Abstract
Sleep-related disorders are common in patients with chronic obstructive pulmonary disease (COPD) and, possibily, other lung disorders. Exercise has been shown to improve sleep disturbances. In patients with COPD, pulmonary rehabilitation (PR) produces important health benefits with improvement in symptoms, exercise tolerance, and quality of life. However, the effect of PR on sleep quality remains unknown. The aim of this observational study was to evaluate sleep quality in patients with chronic lung disease and the role of PR as a non-pharmacologic treatment to improve sleep. Sixty-four patients with chronic lung disease enrolled in an 8-week comprehensive PR program, and completed the study (48% male; obstructive [72%], restrictive [20%], mixed [8%]; 44% on supplemental oxygen). Baseline spirometry [mean (SD)]: FEV1% pred = 48.9 (17.4), FVC% pred = 72.5 (18.1), and FEV1/FVC% = 53.1 (18.9). Exercise tolerance and questionnaires related to symptoms, health-related quality of life (HRQL), and sleep quality using the Pittsburgh Sleep Quality Index (PSQI) were obtained before and after PR. 58% reported poor sleep quality (PSQI > 5) at baseline. Sleep quality improved by 19% (p = 0.017) after PR, along with significant improvements in dyspnea, exercise tolerance, self-efficacy, and HRQL. Sleep quality in patients with chronic lung disease was poor. In addition to expected improvements in symptoms, exercise tolerance, and HRQL after PR, the subgroup of patients with COPD had a significant improvement in sleep quality. These findings suggest that PR may be an effective, non-pharmacologic treatment option for sleep problems in patients with COPD.
Keywords :
Introduction
Sleep-related disorders have become important public health concerns that directly impact quality of life (Citation1–5). Sleep is restorative in daily functioning (Citation6) and intrinsically important in sustaining physical and psychosocial well-being (Citation7). Available data in the general population indicate that sleep complaints are common.
Chronic obstructive pulmonary disease (COPD) is the most common chronic lung disease and a major cause of death and disability (Citation8–16). These patients often complain of difficulty sleeping; objective measures have demonstrated impaired sleep, often related to symptoms such as cough or sputum production (Citation17, 18). In addition, patients with COPD commonly have other abnormalities such as nocturnal oxygen desaturation (NOD) that may worsen sleep disturbances. Moreover, sleep disordered breathing (SDB), like obstructive sleep apnea syndrome (OSA), has been linked to higher morbidity and mortality if COPD is present (so called the overlap syndrome [OLS]) (Citation19). Therefore, poor sleep may be an important contributor to impaired quality of life in patients with OLS. Sleep related disorders may also be common in other chronic lung diseases, butthere are little (or no) published data on this topic.
In patients with COPD, pulmonary rehabilitation (PR) produces important health benefits such as improvement in respiratory symptoms, exercise tolerance, and quality of life (Citation20). Physical exercise has been shown to improve sleep in normals, yet its effect on sleep-related disorders has not been previously studied systematically in patients with chronic lung diseases, and specifically in COPD (Citation5, Citation21–23). One might hypothesize that PR, including exercise training, could produce improvements in sleep in such patients and be an important contributor to improved health outcomes after PR (Citation18, Citation24–27).
The purposes of this study were to: 1) evaluate the effect of PR on sleep quality in patients with chronic lung diseases and; 2) explore the relationships between poor sleep quality and quality of life in these patients.
Methods
Patients and study design
This was a prospective, observational study in patients enrolled in the UCSD PR Program during a 1-year period from January to December, 2008. Selection criteria for PR included: age ≥ 18 years; diagnosis of chronic lung disease confirmed by medical history, physical examination, and pulmonary function tests; and clinically stable (no recent acute respiratory exacerbation, normotensive with or without medication, no symptoms of acute heart failure or coronary symptoms, and no other medical conditions that would interfere with full participation in the program). All PR Program patients were invited to participate in the study. Experienced staff performed PR evaluation and treatment. The UCSD Human Subjects Protection Program approved the protocol and written informed consent was obtained from all subjects. A total of 86 subjects enrolled in the PR program, agreed to participate in the study, and completed baseline assessments. Sixty-four patients (74%) completed the PR program and the post-PR assessment and, therefore, were included in the final analyses. The evaluation included questionnaires and measures of exercise tolerance just prior to the start and at the end of the 8-week PR Program.
