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Sleep Breath (2012) 16:723–735 DOI 10.1007/s11325-011-0567-0

ORIGINAL ARTICLE

Effects of exercise training associated with continuous positive airway pressure treatment in patients with obstructive sleep apnea syndrome Carolina Ackel-D’Elia & Antonio Carlos da Silva & Rogério Santos Silva & Eveli Truksinas & Bolivar Saldanha Sousa & Sérgio Tufik & Marco Túlio de Mello & Lia Rita Azeredo Bittencourt

Received: 29 April 2011 / Revised: 7 July 2011 / Accepted: 21 July 2011 / Published online: 30 July 2011 # Springer-Verlag 2011

Abstract Purpose The aim of this study was to evaluate the effects of a 2-month exercise training associated with continuous positive airway pressure (CPAP) treatment on the subjective and objective sleep measurements, quality of life, and mood in moderate to severe obstructive sleep apnea syndrome (OSAS) patients. Methods Male patients were randomized into two treatment groups: CPAP (n=19) and CPAP+exercise (n=13). All patients completed 1 month of sleep hygiene, 2 months of treatment (CPAP or CPAP+exercise), and 1 week of washout (no treatment). Fletcher and Luckett sleep questionnaire, Epworth sleepiness scale, sleep diaries, polysomnography, SF-36 inventory of quality of life, Profile of Mood States (POMS) questionnaire, neck circumference, and body composition were evaluated. CPAP+exercise group also underwent cardiopulmonary exercise test before and after treatment. Results Both treatments were effective in improving subjective sleepiness but CPAP+exercise treatment was more effective in maintaining this improvement after washout. No significant differences were found in most of the sleep

C. Ackel-D’Elia (*) : R. S. Silva : E. Truksinas : S. Tufik : M. T. de Mello : L. R. A. Bittencourt Disciplina de Medicina e Biologia do Sono, Departamento de Psicobiologia, Universidade Federal de São Paulo, Alameda Lorena, 105/ap. 34—Jardim Paulista, CEP 01424-000, São Paulo, SP, Brazil e-mail: [email protected] A. C. da Silva : B. S. Sousa Disciplina de Neurofisiologia e Fisiologia do Exercício, Departamento de Fisiologia, Universidade Federal de São Paulo, São Paulo, SP, Brazil

parameters studied in both groups. CPAP+exercise group showed lower values of tension and fatigue on POMS and higher values of physical functioning, general health perception, and vitality on SF-36 after treatment. Conclusions A 2-month exercise training associated with CPAP treatment for OSAS patients has a positive impact on subjective daytime sleepiness, quality of life (physical functioning and general health perception), and mood state (tension and fatigue). Keywords Obstructive sleep apnea syndrome . CPAP . Exercise training . Mood state . Quality of life . Polysomnography

Introduction Obstructive sleep apnea syndrome (OSAS) is characterized by repetitive episodes of cessation of breathing due to airway obstruction during sleep, resulting in hypoxemia and sleep disruption [1]. The consequences of abnormal breathing during sleep include excessive daytime sleepiness, neurocognitive dysfunction, cardiovascular disorders, metabolic dysfunction, and impaired mood and quality of life [2]. The most significant common risk factors for OSAS include obesity, poor physical fitness, male gender, age between 40 and 65 years, cigarette smoking, and use of alcohol [3]. Physical fitness deficits appear to be common in OSAS patients [4–8]. But there are some studies showing normal exercise capacity in OSAS [9, 10]. The most commonly accepted intervention in the management of OSAS is the administration of nasal continuous positive airway pressure (CPAP) [11, 12]. Recently, some authors have evaluated the effect of CPAP treatment on exercise

