Respiratory muscle training improves cardiopulmonary function and exercise tolerance in subjects with subacute stroke: a randomized controlled trial

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1 Clinical Rehabilitation 2010; 24: Respiratory muscle training improves cardiopulmonary function and exercise tolerance in subjects with subacute stroke: a randomized controlled trial Serap Tomruk Sutbeyaz, Fusun Koseoglu Fourth Physical Medicine & Rehabilitation Clinic, Ankara Physical Medicine and Rehabilitation Education and Research Hospital, Levent Inan and Ozlem Coskun Department of Neurology, Ministry of Health Ankara Education and Research Hospital, Ankara, Turkey Received 11th April 2008; returned for revisions 21st June 2008; revised manuscript accepted 24th October Objective: To determine whether two types of exercise breathing retraining (BRT) and inspiratory muscle training (IMT) improve on cardiopulmonary functions and exercise tolerance in patients with stroke. Design: A randomized controlled trial. Setting: Education and research hospital. Subjects: Forty-five inpatients with stroke (24 men, 21 women) were recruited for the study. The subjects were randomized into three groups: 15 assigned to receive inspiratory muscle training (IMT); 15 assigned to received breathing retraining, diaphragmatic breathing and pursed-lips breathing (BRT); 15 assigned to a control group. Interventions: All study groups participated in a conventional stroke rehabilitation programme. For the same period, the IMT and BRT groups trained daily, six times a week, with each session consisting of one half-hour of training for six weeks. Main measures: Each subject underwent pulmonary function and cardiopulmonary exercise tests. Subjects were also assessed for exertional dyspnoea, stages of motor recovery, ambulation status, activity of daily living and quality of life. Results: After the training programme, the IMT group had significantly improved forced expiratory volume at 1 second (FEV 1 ), forced vital capacity (FVC), vital capacity (VC), forced expiratory flow rate 25 75% (FEF 25 75%) and maximum voluntary ventilation (MVV) values compared with the BRT and control groups, although there were no significant differences between the BRT and control groups (P50.01). Peak expiratory flow rate (PEF) value was increased significantly in the BTR group compared with the IMT and control groups. The IMT group also had significantly higher peak oxygen consumption (Vo 2peak ) than the BRT and control groups, although there were no significant differences between the BRT and control groups (P50.001). There was a statistically significant increase in maximum inspiratory pressure (PI max ) and maximum inspiratory and expiratory pressure (PE max ) in the BRT group and, PI max in the IMT group compared with baseline and the control group. In the IMT group, this was associated with improvements in exercise capacity, sensation of dyspnoea and quality of life. Conclusions: Significant short-term effects of the respiratory muscle training programme on respiratory muscle function, exercise capacity and quality of life were recorded in this study. Address for correspondence: Serap Tomruk Sutbeyaz, Karakusunlar M 339. sok No: 12/9, Ankara 06530, Turkey. serapts@yahoo.com ß The Author(s), Reprints and permissions: /

2 Respiratory muscle training in stroke 241 Introduction It has been reported 1 that little attention is generally paid to the pulmonary system during the examination of patients with stroke, probably because these patients are free from pulmonary symptoms or disease. However, in patients with stroke, partial or total weakness of the diaphragm, intercostal and abdominal muscles has been reported on the affected side. 1 4 A larger hemidiaphragmatic excursion on the unaffected side was observed in these patients. 5,6 For example, Lanini et al. 4 using optoelectronic plethysmography reported a reduction of respiratory movement of the affected hemithorax during voluntary hyperventilation when compared with spontaneous breathing of eight patients with stroke. In another report, Teixeira-Salmela et al. 7 showed significant decrease in maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) in community-dwelling chronic stroke survivors compared with healthy age-matched subjects. They also found that the stroke subjects had a significant lower tendency for the predominance of ribcage contributions during tidal breathing. Indeed, respiratory dysfunction as a result of reduced vital capacity, inspiratory capacity, total lung capacity, maximum inspiratory capacity and especially expiratory reserve volume has been reported 3 after stroke. In addition, low respiratory muscle strength is an independent risk factor for cardiovascular disease, and has been suggested to lead to an increased risk for stroke. 