Pulmonary Rehabilitation does not Improve Objective Measures of Sleep Quality in People with Chronic Obstructive Pulmonary Disease

Abstract

Abnormal sleep duration is associated with poor health. Upwards of 50% of people with chronic obstructive pulmonary disease (COPD) report poor sleep quality. The effect of pulmonary rehabilitation on self-reported sleep quality is variable. The aim of this study was to assess the effect of pulmonary rehabilitation on objectively measured sleep quality (via actigraphy) in people with COPD. Sleep quality was assessed objectively using the SenseWear Armband (SWA, BodyMedia, Pittsburgh, PA), worn for ≥4 days before and immediately after completing an 8-week pulmonary rehabilitation program. Sleep characteristics were derived from accelerometer positional data and registration of sleep state by the SWA, determined from energy expenditure. Forty-eight participants (n = 21 male) with COPD (mean (SD), age 70 (10) years, mean FEV₁ 55 (20) % predicted, mean 45 (24) pack year smoking history) contributed pre and post pulmonary rehabilitation sleep data to this analysis. No significant differences were seen in any sleep parameters after pulmonary rehabilitation (p = 0.07–0.70). There were no associations between sleep parameters and measures of quality of life or function (all p > 0.30). Sleep quality, measured objectively using actigraphy, did not improve after an 8-week pulmonary rehabilitation program in individuals with COPD. Whether on-going participation in regular exercise training beyond the duration of pulmonary rehabilitation may influence sleep quality, or whether improving sleep quality could enhance rehabilitation outcomes, is yet to be determined.

Keywords:

• COPD
• pulmonary rehabilitation
• sleep
• actigraphy

Introduction

Sleep is fundamental for both life and good health (1). Healthy sleep needs to occur regularly, at an appropriate point in the circadian cycle and be of sufficient duration and quality (2). In healthy individuals abnormal sleep duration, either too much or too little sleep, is associated with poor health – including increased risk of hypertension, metabolic syndrome, diabetes mellitus; and reduced cognitive capacity and mood disturbance (3). The prevalence of complaints of insufficient sleep in the general population is between 20% and 40% (4).

Chronic obstructive pulmonary disease (COPD) is characterised by a progressive decline in lung function, multiple comorbidities and recurrent exacerbations. Poor sleep is also a common feature of COPD, with upwards of 50% of patients reporting poor sleep quality (5). In people with COPD sleep quality can have a profound effect on daily quality of life (6), and poor sleep is associated with increased morbidity and mortality (7).

In the general population the relationship between physical activity and sleep quality has been widely investigated (8). A complementary relationship between physical activity and sleep quality has been reported, such that sleep quality can influence amount of physical activity and activity participation can affect sleep quality (9). Exercise training programs can effectively improve sleep quality in middle age and older adults (10), with interventions, such as brisk walking four times per week (11), or structured daily low-intensity activity (12) improving self-reported sleep quality in older adults. In younger healthy populations, greater objectively measured physical activity participation is associated with better sleep quality (13). In people with COPD studies of the effect of exercise training, in the form of pulmonary rehabilitation, on sleep quality are limited.

Pulmonary rehabilitation is an integral component of COPD management, achieving positive patient-related outcomes with respect to symptoms and function (14), and reducing the frequency of exacerbations and need for hospitalisation (15). Interdisciplinary pulmonary rehabilitation programs, commonly comprise 2–3 sessions of exercise training – including both aerobic training and strength training – over 8–12 weeks, and may include education and behaviour change interventions (14). Three studies have reported subjective sleep quality outcomes for people with COPD after pulmonary rehabilitation. Two studies reported statistically significant improvements in Philadelphia Sleep Quality Index (PSQI) following pulmonary rehabilitation, however, post rehabilitation PSQI scores remained high (≥5), indicating the persistence of poor sleep quality (16,17). In addition, improvement in PSQI did not exceed the minimal important difference (18). A third study found no difference in PSQI following pulmonary rehabilitation (19). To date, there have been no reports of objectively measured changes in sleep parameters relative to pulmonary rehabilitation participation.

Objective sleep assessment is not a routine part of clinical management for most people with COPD. However, activity-based sleep-wake monitoring (actigraphy) provides a cost-effective, easily accessible and unobtrusive assessment tool (20) to investigate sleep patterns in this population. Activity-based assessment has previously been used to characterise sleep abnormalities in people with COPD, and has the capacity to provide information on patterns of rest and circadian rhythm disturbances (6). The Sensewear Armband (SWA; BodyMedia, Pittsburgh, PA) is a valid tool for the assessment of physical activity participation in people with COPD (21), and has been validated for the assessment of sleep and wake in people with sleep disordered breathing (22). The aim of this analysis was to assess the effect of pulmonary rehabilitation on objectively measured sleep quality (measured via actigraphy using the SWA) in people with COPD.