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performance in OSAS patients. Some of them found that CPAP improved physical fitness in these patients [13, 14] but others did not [15–17]. Lifestyle modifications, especially weight loss, sleep hygiene, and exercise, are often recommended [18]. Weight loss has been recommended on the basis that it should decompress the upper airway and promote its patency [19–21]. Exercise is primarily recommended in order to lose weight, but may also alter the sleep structure [18]. Considering the effect of exercise training on clinical and polysomnographic parameters in OSAS patients, some studies have been showed improvement on subjective sleepiness, quality of life, mood state [3], and decrease of respiratory disturbance index [3, 22, 23]. The main limitation of these studies is the uncertainness if all patients used CPAP associated with exercise training, i.e., data were analyzed together although some patients concurrently used CPAP regularly throughout the exercise training period while the others did not [3, 22, 23]. In another study, Sengul and co-workers [24] showed improvement on apnea–hypopnea index (AHI), healthrelated quality of life, quality of sleep, and exercise capacity after breathing and aerobic exercises in OSAS patients. However, these patients did not use CPAP associated with exercise training. Recently, Ueno and colleagues [25] showed that aerobic exercise training lessens the severity of OSAS in patients with heart failure. It remains uncertain if exercise training associated with CPAP is effective in reducing OSAS symptoms and, if it is effective, whether the benefits are sustained. The aims of this study were to evaluate the effects of a 2-month chronic exercise training program associated with CPAP on the (1) subjective and objective sleep measurements and (2) quality of life and mood state in moderate to severe OSAS patients. We hypothesized that the effects of a 2-month chronic exercise training program associated with CPAP in moderate to severe OSAS patients are different from that observed in patients treated only with CPAP.

Methods Study population Male patients with a clinical and polysomnographic diagnosis of moderate to severe OSAS and considered candidates for nasal CPAP treatment were assessed in the sleep ambulatory unit of Universidade Federal de São Paulo (UNIFESP), Brazil. Inclusion criteria were age between 25 and 65 years, sedentary [26, 27], body mass index (BMI) 15/h, and Epworth Sleepiness Scale (ESS) >9 [28, 29]. Exclusion criteria were a history of regular sportive

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activities (i.e., patients that have ever practiced physical exercises regularly before the study), previous treatment for OSAS (i.e., patients should be naive for CPAP treatment), previously diagnosed chronic diseases that could have an influence on the sleep parameters (i.e., chronic obstructive pulmonary diseases, neuromuscular diseases, chronic heart failure, psychiatric diseases, and rheumatologic disorders), alcohol, abuse drugs, and sedative use. All subjects underwent blood analysis; thoracic X-ray image; pulmonary function tests; ear, nose, and throat (ENT) assessments; and resting electrocardiogram (ECG) to confirm the health status. This study was approved by the institutional review board, and a written informed consent was obtained from each patient in accordance with the policy of the Ethics in Research Board of UNIFESP. Subjects were allowed to withdraw at any time throughout the study. Study design Patients were randomized by entrance order into two treatment groups: CPAP and CPAP+exercise groups. Model study design is presented in Fig. 1. All patients in both groups completed 1 month of sleep hygiene in which they were instructed to avoid alcohol, sedative medicines, and heavy meals before going to sleep. They were also instructed to maintain regular time to go to sleep and avoid sleeping in a supine body position [30, 31]. After that, they completed 2 months of treatment (CPAP or CPAP+ exercise) in which they were stimulated to use CPAP for at least 5 h per night and to participate of the exercise protocol three times per week (only CPAP+exercise group). Patients of the CPAP+exercise group also underwent ECG during exercise. Finally, all patients completed 1 week of washout (no treatment). This period was chosen to eliminate CPAP residual effect. Subjective assessment All patients in both groups completed the Fletcher and Luckett questionnaire to evaluate sleep disturbances [32] in the baseline condition. Subjective sleepiness was assessed using the ESS [28]. This scale was administered four times in the study for both groups: baseline, after sleep hygiene, after treatment, and after washout. All patients also completed sleep diaries for 7 days in the beginning and end of sleep hygiene, in the beginning and end of treatment, and in the washout period (total of 35 days). Patients were asked to score sleep latency (minutes), total sleep time (minutes), number of awakenings, sleep quality (0% to 100%, where 0% means the worst and 100% means the best), and how they feel when they awake (0% to 100%, where 0% means the worst and 100% means the best).

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725 N= 244 OSA male patients assessed

N= 47 OSA patients meet inclusion criteria

CPAP group N= 22 patients

N=3 patients excluded or dropped-out

N=19 patients completed protocol

CPAP + exercise group N= 25 patients

N=13 patients completed protocol

N=12 patients excluded or dropped-out

F&L, ESS, sleep diaries, SF-36, POMS, PSG1, NC and BC evaluations.

F&L, ESS, sleep diaries, SF-36, POMS, PSG1, NC and BC evaluations.