6 Decrease in the strength of respiratory muscles and lower abdomen contributions were also shown during the respiratory cycle in stroke subjects. 7 Inspiratory muscle training has been shown to improve inspiratory muscle function resulting in additional improvement of exercise capacity, decreased dyspnoea and nocturnal desaturation time in patients with inspiratory muscle weakness. 8 Stroke survivors often have poor exercise capacities, which have been found to be approximately 40% below those of age- and sex-adjusted norms for sedentary individuals. Cardiovascular training has been shown to improve cardiovascular fitness after stroke. However, no studies have associated respiratory muscular training with cardiovascular training. Based on these findings, the observed reduction in respiratory muscular strength could lead to the hypothesis that specific respiratory training could optimize the gains associated with cardiovascular training with stroke survivors. 7,9 The aim of the study, therefore, was to determine whether two types of exercise (breathing retraining (BRT) and inspiratory muscle training (IMT)) improve cardiopulmonary function and exercise tolerance in patients with stroke. Material and methods Subjects Fifty-eight patients with stroke (32 male, 26 female) were recruited from the inpatient rehabilitation department of the Ankara Physical Medicine and Rehabilitation Education and Research Hospital and were screened (Figure 1). Before participating in the study, subjects underwent a complete medical assessment including medical history, physical and neurological examination, posteroanterior teleradiograph, a resting 12-lead electrocardiogram (ECG) and routine laboratory measurements. The criteria for recruitment of subjects for the study were: (1) first episode of unilateral stroke with hemiparesis during the previous 12 months, (2) sufficient unilateral upper torso and extremity nerve function and strength to accomplish arm crank ergometry (ACE), (3) ability to understand and follow simple verbal instructions, (4) no previous history of cardiovascular or respiratory problems, (5) no medication that would influence metabolic or cardiorespiratory responses to exercise, and (6) no previous history of regular exercise training and sports activity to strengthen upper extremity and ventilatory muscles. The exclusion criteria included chronic pulmonary and/or cardiac disease, clinical signs of cardiac and/or respiratory disease, impaired level of consciousness and evidence of gross cognitive impairment. The hospital s ethical committee approved the study, and all patients gave informed consent. Study design All subjects underwent a standardized interview regarding their current medications, physical

3 242 ST Sutbeyaz et al. Total number of patients that could have been recruited (n=58) Exclusion (n=13) due to 5 severe cognitive deficits, 3 second attack stroke, 5 insufficient upper limb strength Randomized (n=45) BRT group (n=15) Received breathing retraining and conventional stroke rehabilitation programme IMT group (n=15) Received inspiratory muscle training and conventional stroke rehabilitation programme Control group (n=15) Conventional stroke rehabilitation programme Completed trial (n=15) Completed trial (n=15) Completed trial (n=15) Figure 1 Progress of participants through the trial. activity level and smoking habits. Body weight was measured with subjects wearing light clothing. Because some subjects were unable to stand, arm span was used to obtain height. Body mass index was calculated as the ratio of body weight and height squared (kg/m 2 ). We used a randomized controlled design in which the assessor was blind to the group allocation of the subject. Blinding the patients was not possible because of the nature of the treatment. An independent physician who did not otherwise participate in the study took charge of the randomization process. After informed consent and baseline data collection, stratified, variable block randomization was used to assign eligible participants to one of the three groups. The factor used for stratification was gender. The patients were randomized using a computer-generated random number list by an independent investigator and allocated to BRT, IMT or control groups. Randomization was performed using sequential sealed envelopes prepared by the independent physician before enrollment of the subject. The sealed envelopes were then opened for each patient was