (5.17 2 . 1 1 vs 5.71 +_ .22L), vital capacity (VC) (2.90 2 . 2 6 vs 3.10 2.27L), and FRC (2.52 2 . 1 5 vs 3.13 + .16L). No significant differences for any of the parameters were observed at week 4 compared with baseline, although a general trend toward improvement was noted (table 2). The mean percentage increase from baseline to week 8 was significant (p < .05) for all pulmonary function and respiratory strength parameters except residual volume (RV) and FEV1 (fig 1). Furthermore, although no statistical difference was observed for resting dyspnea using the modified Borg scale, subjects generally reported reduced levels of perceived difficulty breathing, with a mean improvement over baseline values of 43% + 21.30% (fig 1). In the seven subjects whose spirometry (FVC, FEV1, and FIVC) and respiratory muscle strength were measured 6 months after the study, no significant differences from baseline values were found (table 3). DISCUSSION We found that 8 weeks of regular resistive IMT improves respiratory muscle strength, pulmonary function, and perceived difficulty breathing in individuals with chronic cervical SCI. Strengthening the muscles of respiration was most likely responsible for the improved maximum inspiratory pressure, which resulted in increases in both spirometric and lung volume parameters. These factors combine to help reduce the mechanical disadvantage and work of breathing in subjects with cervical SCI, with resultant decreased dyspnea. It should be noted that measures of absolute values of expiratory muscle strength (FEV1, expiratory reserve volume [ERV], MEP) did not increase significantly from baseline. The amount of work performed by a muscle is reflected in changes in the muscle itself. Several recognizable alterations occur in all muscle fiber types due to training: there is an increase in capillary density of the trained muscles, as well as in mitochondria within the cells, and the fibers synthesize more myoglobin. These changes are most dramatic, however, in the slow-twitch, fatigue-resistant fibers that depend primarily on aerobic pathways and result in more efficient muscle metabolism and in greater endurance, strength, and resistance to fatigue. Strength training of the respiratory muscles has been studied in several different populations, including patients with chronic

Table 1: Subject Characteristics Subject

Age (yrs)

Ouratrion of Injury (yrs)

6 7 8 9 10 Mean _+ SE

24 25 23 43 39 41 34 45 65 36 36 + 3.96

4 5 2 8 8 9 9 10 19 17 9 -+ 1.69

Abbreviations: Corn,complete; Inc, incomplete.

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Level of Lesion C-4, Com C-5, Corn C-6, Inc C-7, Inc C-5, Corn C-5, Inc C-6, Inc C-5, Corn C-7, Inc C-5, Inc

Smoking Status

Medications

Compliance (%)

Never Never Former (2yrs) Former (10yrs) Former (8yrs) Never Active (15py) Never Former (Syrs) Former (15yrs)

Theravac Baclofen Baclofen, diazepam None Dilantin, diazepam Oxybutyn chloride Baclofen, diazepam None None Baclofen

100 54 83 86 66 95 65 92 48 99 79 _+ 6.04

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Table 2: Mean Pulmonary Results and Percentage Change

Parameters

Baseline

(% Predicted)

FVC (L) FEVl (L) FIVC (L) TLC (L) VC (L) FRC (L) RV(L) IC (L) ERV VT (L) f (L/min) MIP (cmH20) MEP (cmH20) Borg scale

2.81 ± ,27 2.25 _+ .18 2.60 + .26 5.17 _+ ,11 2.90 ± ,26 2.52 2 .t5 2.33±.19 2.36 ± .21 .45 ± .09 .92 ÷ .11 13.6 ± 1.28 66.2 _+ 5.42 21.1 ± 6.01 1.00 ± .4

(51 ± 4.90) (54 ± 4,10) (47 + 4,76) (69 ± 2,26) (53 ± 4,69) (66 ± 2.90) (110±9.40)

Week 4 2.92 2.36 2.69 5.42 2.92 3.01 2.51 2.21 .51 .93 13.4 73.6 33.4 .88

± .21 ± .19 + .21 _+ .29 ± .21 ± .29 +.28 _+ .17 ± .08 ± .09 ± 1.04 ± 5.01 _+ 9.06 ± .39