1 month sleep-hygiene

1 month sleep-hygiene

ESS, sleep diaries, SF-36, POMS, PSG2, PSG3 (CPAP), NC and BC evaluations.

ESS, sleep diaries, SF-36, POMS, PSG2, PSG3 (CPAP), NC and BC evaluations, ECGex, CPET.

2 months CPAP

2 months CPAP+exercise

ESS, sleep diaries, SF-36, POMS, PSG4 (CPAP), PSG5, NC and BC evaluations.

ESS, sleep diaries, SF-36, POMS, PSG4 (CPAP), PSG5, NC and BC evaluations, CPET.

1 week washout

1 week washout

ESS, sleep diaries, SF-36, POMS, PSG6, NC and BC evaluations.

ESS, sleep diaries, SF-36, POMS, PSG6, NC and BC evaluations.

Fig. 1 Model study design. F&L Fletcher and Luckett questionnaire, ESS Epworth sleepiness scale, SF-36 quality of life inventory (SF-36), POMS profile of mood state questionnaire, PSG polysomnography,

NC neck circumference, BC body composition, ECGex electrocardiogram during exercise, CPET cardiopulmonary exercise test

We used the Short Form Health Survey (SF-36) questionnaire to assess quality of life of the patients [33]. To evaluate mood state, we used the profile of mood states (POMS) [34]. These instruments were administered four times in the study for both groups: baseline, after sleep hygiene, after treatment, and after washout.

performed in two consecutive nights. Finally, after washout, patients underwent the PSG6. Overnight PSG was performed using an EMBLA digital system (EMBLA S7000; Embla Systems Inc., CO, USA). The following variables were monitored: electroencephalogram (four channels— C3-A2, C4-A1, O1-A2, O2-A1), electrooculogram (two channels—LOC-A2, ROC-A1), electromyogram (two channels—submental and anterior tibialis muscles) using surface electrodes, and ECG (one channel); snoring and body position were detected with EMBLA sensors. Airflow was detected by thermocouple and by nasal pressure flow transducer. Respiratory effort of chest and abdomen were monitored by inductance plethysmography. Oxyhemoglobin saturation (SpO2) and pulse were recorded with a pulse oximeter. Sleep stages and events were manually scored using the international rules [35–37].

Sleep study All patients in both groups completed six nights of in-lab polysomnography (PSG) in the study. The first baseline PSG was realized to confirm OSAS diagnosis (PSG1). After sleep hygiene, patients underwent two consecutive nights of polysomnography (PSG2 and 3; PSG 3 was done for CPAP titration). After treatment (CPAP or CPAP+ exercise), PSG 4 (with CPAP) and 5 (without CPAP) were

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Measurement of neck circumference and body composition Neck circumference was measured using a metric string in the neck to determine its diameter [38]. Body composition was measured using whole-body plethysmography and skinfold measurements. Details regarding the physical concepts and operational principles of air displacement plethysmography (ADP) are reported by Dempster and Aitkens [39]. The BOD POD® Body Composition System (Life Measurements Instruments, Concord, CA, USA) was used to assess body composition. Patients were clothed in a tight-fitting bathing suit and acrylic bathing cap to compress the hair. Patients were weighted to the nearest 0.01 kg using ADP system’s electronic scale (Tanita® Corp., Tokyo, Japan). The scale was calibrated daily using a 20-kg weight. Before patient evaluation, a two-point chamber calibration was performed using the empty chamber and 50.003-L calibration cylinder. The patient’s thoracic gas volume (TGV) was estimated using the BOD POD breathing circuit system [39]. The patient was connected to the breathing circuit housed in the rear chamber through a disposable filtered tube, and the patient was instructed to breathe normally until the moment the system induced an airway occlusion. TGV was calculated during occlusion, where subjects were instructed to puff gently. Final body volume (Vb) was computed based on the initial body volume corrected for TGV and a surface area artifact. Finally, to obtain percentage fat estimates, Vb was converted to body density (Db) (BM/Vb). Percentage fat was calculated using general equation of Siri [40]. Skinfold measurements were taken in accordance with Jackson and Pollock [41]. Neck circumference and body composition were evaluated four times in the study for both groups: baseline, after sleep hygiene, after treatment, and after washout. CPAP treatment All patients (CPAP and CPAP+exercise groups) used CPAP for 2 months and were examined after 1 week, 1 month, and 2 months by trained professionals. Side effects were evaluated. Nocturnal usage was verified by means of a pressure horimeter and the percentage of nights of CPAP use was calculated from data registered in a sleep diary. The average nightly use over the period was calculated by the following ratio: hours of pressure horimeter/nights of sleep with CPAP reported. Cardiopulmonary exercise test and physical training Both cardiopulmonary exercise test and physical training were performed on a treadmill. Physical training was prescribed after all CPAP+exercise group patients under-