included in the study a record of the allocation. Physicians remained blind to the group allocation throughout the study. Training programme Training was performed in the cardiorespiratory rehabilitation unit of the hospital. Each session in the exercise training group consisted of 15 minutes of diaphragmatic breathing combined with pursed-lips breathing, followed by 5 minutes of air-shifting techniques and 10 minutes of voluntary isocapnoeic hyperpnoea. The patients had a 5-minute interval before each type of exercise. The training was performed daily over six weeks. In the second group, IMT training was performed using a threshold inspiratory muscle trainer (Threshold IMT, ref HS730EU, NJ, USA). The subjects started breathing at a load of 40% of the maximum inspiratory pressure (PI max ). 8 Exercise intensity was gradually increased, 5 10% each session, to 60% of PI max as tolerated. All patients trained daily for two sessions of 15 minutes each, six times a week for six weeks. Both the training groups and the control group participated in a conventional stroke rehabilitation programme, five days a week for six weeks. Outcome measures Outcome measures were repeated at baseline (pre-treatment) and at the end of the training

4 Respiratory muscle training in stroke 243 programme after six weeks (post-treatment). A same physiatrist, blinded to the type of training programme, evaluated changes with training programme. Stages of motor recovery: Brunnstrom stages are six sequential stages of motor recovery through which the hemiplegic upper and lower extremities progress used as a method for assessing recovery. 10 Ambulation status: Functional Ambulation Categories (FAC) is a reliable and valid assessment with six categories designed to provide information on the level of physical support needed by patients to ambulate safely both indoors and outdoors. 11 Activities of daily living: The Barthel Index 12 has 10 items, including feeding, transfers, personal grooming and hygiene, bathing, toileting, walking, negotiating stairs, and controlling bowel and bladder. A patient with a maximum score of 100 points is defined as continent, able to eat and dress independently, walk at least a block, and climb and descend stairs. Pulmonary function: Resting spirometric measurements including forced vital capacity (FVC), vital capacity (VC), forced expiratory volume at 1 second (FEV 1 ), the ratio of FEV 1 to FVC (FEV 1 /FVC), forced expiratory flow rate 25 75% (FEF 25 75%), peak expiratory flow rate (PEF) and maximum voluntary ventilation (MVV) were performed on a hand-held spirometer (Sensormedix, Vmax29, Yorba Linda, CA, USA). All studies were performed in a sitting position. Each subject performed at least three trials and the best performance was used for analysis. Measurements were expressed as percentages of the predicted values. Eighty per cent of predicted maximum or greater was accepted as normal. The maximum inspiratory and expiratory pressures (PI max,pe max ) were obtained using a digital mouth pressuremeter (MPM, Sensormedix, Yorba Linda, CA, USA). PI max was measured following exhalation to residual volume (RV), and PE max following inspiration to total lung capacity. Each measure was repeated three times. The subject s best sustained effort for 1 second was used for data analysis. Values greater than cmh 2 O for PI max and cmh 2 O for PE max were taken as normal. Cardiopulmonary exercise test: This was performed on an electronically braked arm crank ergometer (Sensormedix, Ergoline, Yorba Linda, CA, USA). A computerized gas analysis system collected and analysed expired gases during exercise (Sensormedix Vmax29, Yorba Linda, CA, USA). A standard open-circuit method was used to collect expired gases. It was calibrated with known gas concentrations and volumes prior to each test. Heart rate and ECG were displayed throughout the cardiopulmonary exercise test. Capillary oxygen tension was measured by an oxygen photometer attached to the earlobe. An incremental exercise test was used to determine maximum exercise performance. After stabilization and a 3-minute warm-up period at 25 W, the load was increased every 3 minutes until exhaustion. The subjects were instructed to maintain a crank rate of 50 rpm and verbally encouraged to continue exercise as long as possible. Oxygen consumption (Vo 2 ), carbon dioxide exhaled (Vco 2 ), minute ventilation (V E ), respiratory rate (RR), respiratory exchange ratio (RER), the ratio of physiologic dead space to tidal volume (V D /V T ), oxygen saturation (Sao 2 ), and power output (PO) were recorded every 20 seconds during the cardiopulmonary exercise test. Anaerobic threshold was determined by computerized V-slope method of the gas exchange data. Exertional dyspnoea: Subjects were asked to rate their perceived exertion by using the 16-point Borg rating of perceived effort. 