(% Predicted) (54 _ 3.90) (56 ± 4.57) (49 ± 3.89) (72 _+ 4.01) (54 ± 4.73) (71.4 ± 5.97) (116__ 13.70)

Week 8 3.07 2.30 3.00 5.71 3.10 3.13 2.61 2.42 .52 .98 14.5 78.5 36.6 .65

% Change (Baseline to Week 8)

(% Predicted)

± .26" ± .17 _+ .28* ± .22" _+ .27* ± .16" 2.17 ± .18 ± .11 ± ~12 ± 1.10 ± 3.62* ± 6.22 ± .33

11 ± 2.82* 2 + .84 21 ± 6.91' 12 ± 3.23* 8 ± 4.36* 15 ± 5.96* 16+8.73 7 _+ 1.64' 24 ± 8.84* 6 ± ,11 6 _+ 1.15 24 ± 6.96* 51 _+ 21.92' 43 ± 21.30

(56 ± 4.63) (55 ± 3.89) (54 ±5.22) (76 ± 3.02) (56 ± 4.74) (74 ± 2.83) (124±9.56)

Data are presented as means _+ SE. Abbreviations: FVC, forced vital capacity; FEV1, forced expiratory volume in 1 second; FIVC, forced inspiratory vital capacity; TLC, total lung capacity; VC, vital capacity; FRC, functional residual capacity; RV, residual volume; IC, inspiratory capacity; ERV, expiratory reserve volume; VT, tidal volume; f, frequency; MIP, maximum inspiratory pressure; MEP, maximum expiratory pressure. * Significantly different from baseline values. *Percentage change is significantly different from 0 (p < .05).

obstructive pulmonary disease, asthma, muscular dystrophy, and in both acute and chronic tetraplegia, s4°,19-22 Interventions attempting to strengthen muscles of breathing have included abdominal weight training, incentive spirometry, positive pressure trainers, face masks, and other devices. 8-u,2°,21 The most successful findings, however, have been attained using a resistive IMT device in the SCI populations, consisting of both acute and chronic tetraplegia, in which several investigators 7I° have demonstrated significant and progressive increases in respiratory muscle strength and endurance while improving lung volumes. Gross 8 used electromyography to evaluate the effect of resistive IMT in subjects with tetraplegia, training 30 minutes daily, 6 days a week, against a resistance that produced electromyographic changes of fatigue. A significant and progressive increase in inspiratory pressure was found, in addition to enhanced respiratory muscular endurance. The authors suggested the possibility that improvements in respiratory muscular strength and endurance in these subjects after resistive training may be a result of individual muscle fibers of the 6050403020' C to 0 -10. -20 -30 -40 -50

~

diaphragm increasing their oxidative capacity and that the diaphragm muscles may change easily fatigable, slow oxidative fibers to more fatigue-resistant, fast oxidative fibers, which has been demonstrated in several animal models. 23,24 An alternative explanation for measured increases in respiratory muscle strength and endurance, using resistive IMT in individuals with restrictive ventilatory impairment postulated by other investigators, 19,25is a compensatory breathing strategy. Loveridge and colleagues 25 found no differences in maximal and sustainable inspiratory pressures after 8 weeks between a study group undergoing IMT and a group of controls, both with tetraplegia. Surprisingly, the two groups showed similar improvement. A suggested explanation was that the positive change in both groups represented an altered breathing strategy rather than training effects of respiratory muscles. Furthermore, the altered strategy to breathe against a resistive load appeared to induce an effect on the inspiratory timing mechanism, resulting in slower, deeper respiration during tidal volume breathing. Several limitations to the study are apparent and include the small sample size (n = 6) of the study group (which generated large standard deviations in the measurements reducing the statistical power and increasing the likelihood of a type II error), the failure to report compliance among the study group, and, most notably, that three of the six subjects in the study group exhibited normal percent predicted inspiratory capacity values at baseline, without chance for appreciable improvement during the IMT program. Table 3: Mean Results for Baseline Versus 6 Months After Study Parameters

MIP MEP FVC FtVC TLC VC FRC ERV FEV1 RV Borg Scale

Fig 1. Means -+ SE for percent change in pulmonary parameters from baseline to week 8. MIP, maximum inspiratory pressure; MEP, maximum expiratory pressure; FVC, forced vital capacity; FIVC, forced inspiratory vital capacity; TLC, total lung capacity; VC, vital capacity; FRC, functional residual capacity; ERV, expiratory reserve volume; FEV1, forced expiratory volume in 1 second; RV, residual volume. (*Statistically significant differences, p < .05.)