The UCSD PR Program encompassed 16 sessions over 8 weeks, including components of individual and group education, physical and respiratory care instruction, psychosocial support, and exercise training. Psychosocial support was provided by enthusiastic and supportive staff as well as through a weekly support group led by a psychologist. Sleep issues were not specifically addressed in these sessions. The exercise program included lower and upper extremity endurance as well as strength and flexibility training.
Measurements
Information obtained from the PR evaluation included: demographics; body mass index (BMI); co-morbidities; use of medications and supplemental oxygen; available pulmonary function tests; exercise tolerance evaluated with a 6-minute walk (6MW) test; and questionnaires to assess sleep quality, health-related quality of life (HRQL), dyspnea, and self-efficacy for walking (SEW).
Sleep quality was evaluated with the Pittsburgh Sleep Quality Index (PSQI) (Citation28). The PSQI consists of 19 items and provides a well-validated global index of sleep quality over the previous 1-month time interval. It can be divided into 7 components that evaluate various aspects of sleep quality: subjective sleep quality; latency, duration, efficiency, and disturbances of sleep; use of sleep medication; and daytime dysfunction. The global PSQI score has a range of 0 to 21, with higher scores indicating worse sleep quality. PSQI >5 is generally considered to be an indicator of poor sleep quality.
Health-related quality of life was evaluated using the SF-36 Health Survey (SF-36), a general health profile. The SF-36 contains 36 items used to develop eight subscales: physical functioning, role limitations due to physical health problems, bodily pain, general health perceptions, vitality, social functioning, role limitations due to emotional problems, and mental health (Citation29). In addition, physical (PCS) and mental (MCS) composite summary scores were calculated from the subscales.
Dyspnea was assessed with the UCSD Shortness of Breath Questionnaire (SOBQ) (Citation30). The SOBQ asks patients to rate the severity of their breathlessness experienced with 21 various daily activities on a 6-point scale from “None at all” to “Maximal or unable to do because of breathlessness.”
Self-efficacy for walking was measured with a questionnaire modified from that developed by Kaplan and coworkers (Citation31). Subjects were asked to rate the level of walking duration they are 100% confident they can perform using nine statements of increasing difficulty.
Statistical analysis
Descriptive statistics were used to characterize measures before and after the PR program. Comparisons of outcomes before and after PR in all patients and in obstructive and restrictive subgroups were evaluated by paired t-tests. The results in patients with mixed obstructive and restrictive diseases were not analyzed separately because of the small number of subjects. The relationships among baseline measures of sleep quality, lung function, exercise tolerance, and psychosocial function were evaluated initially with a correlation matrix. Variables found to be significantly correlated (p < 0.15) were then evaluated further using stepwise, multivariate regression models to explore the interrelationships and independence among these various measures. Physical (PCS) and mental (MCS) composite scores of the SF-36 were used as dependent variables in these analyses. A p-value < 0.05 was considered statistically significant. All data analyses were conducted using SPSS software, release 17.0 (Chicago, IL, USA).
Results
Sixty-four patients (74%) completed pre- and post-program assessments. The subjects who completed the initial assessment only and, therefore, were not included in the analyses [COPD (Citation17); restrictive (Citation4); mixed (Citation1)] did not differ at baseline from the remaining 64 in age, BMI, pulmonary function, exercise tolerance, use of supplemental oxygen, medications, co-morbidities (including OSA prevalence), dyspnea, or PSQI.