13 Health-related quality of life: The Medical Outcomes Study Short Form 36 (SF-36) questionnaire (Turkish version) was used to measure quality of life. The validity and reliability study of the Turkish version of SF-36 has been well documented. 14 Data analysis Sample size The required sample size was determined by using the pooled estimate of within-group standard deviations obtained from pilot data. Power calculations indicated that a sample of 36 subjects would provide an 80% (b ¼ 0.20) chance of

5 244 ST Sutbeyaz et al. Table 1 Baseline characteristics of the study participants (n ¼ 45) a BRT group IMT group Control group P-value Number of patients Age (years) 60.8 (6.8) 62.8 (7.2) 61.9 (6.15) 0.72 Female/male 7/8 7/8 7/8 1.0 BMI (kg/m 2 ) 27.2 (1.9) 26.4 (2.6) 26.1 (2.3) 0.88 Time since stroke (days) 156 (49.7) (46.9) (36.5) 0.91 Paretic side (right/left) 12/3 11/4 10/ Lesion type (ischaemic/haemorrhagic) 10/5 12/3 11/ Hypertension (%) 46.7% 40% 40% Diabetes (%) 26.7% 20% 13.3% Tobacco abuse (%) 35.5% 28% 15% Brunnstrom stages (upper extremity) 4.2 (0.5) 4.6 (0.5) 4.4 (0.3) 0.69 Brunnstrom stages (lower extremity) 4.4 (0.5) 4.7 (0.4) 4.7 (0.5) 0.22 Barthel Index 75.3 (4.4) 76.3 (3.9) 76.0 (3.8) 0.83 FAC 4.2 (0.5) 4.1 (0.4) 4.3 (0.5) 0.48 MIP, cmh 2 O 50.2 (6.7) 49.4 (5.9) 51.0 (6.3) 0.80 MEP, cmh 2 O 60.8 (7.1) 60.7 (9.2) 62.9 (6.5) 0.67 MVV, L/min 57.9 (4.4) 60.2 (3.7) 58.2 (4.3) 0.25 FEV 1, L 2.5 (0.1) 2.4 (0.2) 2.6 (0.1) 0.70 FVC, L 3.1 (0.3) 3.2 (0.4) 3.1 (0.4) 0.68 PEF, L/s 4.11 (0.39) 4.12 (0.28) 4.11 (0.34) 0.99 Vo 2max, ml/kg/min 12.4 (0.9) 13.2 (1.3) 12.4 (0.7) 0.08 V E, L/min 39.8 (2.8) 39.6 (2.5) 39.5 (2.9) 0.92 HR (4.8) (6.4) (3.9) 0.92 PO 49.6 (5.3) 48.6 (6.1) 50.2 (4.9) 0.74 a Values expressed as mean SD or no. (%). BMI, body mass index; FAC, Functional Ambulation Categories; MIP, maximum inspiratory pressure; MEP, maximum expiratory pressure; MVV, maximum voluntary ventilation; FEV 1, forced expiratory volume in 1 second; FVC, forced vital capacity; PEF, peak expiratory flow rate; Vo 2peak, peak oxygen consumption; HR, heart rate; V E, minute ventilation; RER, respiratory exchange ratio; PO, power output. detecting a 20% (a ¼ 0.05) difference in improvement between the groups. All statistical analyses were performed using SPSS version 10.0 statistical software (SPSS Inc., Chicago, IL, USA). Results were presented as mean standard deviation (SD) and/or median range or as counts with proportions as appropriate. Prior to all analyses, the normality of the data was assessed by one-sample Kolmogorov Smirnov test, accepting an a level of P Chi-square analysis was calculated to examine differences in frequencies for categorical variables. Comparisons of the changes between groups were performed using a one-way ANOVA with significant differences being further investigated using unpaired t-tests with adjustment for multiple comparisons (Bonferroni). Baseline and posttraining data were compared within groups using a paired t-test. For all tests, statistical significance was set at 0.05 (two-tailed). Results The clinical and demographic features of the patients are shown in Table 1. The average Barthel Index score was estimated to be , and in the groups, respectively. There were no differences between the groups as regards age, height, weight, body mass index, duration of the disease, Functional Ambulation Categories and Barthel scores, spirometric, cardiopulmonary and metabolic values at the beginning of the study. Pulmonary function Table 2 shows the mean resting spirometric values in stroke subjects at baseline and at the end of the six weeks. In comparison with the predicted normal values, we observed a decrease in baseline values of the

6 Respiratory muscle training in stroke 245 Table 2 Pre- and post-training lung volumes a Variables n Pre-training Post-training Change score P-value FEV 1,L BRT group (0.2) 2.48 (0.1) 0.0 (0.1) 0.96 IMT group (0.2) 2.71 (0.1) 0.22 (0.1) 0.01 y Control group (0.1) 2.54 (0.2) 0.0 (0.1) 0.77 FVC, L BRT group (0.3) 3.11 (0.3) 0.01 (0.1) 0.41 IMT group (0.4) 3.45 (0.3) 0.23 (0.1) 0.01 y Control group (0.3) 3.17 (0.3) 0.0 (0.1) 0.43 VC, L BRT group (0.3) 2.95 (0.4) 0.0 (0.1) 0.94 IMT group (0.3) 3.23 (0.3) 0.13 (0.1) 0.01 y Control group (0.4) 2.95 (0.4) 0.0 (0.1) 0.59 FEF 25 75% BRT group (0.2) 2.38 (0.2) 0.0 (0.1) 0.28 IMT group (0.2) 2.45 (0.2) 0.14 (0.1) 0.01 y Control group (0.2) 2.40 (0.2) 0.0 (0.1) 0.76 PEF (L/s) BRT group (0.4) 4.68 (0.1) 0.1 (0.8) 0.01 y IMT group (0.2) 4.22 (0.3) 0.17 (0.2) 0.06 Control group (0.3) 4.18 (0.3) 0.1 (0.1) 0.09 MVV BRT group (4.9) (3.7) 0.8 (2.4) 0.23 IMT group (3.7) (4.8) 5.6 (3.9) y Control group (4.0) (4.1) 1.0 (1.3) 0.02 MIP BRT group (6.7) (7.9) 7.07 (4.8) IMT group (5.9) (8.6) 7.87 (6.6) y Control group (6.3) 53.9 (6.3) 2.9 (1.9) MEP BRT group (7.1) 66.2 (8.2) 5.40 (2.9) y IMT group (9.2) 62.8 (9.9) 2.07 (2.0) Control group (6.4) 65.9 (5.7) 3.0 (1.6) a Values expressed as mean standard deviation. FEV 1, forced expiratory volume in 1 second; FVC, forced vital capacity; VC, vital capacity; FEF 25 75%, forced expiratory flow rate 25 75%; PEF, peak expiratory flow rate; MVV, maximum voluntary ventilation; MIP, maximum inspiratory pressure; MEP, maximum expiratory pressure. y The IMT group had significantly improved FEV 1, FVC, VC, FEF 25 75% and MVV values than the BRT and control groups, although there were no significant differences between the BRT and control groups (P50.01). PEF values were increased significantly in the BTR group compared with the IMT and control groups. following measures: FEV 1 and FVC in 35 patients; VC in 33 patients; PEF in 25 patients; FEF 25 75% in 33 patients. No significant difference was determined as regards FVC, VC, FEV 1, FEF 25 75% and MVV in the BRT group at the end of the training compared with baseline and the control group. Only PEF values were improved by the BRT intervention. Following training, Statistically significant improvement was observed in the IMT group regarding FVC, VC, FEV 1 and MVV values compared with baseline and FVC, VC, FEV 1, FEF 25 75% and MVV values compared with the control group. Inspiratory muscle strength In comparison with the normal values, we observed a substantial decrease in baseline PI max and PE max measures in all groups. After six weeks of training, there was a statistically significant increase in PI max and PE max in the BRT group and PI max in the IMT group compared

7 246 ST Sutbeyaz et al. Table 3 Pre- and post-training cardiopulmonary and metabolic values a Variables N Pre-training Post-training Change score P-value Vo 2 peak, ml/kg/min BRT group (0.91) (0.83) 0.1 (0.1) 0.01 IMT group (1.31) 13.7 (1.37) 0.56 (0.2) 0.01 y Control group (0.86) 12.5 (0.76) 0.04 (0.2) 0.01 HR peak, bpm BRT group (4.84) (3.96) 0.5 (3.5) 0.01 IMT group (6.42) (5.16) 3.2 (3.4) 0.01 Control group (4.84) (3.96) 0.5 (3.5) 0.01 V Epeak, L/min BRT group (2.82) (2.78) 2.3 (1.2) 0.01 IMT group (2.82) (2.78) 2.3 (1.2) 0.01 Control group (2.96) (3.58) 1.2 (1.7) 0.01 PO BRT group (5.32) 51.4 (5.87) 1.8 (1.7) 0.01 IMT group (6.11) (5.62) 9.0 (2.1) 0.01 y Control group (4.92) 53 (4.02) 2.8 (2.9) 0.01 Sao 2,% BRT group (1.35) 92.0 (1.31) 0.1 (0.3) 0.99 IMT group (1.99) 93.4 (1.76) 0.5 (1.0) 0.01 Control group (1.01) 91.7 (1.13) 0.1 (0.4) 0.06 V D /V Tpeak BRT group (0.0) 0.39 (0.0) 0.01 (0.1) IMT group (0.06) 0.39 (0.07) 0.01 (0.1) Control group (0.0) 0.41 (0.0) 0.01 (0.1) RPE BRT group (0.88) (1.03) 0.1 (0.9) 0.07 IMT group (1.0) (1.03) 1.67 (0.6) 0.01 y Control group (1.22) (1.28) 0.0 (1.1) 0.02 a The values were expressed as mean standard deviation. Vo 2peak, peak oxygen consumption; HR, heart rate; V E, minute ventilation; PO, power output; Sao 2, oxygen saturation; V D /V T, ratio of physiologic space to tidal volume; RPE, rating perceived exertion. y The IMT group had significantly improved Vo 2peak, HR, PO, V E values than the BRT and control groups, although there were no significant differences between the BRT and control groups (P50.001). with baseline and the control group. Between the training groups, inspiratory muscle strength was increased most in the IMT group. Exertional dyspnoea Following training, there was a statistically significant decrease in exertional dyspnoea in the IMT group but not in the BRT group compared with baseline and the control group. Cardiopulmonary and metabolic function When compared with the baseline values and the control group, statistically significant improvement was observed in the values of Vo 2, PO, HR and V E in the IMT group but not in the BRT group at the end of the training (Table 3). Functional status Barthel Index and Functional Ambulation Categories scores increased significantly in the IMT group at the end of the training compared with baseline and the control group. Following training, only Barthel Index score improved significantly in the BRT group compared with the baseline. When compared with the control group, an increase was observed in Barthel Index and Functional Ambulation Categories scores after the BRT programme, but the results were not significant statistically.

