Sleep-Wake Disturbances in Patients with Advanced Cancer and Their Family Carers

Article Outline

• Abstract
• Introduction
• Methods
• Results
  • Subjective Data: Sleep History, Sleep Diary, and Validated Tools
  • Objective Data: Actiwatch
  • Interrelationship of Subjective and Objective Data
• Discussion
  • Limitations
• Conclusions
• Acknowledgments
• References
• Copyright

Abstract 

Sleep disturbance is common in patients with advanced cancer, and their family carers also may suffer from sleep problems. The aims of this study were to determine the prevalence of sleep-wake disturbances in patients with advanced cancer and their carers, to monitor the amount of daytime spent in activity and rest, and to examine the relationship between sleep, physical, and psychological symptoms. This was a prospective, descriptive observational study in patients with advanced incurable cancer and their carers attending a regional cancer center, using subjective (Short Form-36, Epworth Sleepiness Score, Hospital Anxiety and Depression Scale, Memorial Symptom Assessment Scale, and sleep history and diary) and objective (Actiwatch) assessments over a seven-day period. Sixty patients with advanced cancer and their family carers completed the study. Poor sleep was a frequent complaint: 47% of the patients and 42% of the carers reported that they did not sleep well, yet patients reported sleeping an average of 8.2hours and carers 7.8hours per night. The objective assessments revealed that although sleep efficiency (SE) was greater than 90% for most patients and carers, sleep fragmentation was high in both groups. Patients and carers who complained of poor sleep were significantly more anxious (P<0.001 and <0.05) compared with patients and carers who reported sleeping well. Patients who complained of poor sleep had significantly more pain (P<0.05). These results show that a substantial proportion of advanced cancer patients and their carers complained of poor sleep despite reporting “normal” duration of sleep. Objective measurements using Actiwatch revealed good SE but high levels of sleep fragmentation and movement, suggesting that sleep quality may be disturbed. Further work is required to investigate sleep quality and the consequences of poor sleep. In the meantime, health care professionals need to routinely inquire about sleep and consider possible reversible underlying factors, such as pain and anxiety, for those who report sleep disturbance.

Key Words: Sleep-wake disturbances, insomnia, advanced cancer, family carers, nonprofessional carers, sleep

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Introduction 

Restorative sleep is a fundamental and an essential component of daily life. Sleep disturbance from whatever cause can result in numerous physical and mental effects on individuals, as well as an inability to take pleasure from work or social activities. This can lead to a rapid decline in quality of life, with an impact on an individual's ability to function and gain satisfaction in living.¹

Sleep-wake disturbances are common in patients with cancer², ³, ⁴, ⁵, ⁶ and can be disturbing.⁷ Sleep is not routinely assessed by health care professionals in clinical practice⁸ and patients are unlikely to volunteer information about this symptom;⁹ it is, therefore, often neglected.⁸ Despite being reported as a main concern for patients,⁵, ¹⁰ sleep-wake disturbances are poorly understood in patients with advanced cancer.², ⁶ Sleep-wake disturbances have been associated with a decline in cognitive, psychological, and physical function, as well as the ability to take pleasure in daily activities,³, ⁶, ¹¹ but very few studies have investigated this process in patients with advanced cancer.

There has been a general shift to outpatient care and care at home, which has moved some of the responsibility of care from health care professionals to nonprofessional carers. Many patients with advanced cancer are cared for by their families, which help with physical, psychological, social, and financial needs. It is recognized that caring for someone with a chronic illness has an impact on the carers’ overall health and well-being,¹², ¹³, ¹⁴ and several authors have reported that family carers of patients with advanced cancer may suffer from sleep-wake disturbances.⁴, ¹³, ¹⁵ The needs of these carers should be considered as they can sometimes be ignored (by carers and health care professionals) because the focus of care is usually on the patient. If their needs are not assessed, it is unlikely that they will be able to perform their role as a carer. Chronic sleep deprivation among carers also can lead to longer-term problems.

Very few studies have investigated sleep-wake disturbances in carers of patients with advanced cancer,¹⁵ and this symptom is, therefore, poorly understood in these individuals.

The aims of this study were to use subjective and objective assessments to determine the prevalence of sleep-wake disturbances in patients with advanced cancer and their carers, to determine the amount of daytime spent in activity and rest, and to examine the relationship between sleep disturbances, physical and psychological symptoms, and quality of life in these patients and their carers.

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Methods 

This was a prospective, observational, descriptive study comparing sleep in a sample of patients with advanced incurable cancer and their carers attending a regional cancer center in the United Kingdom. Over a 15-month period, notes of patients attending oncology clinics were screened to determine whether they met the inclusion criteria: a diagnosis of incurable cancer and living with a nonprofessional carer. The exclusion criteria included the following: an estimated prognosis of less than one month, cognitive impairment, impaired use of the nondominant arm, and receiving chemotherapy or radiotherapy within the past two weeks. If the inclusion/exclusion criteria were met, the patient and carer were given an information leaflet by the clinic nurse and invited to take part in the study. The local research ethics committee approved the study.