Baseline data prior to the PR program are presented in for all 64 subjects, as well as for those with obstructive (Citation46), restrictive (Citation13) and mixed (Citation5) lung diseases. These results indicate that the cohort includes generally elderly patients with moderate to severe chronic lung diseases and a high prevalence of associated co-morbidities. Of note, 19% had a previous diagnosis of obstructive sleep apnea. Poor sleep quality (PSQI > 5) was reported in 58% of subjects [mean PSQI = 6.9 + 3.9 (SD)]. PSQI was negatively correlated with mental (r = –0.47, p < 0.001) and physical r = -0.28, p = 0.03) components of quality of life, and also with shortness of breath (r = 0.27, p = 0.03). Both OSA and non-OSA patients reported similar poor sleep quality at baseline (OSA: mean = 6.9 + 3.8 (SD); no OSA: mean = 6.9 + 4.5 (SD), p = NS).
Table 1 Clinical, demographic and anthropometric characteristics of the patients*
Results of the multiple regression analyses for evaluating the relationships among baseline HRQL and other measures are presented in for multivariate regression models with either MCS or PCS as dependent variables. These results suggest that sleep quality was significantly related to both mental and physical quality of life, independent of dyspnea and exercise tolerance. The best predictors for the mental component of HRQL were sleep quality, dyspnea, the physical component of HRQL, and exercise tolerance (adjusted R Square = 0.38). The best predictors for the physical component of HRQL were dyspnea, the mental component of HRQL, and sleep quality (adjusted R Square = 0.37).
Table 2. Results of the stepwise multiple regression analysis with the mental and the physical components of health-related quality of life as dependent variables
Changes after PR in measures of dyspnea, sleep quality, quality of life, and exercise tolerance are presented in for the 46 subjects with obstructive lung disease and 13 with restrictive disease who completed the PR Program and post-program assessments. The results show that PR produced significant improvements in dyspnea (SOBQ), exercise tolerance (6MW), self-efficacy (SEW), and health-related quality of life (HRQL [MCS and PCS]) in subjects with COPD. Mean changes for SOBQ, 6MW, SEW, and SF-36 in patients with restrictive diseases were similar in magnitude as for those with COPD, but only the changes in 6MW and SEW reached statistical significance.
Table 3. Baseline values and changes from baseline after pulmonary rehabilitation in obstructive and restrictive lung disease patients
Sleep quality improved significantly in all subjects (6.9 ± 3.9 to 6.0 ± 3.8, p = 0.02) and in the subgroup with COPD (6.6 ± 3.9 to 5.5 ± 3.6, p = 0.01). In the restrictive subgroup, baseline sleep quality was slightly worse than for patients with COPD (8.2 ± 3.7 versus 6.6 ± 3.9, p = NS) and did not change after PR. Statistically significant changes were found in the PSQI Subscales of Sleep Disturbances in all subjects and in those with COPD and in Sleep Latency for restrictive patients. Poor sleep quality was reported by 58% of patients before PR and 47% after PR (p < 0.001).
Discussion
The results of this study suggest that sleep is severely disturbed in patients with chronic lung diseases. In addition, in patients with COPD sleep quality improves significantly after comprehensive PR. Because improvement in sleep quality after PR has not been reported previously, this may represent an important health issue not adequately addressed in current PR programs and guidelines.
Given the severity of disease of patients typically referred to PR, it is not unexpected for a number of patients not to complete the full program, mostly for medical reasons. The rate of drop-outs in our study was similar to other published literature (Citation32). There were no clinical differences, including OSA prevalence, between completers and non-completers. Also, OSA was not a confounding factor of poorer sleep quality.
Epidemiological studies have demonstrated a higher risk of cardiovascular disease, lower quality of life, and increased health care costs in patients with various sleep disorders (Citation33–35). Published large epidemiologic studies found a similar prevalence of poor sleep in the elderly, comparable to our results (Citation36, 37). Interestingly, a large San Diego County population-based study of 3667 subjects reported an even higher prevalence of poor sleep quality (64% for both Non-Hispanic Whites [NHW] and Hispanics of Mexican Descent [HMD]) (unpublished results). Compared to the present report, subjects in this previous study were significantly younger (55 ± 17 years for NHW and 41 ± 16 years for HMD versus 68 ±10 years in the present study)). One possible explanation for the observed differences is that patients with chronic disease are more accustomed to having sleep disturbances and may, therefore, report better sleep quality (i.e., lower score on the PSQI).