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went a cardiopulmonary exercise test on a computerized metabolic gas analysis system (Quark PFT4 FRC and DLCO modules; COSMED, Italy). The protocol of the maximum effort test consisted of a 2-min warm-up with a speed of 4 km/h and speed increments of 1 km/h each minute until exhaustion. The data were calculated automatically using the standard formulae and displayed in a descriptive numerical form (average of 20 s). The following data were obtained: oxygen uptake (L min−1 and mL kg−1 min−1), respiratory exchange ratio (RER), minute ventilation (VE, L min−1), ventilatory equivalent for O2 and CO2 (VE/VO2 and VE/VCO2), expired fraction of O2 and CO2 (FEO2 and FECO2, mmHg), and heart rate (HR, bpm). VO2 at the anaerobic threshold (VO2 at AT) was estimated by the ventilatory method, when VE/VO2 and FEO2 increased while VE/VCO2 and FECO2 remained stable [42]. In the present study, VO2 at AT was identified in all the patients of the CPAP+exercise group. The anaerobic threshold (AT) is a convenient mark used to delimit the upper intensity of aerobic exercise in training programs, corresponding to the work intensity at which the respiratory response to gradual exercise first deviates from linearity [42]. The cardiopulmonary exercise test was repeated after 2 months of training and data were compared to the first test. The exercise sessions consisted only of aerobic exercise (walk and run) and were conducted at the University wellness center. The patients were supervised over a 2-month period, three times per week, with a mean duration of 1 h, according to the results obtained during the maximum effort test. During the sessions, heart rate was monitored and the intensity of the training was adjusted for each patient. Patients started walking in the treadmill in the intensity of 85% of the AT but finished the last week running continuously above the AT for 40 min. All of them exercised in accordance with the exercise training prescribed. Statistical analysis Each variable was tested for the normality of the distribution by the Kolmogorov–Smirnov test. Data were expressed as mean ± SD (standard deviation). Unpaired Student t test was used to compare patient characteristics, sleep parameters, POMS, and SF-36 at baseline (CPAP×CPAP+exercise groups). Paired Student t test was used to compare the exercise parameters before and after treatment on CPAP+exercise group. Two-way analysis of variance (ANOVA) was applied to compare both groups and the effects of the treatments (sleep hygiene, CPAP or CPAP+exercise and washout). In this case, Duncan was the post hoc test used. The level of significance was set at p 0.05). No significant differences were found in both groups according to neck circumference and percentage of body fat (data not shown).

CPAP group (n=19)

CPAP+exercise group (n=13)

p value

49.5±7.7 84.4±9.7 1.7±0.1 28.5±2.2 40.8±1.7 30.7±6.7 24.0

48.4±9.2 81.0±10.0 1.7±0.1 28.0±3.1 40.9±2.8 28.6±8.0 26.6±4.0

NS NS NS NS NS NS NS

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Table 2 Baseline questionnaires, sleep parameters (PSG), profile of mood state scores (POMS questionnaire), and quality of life scores (SF-36 questionnaire) Questionnaires Fletcher and Luckett questionnaire (score) Epworth Sleepiness Scale Sleep latency (min) (sleep diaries) Total sleep time (min) (sleep diaries) Number of awakenings (sleep diaries) Sleep quality (0% the worst–100% the best) (sleep diaries) How they feel when they awake (0% the worst–100% the best) (sleep diaries) PSG Sleep onset latency (min) REM latency (min) Sleep efficiency (TST/TRT %) Stage 1 (%TST) Stage 2 (%TST) Stages 3+4 (%TST) REM sleep (%TST) Arousal index (ev/h) Apnea/hypopnea index (ev/h) Mean oxygen saturation (%) Minimum oxygen saturation (%) Total sleep study time with SaO2