Following written consent from the patient and carer, demographic data were collected and a standardized sleep history was taken to reflect questions that would be asked in usual clinical practice (Fig. 1) because no single-item screening tool has been established for insomnia in patients with cancer.¹⁶ Patients and caregivers were asked to wear an Actiwatch for seven consecutive days on their nondominant wrist, which has been validated in several populations to provide an objective measurement of sleep efficiency (SE), daytime activity, and daytime sleeping.¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹ This device (model AW4; Cambridge Neurotechnology, Cambridge, United Kingdom), which looks like an ordinary wristwatch, contains a miniature uniaxial accelerometer that produces a signal as the wearer makes physical movement, with a sensitivity of 0.01g or more. The signal was measured 32 times/second and processed to provide the digital integration of the amount and duration of movement. Each device was set to an epoch length of 15 seconds, permitting a period of up to 11.5 days of data recording. The sensitivity setting used for all measurements was medium. The data were stored within the Actiwatch in nonvolatile memory for subsequent analysis. Participants were asked to complete a daily sleep diary (Figure 2).

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• Fig. 1 

  Sleep history questions.

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• Fig. 2 

  Sleep diary.

Once the study period was completed, the data were downloaded and analyzed using the manufacturer’s supplied software (Actiwatch Activity and Sleep Analysis 5, version 5.32, Cambridge Neurotechnology). For all data analysis, the software uses automated analysis, with the user setting the start time and the end time of the analysis. The software assigns an epoch of either wake or sleep. Analysis of the sleep period included the following: 1) the total sleep time (TST), defined as the time elapsed from the set sleep start (nighttime bedtime) to the sleep end (morning wake up); 2) the total nighttime sleep period or the sum of all sleep epochs within the interval between these two set times; 3) SE, calculated as the ratio of total nighttime sleep duration to the total sleep period; 4) wake after sleep onset, measured as the sum of all wake epochs during the sleep period (reflecting the number of minutes that exceeded the sensitivity threshold and were scored as wake); and 5) the movement and fragmentation index (MFI), calculated as the sum of the percent of mobile minutes plus the percent of immobile bouts less than one minute duration divided by the number of immobile bouts for a given interval. The MFI captures all movements regardless of the intensity of the movement. Daytime activity was obtained with the time markers set from morning wake-up time to the next nighttime bedtime period, and the automated analysis of activity was obtained. The nap analysis (the sum of all sleep epochs within the interval between the time set) was used to calculate the number of naps within the daytime period and their duration. A nap was defined as a period of inactivity between 5 and 15minutes.

At the end of the seven-day period, patients and their carers both independently completed four validated questionnaires in their own home:

Data were analyzed using GraphPad Prism (v5, 2007). Demographic statistics are reported using mean and standard deviations for parametric data, and median and range for nonparametric data. Demographic characteristics and data from the questionnaires of both patients and caregivers were compared using either the Wilcoxon signed rank test or the unpaired t-tests. The Actigraph data were analyzed over the seven-day period with completed data sets for both the patients and the carers. Data were obtained from the Actigraph analysis software as previously outlined. To compare data over the seven consecutive days in either patients or carers alone, one-way analysis of variance (ANOVA) was used with Bonferroni's multiple comparisons test to determine where significant differences were occurring. This was only used where a significant difference was obtained. To compare data over the seven days between the patients and the carers, two-way ANOVA was used with Bonferroni's multiple comparisons test.

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Results 

Over a 15-month period, 2974 sets of patients' notes were screened, yielding 190 patients who met the inclusion criteria. Of these, 55 patient-carer couples were ineligible (18 couples slept in different rooms, 10 were starting chemotherapy/radiotherapy, eight had no partner, six had distressing news from clinic, seven lived apart for some of the week, two were unable to wear an Actiwatch, two were admitted to hospital, one patient had narcolepsy, and one was unable to read and write) and 73 patient-carer couples did not want to take part (51 no reason given, 6 felt too unwell, nine felt too busy, six were taking part in another trial, and in one, the family did not feel the patient and carer would cope). Sixty-two patients and their carers enrolled in the study, but two couples withdrew: one patient was hospitalized for stroke and one couple did not complete the sleep diary or questionnaires (Fig. 2).

Subjective Data: Sleep History, Sleep Diary, and Validated Tools 

When asked directly, 47% of the patients and 42% of the carers reported that they did not sleep well. Of the patients who reported not sleeping well, 25% stated that they had sleep problems before their cancer diagnosis only, 29% reported sleep disturbance since their cancer diagnosis, and 29% reported a combination of both (data not available for five patients). Of those carers who reported not sleeping well, 12% stated that they had sleep problems before the patient's cancer diagnosis only, 36% reported sleep disturbance since their partner was diagnosed with cancer, and 36% reported a combination of both (data not available for four carers). In 19 (32%) pairs, both the patient and the carer reported that they slept well; in 14 (23%) pairs, both reported they did not sleep well; and in 27 (45%) pairs, either the patient or the carer reported not sleeping well. Characteristics of patients and carers are shown in Table 1.