8 Respiratory muscle training in stroke 247 Health-related quality of life Physical role, general health, and vitality domains of the SF-36 improved significantly in the IMT group and emotional role, general health, pain, vitality domains in the BRT group after the training programme compared with baseline and the control group. Discussion This study demonstrated that a six-week programme of IMT improves inspiratory muscle function in stroke patients. This was associated with an increase in lung volumes and improvements in exercise capacity, sensation of dyspnoea score and SF-36 domains. It is commonly accepted that the motor cortical representation of the diaphragm and intercostal muscles is bilateral, and thus that these muscles are little influenced by unilateral corticospinal lesions. However, a decrease in lung volumes and respiratory strength has been established in stroke subjects. 1 4,7 Furthermore, the efficiency of the unaffected muscles may be decreased as a result of instability of the chest wall and an inactive lifestyle. Similowski et al. 2 and Khedr et al. 5 found that stroke patients had abnormal magnetic evoked potentials, cortical latency and central conduction time of the affected hemisphere, and no bilateral motor representation of each hemidiaphragm in stroke patients. Khedr et al. also demonstrated a significant association between the degree of respiratory dysfunction and abnormal magnetic evoked potentials and central conduction time of the affected hemisphere. To our knowledge, this is the first randomized controlled trial of respiratory muscle training in stroke survivors. The methods of inspiratory muscle training are voluntary isocapnoeic hyperpnoea, inspiratory resistive loading and inspiratory threshold loading (IMT). IMT has been extensively investigated in patients with chronic obstructive pulmonary disease. Results indicated that IMT was associated with significant improvements in some outcomes of inspiratory muscle strength and endurance, exercise capacity, power output and dyspnoea. 9,15 Moreover, the benefits of IMT has also been documented in Parkinson s disease, cystic fibrosis, myasthenia gravis and bronchiectasis The joint American College of Chest Physicians/American Association of Cardiovascular and Pulmonary Rehabilitation Committee has recommended IMT as a part of pulmonary rehabilitation. 15 Our IMT programme results are consistent with previous studies in other disorders. MVV is often used as an index of inspiratory muscle endurance that approximates the maximal ventilatory reserve during exercise (V Emax ). The reduction in V Emax produces a ventilatory limitation to maximal oxygen transport (Vo 2 ) and exercise tolerance. 20 In our study, IMT programme has been shown to improve MVV, therefore, V Emax and Vo 2max. The measurement of peak oxygen uptake (Vo 2max ) is considered to be the best measure of cardiorespiratory fitness and exercise capacity. Peak power output (PO) is a second important indicator of exercise capacity. 21 Peak Vo 2 in individuals with stroke has been found to be low Peak Vo 2 in individuals with stroke has been measured as low as 50 70% of the age- and sex-matched value in sedentary individuals. The low peak Vo 2 values found in patients with stroke suggest that many stroke survivors do not meet the minimum fitness level required for independent living. Low aerobic fitness has also been related to an increased risk of various forms of cardiovascular disease in these individuals. 22 Poor cardiorespiratory fitness has also been linked to a higher risk of stroke and stroke mortality. 21,24 The present study showed that Vo 2 and PO are increased by IMT training in a stroke population. These findings imply that risk of stroke, stroke mortality and risk of various forms of cardiovascular disease in these populations might be reduced by respiratory muscle training. Our results suggest that respiratory muscle function, cardiorespiratory fitness, exercise capacity and functional status are improved by an IMT programme in patients with stroke. In addition, these improvements were translated by the patients into a better quality of life. It has been found that lower levels of forced expiratory volume in 1 second are associated with an increased risk of stroke in those already at high risk. 25 In addition, recurrent stroke rate has been found around 25% following first stroke. 26