Methods

This is a secondary analysis of data collected as part of two separate pulmonary rehabilitation clinical trials, including a randomised, controlled equivalence trial comparing home-based and centre-based rehabilitation for COPD (23). Both parent studies were approved by the Human Research Ethics Committees of Alfred Health and Austin Health, Melbourne, Australia.

The current sub-group of participants was recruited prospectively on referral to the pulmonary rehabilitation program at one of two tertiary referral centres. To be eligible for inclusion participants had a diagnosis of COPD; a smoking history ≥10 pack years; no respiratory exacerbations within the previous four weeks, and absence of comorbidities that preclude exercise training. Potential participants were excluded if they had a clinical diagnosis of asthma or had undertaken pulmonary rehabilitation within the last 2 years. At recruitment participants completed a standard pulmonary rehabilitation assessment, including assessment of exercise capacity (6-minute walk test), health related quality of life (chronic respiratory disease questionnaire (CRQ); COPD assessment test (CAT)) and perceived dyspnoea (modified Medical Research Council dyspnoea score (mMRC)). Written informed consent was obtained from all participants.

Objective measures of sleep quality were obtained from the SWA. The SWA is a portable, multi-sensor armband that contains a tri-axial accelerometer and sensors that measure galvanic skin response, heat flux and skin temperature. The SWA is worn over the triceps muscle of the left upper arm continuously with the exception of bathing. The SWA activates automatically on contact with the skin, and adherence to monitor usage can be ascertained on downloading of final data. Data are stored minute by minute during both wake and sleep, and a proprietary algorithm (version 8) estimates energy expenditure and activity intensity (metabolic equivalents (METs)).

Data handling

Participants were provided with the SWA for a period of 7 days prior to commencing pulmonary rehabilitation. The first day of SWA wear was excluded from analysis upon data retrieval. It was determined a priori that a minimum of four valid days (three nights) of actigraphy data (≥10 hours wear time/day) (23) per participant was required for participant data to be included in the analysis. Two researchers extracted data, independently, for determination of daytime and night-time, and resolved discrepancies by consensus. A computer algorithm was used to extract sleep parameters.

Sleep measures

Sleep characteristics were computed from bedtime to rise-time. Bedtime was defined as the start of any period ≥ 10 minutes duration categorised by accelerometer positional data as lying down, coupled with no physical activity registration, which occurred after 9 pm (21:00 hours). Night-time was considered to commence from 9 pm to account for the peak in evening napping behaviour, but not night-time sleep, found to occur between 8.30 pm and 9 pm in community dwelling older adults (24). Rise-time was determined as the start of any period of upright positioning ≥ 10 minutes duration, without concurrent sleep registration, after 5 am. Sleep data were excluded where participants failed to register a bedtime within 24 hours of the preceding rise-time, or where there was ≥180 minutes of consecutive SWA non-wear time overnight (25).

Sleep parameters

Sleep parameters were derived from accelerometer positional data, and registration of sleep state by the SWA determined by energy expenditure. Four sleep parameters were considered for analysis: sleep onset latency (SOL), the time (in minutes) between bedtime and first recorded sleep epoch; wake after sleep onset (WASO), the number of minutes spent awake after the onset of sleep; total sleep time (TST) defined as the number of minutes between bedtime and rise-time minus any time spent awake, and sleep efficiency (SE), the ratio of TST and total time in bed from bedtime to rise-time expressed as a percentage (%).

Data analysis

Statistical analyses were conducted using PASW (Version 24 – IBM, Arnorack, NY). Descriptive statistics are presented as mean (standard deviation, SD) or median (interquartile range, IQR). Categorical variables are reported descriptively using frequency (n) and proportion (%). Sleep outcomes pre and post pulmonary rehabilitation were compared using paired t-tests or the non-parametric equivalent depending upon distribution.

The relationship between sleep parameters at completion of pulmonary rehabilitation with number of pulmonary rehabilitation sessions attended and change in exercise tolerance (6 minute walk distance) and quality of life (CAT score and CRQ category scores) were assessed using correlation coefficients. A p-value <0.05 was considered significant.