Baseline

(% Predicted)

FVC (L) 2.80 ± .28 (52 + 5.21) FEVl (L) 2.20 ± .18 (54 ± .543) FIVC (L) 2.60 _+ .26 (47 + 5.63) MIP(cmH20) 68.6 ± 8.81 MEP (cmH20) 26.2 +_ 11.4

Poststudy 2.95 2.30 2.53 72 25.4

± + ± ± ±

.29 .23 .27 5.73 4.4

(% Predicted) (56 ± 6.23) (57 ± 6.32) (46 ± 5.63)

n = 7, data presented as means _+ SE, with no significant difference between values. Abbreviations: FVC, force vital capacity; FEVl, forced expiratory volume in 1 second; FlVC, forced inspiratory vital capacity; MIP, maximum inspiratory pressure; MEP, maximum expiratory pressure.

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Of the various respiratory strength training studies performed, none have adequately addressed the impact of IMT on dyspnea, in part because of both the lack of a universally accepted definition of dyspnea and its subjectivity, which involves both perception of the sensation and reaction to the sensation, similar to pain. 26 Furthermore, degrees of dyspnea are extremely difficult to quantify among patients. To assess subjects' levels of dyspnea throughout the 8-week study, we used the modified Borg scale, 17 adapted by Burdon is to scale the intensity of breathlessness. The numerical equivalent of each descriptor was established using questionnaires concerning perceived exertion with visual analogue scales18; therefore, the scale has "ratio scaling properties" that permit comparison of responses among individuals. 17The 10-point modified scale, with its verbal descriptors to assist subjects in rating the intensity of their breathlessness, enables quantification of a subjective sensory experience. It has been shown to have good test-retest reproducibility, both in the short term 27 and with repeated testing over time. 28 Although a strong trend was observed in this study, statistically significant differences were not found between baseline and week 8 in the level of perceived difficulty breathing. This is potentially a result of the duration of the study, in which an extended training period (ie, 12 weeks) may have helped to achieve statistical differences for this measure. However, the fact that subjects reported a 43% average decrease in dyspnea (Borg scale and questionnaire) at rest and during their daily activities may be of greater importance. Recently, we reported the prevalence of breathlessness in individuals with cervical SCI to be approximately 65%, attributed essentially to the loss of inspiratory muscle function. 29 Breathlessness in this population may also reflect an overall increase in the work of breathing. 3° Because these individuals depend primarily on diaphragmatic function, abnormally large respiratory muscle energy expenditures are required to meet metabolic demands; in addition, efficiency of respiration is reduced because of paradoxical movement of the chest wall with inspiration and reduced lung and chest wall compliance. 5,3~,32 Thus, as a result of respiratory muscle dysfunction and intrapulmonary abnormalities, breathing patterns become altered: breaths are more shallow and rapid with a shorter expiratory time, predisposing individuals to ventilatory muscle fatigue. 33,34 By strengthening the muscles of breathing, it should be possible to decrease muscle fatigue and breathlessness and thereby improve the quality of life of individuals with chronic cervical SCI. In our study, we found significant improvements in respiratory muscle strength and pulmonary function that we attribute to increased strength of the diaphragm and accessory muscles of breathing, although changes in these muscles were not directly measured. In seven of the subjects retested 6 months after the study, mean pulmonary parameters returned to baseline values, suggesting that it is possible to fatigue the diaphragm and other inspiratory muscles of breathing by using high inspiratory resistive loads to induce a "training effect." Moreover, the fact that there were no measurable changes in the pattern of breathing (tidal volume and frequency) from baseline to study end further reinforces this postulate. If the respiratory improvements were the result of an altered breathing strategy, as suggested by LoveridgeY subjects' pulmonary parameters would be expected to remain elevated from their baseline values well beyond the study completion date. CONCLUSION Strengthening respiratory muscles should improve maximal ventilation and the ease of performing functions of daily living, and the experience of breathlessness should, therefore, decrease Arch Phys Med Rehabil Vol 79, March 1998