9 248 ST Sutbeyaz et al. The present study shows that FEV 1 was improved by the IMT programme in stroke patients. This result also suggests that the IMT programme may help to decrease stroke recurrence. Pursed-lips breathing, air-shifting and diaphragmatic breathing are breathing retraining techniques. The goals of breathing retraining are to restore the diaphragm to a more normal position and function, to decrease the respiratory rate, to diminish the work of breathing, to reduce dyspnoea, to improve chest wall motion, ventilation distribution and expiration by preventing airway compression and airway collapse and to increase exercise performance. 9,27 Voluntary isocapneoic hyperpnoea is one of the methods of inspiratory muscle training. It provides low tension and a high level of repetitive activity for the diaphragm and other inspiratory muscles, and has also been shown to improve the strength and endurance of respiratory muscles. 28 Expiratory muscle weakness causes ineffective cough, retantion of secretions and inability to maintain a clear airway. These may lead to pneumonia and microatelectasis. Pneumonia has been estimated to occur in about one-third of stroke patients and is a major cause of morbidity and mortality. 29 In our study, a BRT programme has been shown to improve inspiratory and expiratory muscle strength in our stroke patients. PEF value also increased significantly after the training. Since PEF is effort-dependent, improved PEF values after training may reflect an increase in muscle strength and support the presence of effective cough in our patients. Furthermore, improved expiratory muscle strength may decrease the risk of respiratory infections. A slight increase was observed in exercise performance and functional status after the BRT programme, but the results were not significant statistically. Although the improvement in respiratory muscle function was not associated with the increase in the exercise performance and functional status, it has been found that an improvement in respiratory muscle function leads to increased health-related quality of life. We also think BRT is an easy way to train respiratory muscles, since this type of exercise does not require equipment. The main limitation of our study is that the long-term effects of respiratory muscle training in our patients were not monitored. There is consensus that exercise programmes shorter than 6 8 weeks are less effective. 9,27 Our patients were trained for six weeks, which was considered to be an effective time. We also advised our patients to perform their exercises regularly at home, although it has been shown in a previous study that compliance with maintenance home exercise therapy is relatively low. 27 Therefore, we suggest the long-term effect of increasing respiratory muscle strength in stroke populations should be determined. Another limitation of our study is the relatively small number of cases and patients were in quite late phase after stroke. Respiratory muscle function, especially inspiratory muscle function, has been shown to contribute to dyspnoea, exercise limitation, deconditioning, hypercapnia and reduced health-related quality of life in patients with chronic obstructive pulmonary disease. 9 These important observations suggested that respiratory muscle training might be able to improve exercise performance, symptoms and quality of life in patients with chronic obstructive pulmonary disease. In fact, results showed that respiratory muscle training was associated with significant improvements in respiratory muscle strength and endurance, exercise capacity, power output and dyspnoea. 9,15 Consistent with previous studies in chronic obstructive pulmonary disease, we observed that respiratory muscle function plays an important role in exercise capacity, in most of the cardiopulmonary responses to exercise, functional status, sensation of dyspnoea and quality of life in stroke subjects. Despite the presence of typical abnormalities in respiratory muscle function, our patients did not report respiratory symptoms before and during the study. Neurological deficits promoting a sedentary lifestyle in these patients usually masks ventilatory impairment until increased demand appears, such as during chest infection or strenuous activity. In addition, the presence of problems such as mobility limitations, sensory-perceptual dysfunctions and communication deficits discourage the systematic application of cardiopulmonary exercise testing to determine respiratory function in stroke population. In spite of their neurological deficits and trunk stability problems, the arm

10 Respiratory muscle training in stroke 249 crank ergometer test was well tolerated in our patients. We suggest that the arm crank ergometer can be used to evaluate cardiopulmonary function and proper exercise prescription in this population. As respiratory muscle function plays a strong role in exercise capacity and in most of the cardiopulmonary responses to exercise, systematic measurement of respiratory muscle function should be considered in stroke populations. Once respiratory muscle impairment and respiratory dysfunction is determined, respiratory muscle training should be carried out. Significant short-term effects of the respiratory muscle training programme on respiratory muscle function, exercise capacity, quality of life, sensation of dyspnoea and functional status were recorded in this study. These differences support the need for respiratory muscle training in stroke patients who have respiratory dysfunction. However, as a rule, respiratory muscle training is not a component of traditional stroke rehabilitation programmes, unless patients have evident pulmonary disease. 29 Previous studies have also reported that reduced exercise capacity is related to an increased risk of various forms of cardiovascular disease, 22 a higher risk of stroke and stroke mortality in these population. 