Results

Forty-eight participants (n = 21 male) with COPD had pre and post pulmonary rehabilitation sleep data of sufficient days for inclusion in the analysis. Thirty-five participants undertook centre-based pulmonary rehabilitation and 13 did home-based pulmonary rehabilitation. Participants had a mean (SD) age of 70 (10) years, forced expiratory volume in one second (FEV₁) of 55 (20) %predicted, and 45 (24) pack year smoking history (Table 1). Median [IQR] rise-time was 07:29 hours [06:33 to 08:09 hours] and bedtime 22:23 hours [2157 to 22:46 hours]. Sleep quality was relatively poor with a median sleep efficiency of 75% [66% to 84%]. Forty-one participants (85%) completed ≥70% of all rehabilitation sessions. At the end of pulmonary rehabilitation significant improvements in functional capacity and health related quality of life were achieved (all p < 0.03) (Table 1).

Table 1. Participant characteristics (mean (SD) unless stated).

Participant characteristic	Baseline	End rehab	p
n	48	–
Male: Female, n	21:27	–
Age, years	70 (10)	–
FEV1, %predicted	55 (20)	–
FER	47 (12)	–
Pack year history	45 (24)	–
Current smoker, n	7	–
LTOT, n	3	–
6MWD, m	410 (108)	437 (121)*	0.001
CAT score	21 (7)	18 (7)*	0.027
CRQ: Dyspnoea	13 (6)	18 (7)*	<0.001
Fatigue	15 (5)	16 (5)	0.005
Emotional function	31 (9)	35 (8)*	0.003
Mastery	18 (6)	22 (5)*	<0.001
mMRC 0/1/2/3/4, n	0/20/10/17/1	6/17/14/7/3

Notes: FEV₁ = forced expiratory volume in one second; FER = forced expiratory ratio (FEV₁/forced vital capacity); LTOT = long term oxygen therapy; 6MWD = 6 minute walk distance; CAT = COPD Assessment Test; CRQ = Chronic Respiratory disease Questionnaire; mMRC = modified medical research council dyspnoea score.

*= difference from baseline ≥ minimum important difference.

p < 0.05 = significant.

No significant differences were seen in any sleep parameter between pre and post pulmonary rehabilitation (effect size all <0.2) (Table 2). At end rehabilitation there were no significant between group differences in any sleep parameter between those who had undertaken ≥70% (26) of all exercise training sessions (‘completer’) and those who did not (‘non-completer’) (all p > 0.30) (Table 3). A significant within-group increase in TST was evident in pulmonary rehabilitation ‘completers’ (median [IQR] TST: baseline 390 [339–438] minutes vs. end rehabilitation 405 [343–438] minutes; Z = −2.2, p = 0.03).

Table 2. Sleep characteristics pre and post pulmonary rehabilitation (median [interquartile range]).

	Pre	Post	Change	ES	p*
Sleep onset latency, min	20 [8 to 39]	15 [6 to 28]	−2.2 [−15 to 5]	0.1	0.2
Wake after sleep onset, min	79 [47 to 117]	84 [39 to 125]	−3 [−21 to 16]	0.04	0.7
Total sleep time, min	391 [347 to 439]	399 [358 to 434]	8 [−13 to 44]	0.2	0.07
Sleep efficiency, %	75 [66 to 84]	77 [67 to 87]	1 [−3 to 6]	0.1	0.2
Awakenings, n	9 [6 to 12]	9 [6 to 14]	0 [−1 to 2]	0.08	0.4

Note: ES = effect size; *Via Wilcoxon Signed Rank Test for paired measures. Mean (SD) nights of sleep monitoring pre and post pulmonary rehabilitation were 6(1) and 5(1), respectively.

Table 3. Change in sleep characteristics pre to post pulmonary rehabilitation in completers vs. non-completers (mean (SD)).

	Completers n = 41	Non-completers n = 7	p*
Sleep onset latency, min	−2 (31)	−3 (23)	0.9
Wake after sleep onset, min	−1 (35)	6 (51)	0.6
Total sleep time, min	16 (50)	−10 (81)	0.3
Sleep efficiency, %	2 (8)	−1 (6)	0.3
Awakenings, n	0 (3)	1 (4)	0.3

Note: between group difference via *Independent samples t-test.