Patients with chronic lung diseases have markedly reduced HRQL. Our results suggest that poor sleep quality was significantly related to both mental and physical aspects of HRQL in this cohort with both restrictive and obstructive lung disorders. Although one cannot determine from these associations whether poor sleep quality results from or is causally related to poor HRQL, the fact that the PSQI score was significantly related to both the MCS and PCS summary scores from the SF-36, independent of dyspnea (and exercise tolerance for MCS), might suggest that poor sleep quality is an important, independent contributor to reduced HRQL. Certainly, sleep-related problems such as insomnia, could be contributing to reduced HRQL in these patients.
In addition to the causes of poor sleep quality seen in a general population and in patients with other chronic diseases, patients with COPD may have particular problems that contribute to poor sleep. Arterial hypoxemia (and/or hypercapnia) is common, may be worse at night (e.g., nocturnal oxygenation desaturation), and may contribute to poor sleep quality (Citation38). In addition, changes during sleep in chemoreceptor sensitivity and ventilatory control, respiratory mechanics, respiratory muscle function, and symptoms such as cough and sputum production may occur in these patients (Citation17, Citation35, Citation39–45). The relationships between these respiratory specific abnormalities and sleep quality remains poorly defined (as noted in the NETT trial) (Citation17, Citation46, Citation47), though it is certainly reasonable to speculate that poor sleep quality is an important contributing factor to the markedly impaired quality of life seen in patients with COPD.
The results of this study also suggest that PR improved sleep quality in patients with moderate-to-severe COPD. Multidisciplinary PR programs typically include education, instruction in respiratory and chest physiotherapy techniques, psychosocial support, and exercise training (Citation48–52). Such programs do not typically evaluate or address specific sleep problems. Exercise training may reduce the severity of OSA and improve quality of life related to sleep and functional outcomes (Citation26). However, the amount of exercise usually has been assessed by subject self-report in large epidemiological studies (Citation54, 55). In one small study of patients with COPD studied before and after PR, Zanchet did not find any differences in sleep architecture (Citation53). Although polysomnography (PSG) is a highly reliable tool to evaluate SDB, used alone it may not be sufficiently sensitive to detect minor changes that may occur after a few weeks of low levels of exercise typical in PR. Also, patients with normal or nearly normal PSGs may still report poor sleep quality assessed by questionnaires, which may reflect other sleep-related problems such as insomnia.
Although one cannot be certain about which aspect(s) of PR might be most effective in improving sleep quality, physical activity has been associated with a decrease in the prevalence of sleep disorders (Citation22). Published studies include heterogeneous physical activity assessments that make it difficult to determine which exercise may help the most. In the Wisconsin Sleep Cohort Study, Peppard and Young found that increasing exercise was associated with less SDB (Citation54). They reported significantly decreased odds of having worse sleep-disordered breathing with increasing level of exercise (odds ratio of 0.39 [0.19–0.80] for 3 to 6 hours per week of exercise predicting an apnea-hypopnea index >15). Quan and coworkers found similar results from vigorous exercise and reported that the intensity of physical activity was related to the degree of improvement (Citation55). Interestingly, in Peppard's study, the exercise implemented was similar to that used in PR programs. Our study shows that PR was associated with significantly improved sleep quality in patients with moderate to severe COPD, reducing the PSQI score by 19%. Exercise can improve ventilatory muscle strength and endurance (Citation56), strengthen the pharyngeal musculature (Citation57), and redistribute adipose tissue away from the upper airway (Citation58, 59), with no change in BMI, body weight, body shape, or composition (Citation54, Citation60). It is noticeable, though, that the majority of studies linking exercise and sleep have been performed in normals as part of epidemiological surveys and, therefore, are not fully comparable to patients with chronic lung diseases as in the current study (Citation22, Citation55, Citation61).
Low exercise levels commonly used in training patients with COPD may not be sufficient to result in measureable changes in objective physiological sleep outcomes (such as sleep efficiency or sleep architecture) in addition to significant changes in subjective measures such as sleep quality. It is also possible that the modest levels of exercise may lead to improvements in other sleep disturbances, such as insomnia, that could positively impact HRQL.