21,24 Therefore, our findings imply that risk of stroke and various forms of cardiovascular disease and stroke mortality might be reduced by respiratory muscle training. The inspiratory muscle trainer used in this study, Threshold IMT, is an inexpensive plastic device that is durable, simple to start, and could easily be incorporated into daily rehabilitation sessions in the clinic and then carried over in the home with minimal training. Further research with larger samples is necessary to determine the long-term effect of increasing respiratory muscle strength on clinical outcomes in those populations. Clinical messages Specific inspiratory muscle training in people late after stroke seems to improve respiratory function. General breathing exercises seem to have less effect. References 1 Annoni JM, Ackermann D, Kesselring J. Respiratory function in chronic hemiplegia. Int Disabil Stud 1990; 12: Similowski T, Catala M, Rancurel G, Derenne JP. Impairment of central motor conduction to the diaphragm in stroke. Am J Respir Crit Care Med 1996; 154: Roth EJ, Noll SF. Stroke rehabilitation. 2. Comorbidities and complications. Arch Phys Med Rehabil 1994; 75: S42 S46. 4 Lanini B, Bianchi B, Romagnoli I. Chest wall kinematics in patients with hemiplegia. Am J Respir Crit Care Med 2003; 168: Khedr EM, El Shinawy O, Khedr T, Abdel aziz ali Y, Awad EM. Assessment of corticodiaphragmatic pathway and pulmonary function in acute ischemic stroke patients. Eur J Neurol 2000; 7: van der Palen J, Rea TD, Manolio TA et al. Respiratory muscle strength and the risk of incident cardiovascular events. Thorax 2004; 59: Teixeira-Salmela LF, Parreira VF, Britto RR et al. Respiratory pressures and thoracoabdominal motion in community-dwelling chronic stroke survivors. Arch Phys Med Rehabil 2005; 86: Gosselink R, Houtmeyers E. Physiotherapy. Eur Respir Monogr 2000; 13: Sezer N, Ordu NK, Sutbeyaz ST, Koseoglu BF. Cardiopulmonary and metabolic responses to maximum exercise and aerobic capacity in hemiplegic patients. Func Neurol 2004; 19: Sawner K, Lavigne J. Brunnstrom s movement therapy in hemiplegia: a neurophysiological approach. Philadelphia: JB Lippincott, Collen FM, Wade DT, Bradshaw CM. Mobility after stroke: reliability of measures of impairment and disability. Int Disabil Stud 1990; 12: Mahoney F, Barthel D. Functional evaluation: the Barthel index. Md Med J 1965; 14: Borg GAV. Psychophysical bases of perceived exertion. Med Sci Sports Exerc 1982; 14: Dundar P, Fidaner C, Fidaner H. Comparing the Turkish versions of WHOQOL-BREF and SF-36, convergent validity of WHOQOL-BREF and SF-36. Hippokratia 2002; 6: Geddes EL, Reid WD, Crowe J, O Brien K, Brooks D. Inspiratory muscle training in adults with chronic obstructive pulmonary disease: a systematic review. Respir Med 2005; 99:

11 250 ST Sutbeyaz et al. 16 Inzelberg R, Peleg N, Nisipeanu P, Magadle R, Ralph LC, Weiner P. Inspiratory muscle training and the perception of dyspnea in Parkinson s disease. Can J Neurol Sci 2005; 32: Enright S, Chatham K, Ionescu AA, Unnithan VB, Shale DJ. Inspiratory muscle training improves lung function and exercise capacity in adults with cystic fibrosis. Chest 2004; 126: Fregonezi GA, Resqueti VR, Guell R, Pradas J, Casan P. Effects of 8-week, interval-based inspiratory muscle training and breathingretraining in patients with generalized myasthenia gravis. Chest 2005; 128: Newall C, Stockley RA, Hill SL. Exercise training and inspiratory muscle training in patients with bronchiectasis. Thorax 2005; 60: Ries AL. The importance of exercise in pulmonary rehabilitation. Clin Chest Med 1994; 15: Arsura E. Evaluating cardiorespiratory fitness after stroke: does the best provide less? Chest 2005; 127: Pang MY, Eng JJ, Dawson AS, Gylfadottir S. The use of aerobic exercise training in improving aerobic capacity in individuals with stroke: a meta-analysis. Clin Rehabil 2006; 20: Courbon A, Calmels P, Roche F, Ramas J, Rimaud D, Fayolle-Minon I. Relationship between maximal exercise capacity and walking capacity in adult hemiplegic stroke patients. Am J Phys Med Rehabil 2006; 85: Pang MY, Eng JJ, Dawson AS. Relationship between ambulatory capacity and cardiorespiratory fitness in chronic stroke: influence of stroke-specific impairments. Chest 2005; 127: Myint PK, Luben NK, Surtees PK et al. Respiratory function and self-reported functional health: EPIC-Norfolk population study. Eur Respir J 2005; 26: Petty GW, Brown Jr RD, Whisnant JP, Sicks JD, O Fallon WM, Wiebers DO. Ischemic stroke subtypes: a population-based study of functional outcome, survival, and recurrence. Stroke 2000; 31: Troosters T, Casaburi R, Gosselink R, Decramer M. Pulmonary rehabilitation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2005; 172: Bach JR. Rehabilitation of the patient with respiratory dysfunction. In De Lisa JA, Gans BM. eds. Rehabilitation medicine. Philadelphia; Lippincott-Raven, 2005, Harvey RL, Roth EJ, Yu D. Rehabilitation in stroke syndromes. Physical medicine and rehabilitation. Philadelphia; Saunders Elsevier, 2007,

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