with submaximal effort. Moreover, improvement in lung volumes may decrease microatalectasis at the lung bases, mucus plugging, and accumulation of secretions, which may conceivably lessen the incidence of chronic respiratory complaints, respiratory infections, and complications in this population. It should be emphasized, nevertheless, that such a resistive training program must be regular and continuous and, thus, incorporated into a lifestyle change. Only when such respiratory muscle training is chronically sustained will it induce changes that may help protect against both the development of respiratory muscle fatigue and acute pulmonary infections. Acknowledgment: The authors thank Chris Wade, MSPT, for assisting with the initial study design and for the many insightful suggestions throughout the project. References 1. Buchanan L. An overview. In: Buchanan L, Nawoczenski D, editors. Spinal cord injury: concepts and approaches. Baltimore (MD): Williams and Wilkins; 1987. p. 1-19. 2. DeVivo MJ, Black KJ, Stover SL. Causes of death during the first twelve years after spinal cord injury. Arch Phys Med Rehabil 1993;74:248-54. 3. Jackson AB, Groomes TE. Incidence of respiratory complications following spinal cord injury [abstract]. J Am Paraplegia Soc 1991;14:97. 4. Mansel JK, Norman JR. Respiratory complications and management of spinal cord injuries. Chest 1990;122:591-600. 5. Scanlon PD, Loring SH, Pichurko BM, McCool FD, Slutsky AS, Sarkarati M, et al. Respiratory mechanics in acute tetraplegia: lung and chest wall compliance and dimensional changes during respiratory maneuvers. Am Rev Respir Dis 1989;139:615-20. 6. Fomer JV. Lung volumes and mechanics of breathing in tetraplegics. Paraplegia 1980;18:258-66. 7. Fugl-Meyer AR. A model of treatment of impaired ventilatory function in tetraplegic patients. Scand J Rehabil Med 1971;3:16777. 8. Gross D, Ladd HW, Riley EJ, Macklem PT, Grossino A. The effect of training on strength and endurance of the diaphragm in tetraplegia. Am J Med 1980;68:27-35. 9. Huldtgren AC, Fugl-Myer AR, Jonasson E, Bake B. Ventilatory dysfunction and resph'atory rehabilitation in post-traumatic tetraplegia. Enr J Respir Dis 1980;61:347-56. 10. Derrickson J, Ciesla N, Simpson N, Imte PC. A comparison of two breathing exercise programs for patients with tetraplegia. Phys Ther 1992;72:763-9. 11. Lerman RM, Weiss MS. Progressive resistive exercise in weaning high quadriplegics from the ventilator. Paraplegia 1987;90:130-5. 12. Aldrich TK, Karpel JP, Uhrlass RM, Sparapani MA, Eramo D, Ferranti R. Weaning from mechanical ventilation: adjunctive use of inspiratory muscle resistive training. Crit Care Med 1989;17: 143-7. 13. American Thoracic Society. Standardization of spirometry: 1994 update. Am Rev Respir Dis 1995;152:1107-36. 14. Morris JF, Koski A, Johnson LC. Spirometric standards for healthy nonsmoking adults. Am Rev Respir Dis 1971;103:57-67. 15. Tierney DF, Nadel JA. Concurrent measurements of functional residual capacity by three methods. J Appl Physiol 1962;17:871-3. 16. Ferris BG Jr. Epidemiology standardization project. Am Rev Respir Dis 1978;liB(Part 2):55-88. 17. Borg G. Subjective effort and physical activities. Scand J Rehabil Med 1978;6:108-13. 18. Burdon JGW, Juniper EF, Killian KJ, Hargreave FE, Campbell EJM. The perception of breathlessness in asthma. Am Rev Respir Dis 1982;126:825-8. 19. Belman MJ, Thomas SG, Lewis MI. Resistive breathing training in patients with chronic obstructive pulmonary disease. Chest 1986; 90:662-9. 20. Guyatt G, Keller J, Singer J, Halcrow S, Newhouse M. Controlled trial of respiratory muscle training in chronic airflow limitation. Thorax 1992;47:598-602.

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