It is important to note that only patients with COPD reported improved sleep quality after PR in this study. This may be important because the mechanics and pathophysiology of obstructive versus restrictive patients are very different. Patients with interstitial type restrictive lung diseases typically demonstrate more severe arterial hypoxemia at rest, with exercise, and, possibly, less severe decline of nocturnal levels of O2 than in patients with COPD. Evaluating and optimizing the oxygen prescription is an important treatment goal in PR. Improved oxygenation may positively affect sleep outcomes, at least in cases where nocturnal hypoxemia is an important contributing factor.
Although the number of patients with restrictive lung disease is small in our study and may limit the conclusions, we did not observe even a trend of improved sleep quality in this subgroup. Interestingly, the restrictive subgroup also reported poorer sleep quality at baseline (p = NS). Such findings should be confirmed in larger studies. Nevertheless, the findings in this preliminary study are provocative and emphasize the need to better evaluate sleep in patients with various types of chronic lung diseases.
Although our study was not intended to explore the interactions between COPD and OSA or the effect of PR on OSA (in patients with the OLS), a comment is warranted. Recently, the Sleep Heart Health Study, a prospective multicenter cohort study (Citation62), reported no association between (generally mild) COPD and OSA. Furthermore, the presence of airway obstruction did not seem to affect the number of respiratory events. If CPAP is used to treat OSA, sleep quality and sleep-related symptoms can improve. A recent publication reported that CPAP treatment in the OLS reduced death and exacerbation rates (Citation63). Untreated OSA affects sleep quality, and, therefore, may influence outcomes related to sleep. However, there is a well reported poor compliance in patients using CPAP despite being diagnosed of OSA (Citation64, 65). Also, based only on self-report, it is likely that some patients in the non-OSA group may, in fact, have had OSA that was not yet diagnosed.
There are several limitations in this preliminary, observational study conducted to evaluate the potential benefits of PR on sleep in patients with chronic lung diseases. This study relied on the PSQI questionnaire. Although this is a well-validated measure of sleep quality that explores several domains of sleep, many other factors involved in sleep disturbances are not assessed with the PSQI. Studies that include objective measures of sleep, such as polysomnography, may help elucidate which sleep parameters improve (i.e., sleep efficiency, or sleep architecture).
Subjective and objective measures assess different aspects of an individual's sleep experience; subjective sleep assessment reflects mainly the patient's perception of sleep and may not indicate the symptoms as accurately as objective measures. Because of our significant results, future studies that include objective sleep assessment should be pursued to better understand such changes. Although no data were collected about CPAP compliance and the diagnosis of OSA was by self-report, there were no differences between OSA and no-OSA patients.
In addition, the relatively small number of patients with restrictive lung disorders may be insufficient to draw valid conclusions about change in sleep qualify after PR in this subgroup, although they did improve in other objective measures like SEW and 6-MW. Although patients with COPD may be the subgroup whose sleep is most likely to benefit from PR, this study was not designed to specifically evaluate sleep disorders and dysfunction in these patients. This may be another important area of future investigation. Another limitation is that the study was not designed evaluate which component(s) of PR was(were) responsible for the change in sleep quality.
In summary, we found that sleep quality in patients with chronic lung disease is poor and improved significantly after PR, at least in the subgroup of patients with COPD. Additionally, sleep quality appeared to be an important, independent covariate in prediction models for both mental and physical components of HRQOL in patients with chronic lung diseases. These findings suggest that PR may be an effective, non-pharmacologic treatment to improve sleep quality in patients with COPD and, perhaps, in other chronic lung diseases. If so, then it may be important to fully evaluate and incorporate treatment strategies directed at sleep-related disorders in the optimal design of PR programs.
Declaration of Interest
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
Acknowledgments
The authors want to thank Catherine Larsen for help with data analysis and manuscript editing and, in alphabetical order, Maria Correa, Trina Limberg, Anne Mohney, Russel Trojino, and Arianna Villa for data collection and patient care throughout the program. Also we want to thank all the patients who kindly participated in this study. Part of this study was presented in abstract form at the 2011 International Conference of the American Thoracic Society.
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