Discussion

In the current analysis, objectively assessed sleep parameters were not significantly improved after completion of an 8-week pulmonary rehabilitation program, despite improvements in traditional pulmonary rehabilitation outcomes. There was no relationship between any sleep parameter and measures of health related quality of life or exercise tolerance at either baseline or after completion of pulmonary rehabilitation. At end rehabilitation female participants had significantly less SOL than did male participants, however, there was no significant difference in SOL from baseline to end rehabilitation for either male or female participants. Despite the majority of participants completing at least 70% of prescribed sessions, and achieving statistically and clinically important improvements in functional capacity and quality of life (27–29), the effectiveness of pulmonary rehabilitation largely did not translate into improvements in sleep quality.

Exercise training programs can lead to improvements in sleep quality for healthy middle aged and older adults (10), however, the findings presented here and elsewhere (19) suggest this may not hold true for people with COPD. In the general population there is some evidence of disturbed sleep and/or sleep loss being associated with a reduction in both peak exercise capacity and functional performance of the upper and lower limbs (9). Despite the improvements in exercise and functional capacity achievable by people with COPD with pulmonary rehabilitation (30), and demonstrated by the participants in this study, the duration of training or magnitude of improvement in capacity required to impact on sleep quality is unknown. In people with COPD night-time sleep impairment diminishes an individual’s ability to engage in physical activity on a regular basis (31). Whether an inability to improve sleep quality, despite improvements in functional capacity, could explain the failure of pulmonary rehabilitation to routinely translate into increased daily physical activity (32) requires further investigation.

Previous studies of the effect of pulmonary rehabilitation on self-reported sleep quality in people with COPD have reported variable effects using the PSQI- (16,17,19) when considering sleep disturbance over the preceding 1-month (33). Despite being commonly used to assess sleep quality in people with COPD, the reliability and validity of the PSQI in this population has not been established (34). In addition, co-morbidities seen frequently in people with COPD, particularly depression and impaired cognition (35), have been demonstrated to reduce the accuracy of sleep time perception and contribute to discrepancies between subjective and objective reports of sleep quality (36). These issues associated with self-report measures of sleep quality may help to explain why we did not see a relationship between objectively measured sleep parameters and quality of life, which has been reported previously using subjective sleep measures (6,37).

The exercise training component of pulmonary rehabilitation includes both aerobic training and strength training. Typically, pulmonary rehabilitation sessions consist of up to 30 minutes of aerobic training, which may be performed in shorter bouts interspersed with rest to achieve the total exercise time (14). A meta-analysis of the effects of physical activity on sleep in healthy adults found that activity duration influenced sleep outcomes such that longer exercise bout duration is associated with better sleep quality (38). However, the exact duration of activity required to achieve improvements in sleep quality is not clear. People with COPD have a reduced duration and intensity of daily physical activity compared to healthy control subjects (39). It is possible that the lack of improvement in sleep quality following pulmonary rehabilitation in people with COPD is a consequence of an inability to exercise at sufficient intensity for an arbitrary threshold duration, despite being able to achieve improvements in exercise capacity and function.

This secondary analysis of data collected as part of two separate pulmonary rehabilitation clinical trials suggests that in people with COPD objectively measured sleep quality does not improve as a consequence of pulmonary rehabilitation. Although there was a modest improvement in TST at end rehabilitation by ‘completers’, failure to detect any other changes in sleep quality means the possibility that this finding represents a Type I error cannot be ruled out. A drawback of the present analysis is the lack of a sleep diary for documentation of individual rise-time and bedtime, resulting in the need for data analysis rules regarding determination of time of night after which sleep would be considered to occur (i.e. 21:00 hours) for the purposes of extracting sleep data from the SWA. This may have served to under (or over) estimate factors like bedtime and subsequent sleep parameters; or obscured the effect of co-morbidities, such as depressed mood, which has been associated with actigraphy parameters of inactivity and daytime napping (40). Additionally, the lack of a subjective report of sleep quality means we can only infer patient perception of sleep quality based on objective sleep quality outputs and cannot make direct comparisons with previous reports of subjective sleep quality (both positive and negative) relative to pulmonary rehabilitation completion (16,17,19).

Sleep quality, measured objectively using actigraphy, did not improve after an 8-week pulmonary rehabilitation program in individuals with COPD. Whether ongoing participation in regular exercise training beyond the duration of pulmonary rehabilitation may influence sleep quality, or whether improving sleep quality could enhance rehabilitation outcomes, is yet to be determined.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by a La Trobe University Research Collaboration Grant; National Health and Medical Research Council (NHMRC) under Grant APP 1046353; Institute for Breathing and Sleep, and the Australian Lung Foundation/Ludwig Engel Grant in Aid for Physiological Research. NSC is the holder of an NHMRC Early Career Fellowship Grant APP1119970.