Table 1. Characteristics of Patients and Carers

	Patient	Carer
Male:female	27:33	33:27
Age in years, median (range)	67 (32–80)	66 (27–80)
Cancer
Lung	20	n/a
Breast	20
Colorectal	6
Prostate	14
ECOG score
0	16	n/a
1	27
2	14
3	3
4	0

ECOG = Eastern Cooperative Oncology Group; n/a = not applicable.

Patients reported sleeping an average of 8.2hours per night and carers 7.8hours per night. Nearly half of all the patients and carers reported difficulty getting off to sleep, and waking up in the middle of the night was a frequent occurrence (85% of the patients and 90% of the carers). For patients, the main reasons for waking during the night were going to the toilet (67%) and pain (27%). For carers, going to the toilet (42%), being disturbed by the patient (28%), and worry (26%) were the most commonly reported reasons. Vivid dreams were common to both groups but few had nightmares. Although many patients and carers reported not sleeping well, only a small proportion took medications to help them sleep. The summary of the sleep history and diary data is provided in Table 2.

Table 2. Summary of Sleep Diary and History Questionnaire

n/a = not applicable.

ESS, HADS, SF-36, and MSAS data are summarized in Table 3. The ESS showed that patients reported significantly greater daytime sleepiness than carers (P<0.005), with 26% of the patients and 15% of the carers having scores greater than 10. The SF-36 scores showed that patients had significantly lower scores in six of the eight domains (P<0.0001), particularly in those related to physical functioning whereas mental health, role emotional, and mental scores were not significantly different between the patients and the carers. Vitality, general health, physical, and mental scores were generally low for both groups.

Table 3. Summary of Questionnaires

	Patient, Median (range)	Carer, Median (range)	P
ESS	8.0 (1–24)	5.0 (0–13)	<0.005
HADS
Depression	4.5 (0–15)	4.0 (0–16)	NS
Anxiety	7.0 (0–19)	7.0 (0–19)	NS
Total score	11.0 (1–33)	11.0 (7–35)	NS
SF-36
Vitality	40.5 (0–85)	51 (5–95)	<0.0001
Body pain	29.0 (0–84)	72.0 (10–90)	<0.0001
Physical functioning	35.0 (0–100)	87.5 (0–100)	<0.0001
Role physical	0 (0–100)	100 (0–100)	<0.0001
General health	35.0 (0–85)	65 (5–100)	<0.0001
Social functioning	50 (0–100)	87.5 (0–100)	<0.0001
Physical scores	23.6 (8.6–56.8)	49.5 (20.1–70.8)	<0.0001
Mental health	72 (8–96)	68 (20–96)	NS
Role emotional	100 (0–100)	100 (0–100)	NS
Mental scores	42.9 (6.0–69.9)	47.6 (11.9–73.5)	NS
MSAS
GDI	10.1 (1.6–35.8)	7.3 (0–29.7)	<0.005
PHYS	8.5 (0–27.9)	3.9 (0–18.9)	<0.0001
PSYCH	5.1 (0–28.5)	5.4 (0–18.5)	NS
Total score	24.7 (6.8–93.8)	16.9 (0–65.4)	<0.0001

NS = not significant.

Objective Data: Actiwatch 

The Actiwatch data are summarized in Table 4. SE was greater than 90% for most patients; seven (12%) patients and five (8.3%) carers had SE of less than 86% over the seven-night period (normal range 86%–100%). However, sleep fragmentation and movement were high in both groups, and patients had significantly higher degrees of sleep fragmentation than carers (P<0.05). Although large variations were observed, daytime activity levels were generally low for both patients and carers, with large periods of the day spent immobile (42%–48% of the day for patients and 28%–31% of the day for carers). Patients took between 14 and 17 naps a day lasting approximately nineminutes each. Carers took approximately nine naps a day lasting eightminutes each. Carers were therefore significantly more active (P<0.01), spent less of the day immobile (P<0.05), and took fewer naps than patients (P<0.01). Different cancer diagnoses did not significantly affect the subjective or objective data for the patients or their carers.

Table 4. Summary of Objective Actigraph Data (median [mean ± SD])

		Day 1	Day 2	Day 3	Day 4	Day 5	Day 6	Day 7	P(patient vs. carer)
SE (%)	Patient	91.3±4.5	91.1±4.3	90.7±5.0	90.7±4.5	90.2±6.4	90.5±6.8	90.7±5.4	NS
	Carer	91.3±4.3	91.7±4.7	90.1±5.9	90.8±5.0	90.5±6.1	91.9±4.8	91.2±4.8
Time awake (%)	Patient	8.9±1.3	8.9±1.2	9.1±1.2	8.9±1.1	8.9±1.4	8.8±1.7	8.8±1.7	NS
	Carer	9.0±5.0	8.6±4.6	9.3±5.9	9.2±5.1	9.4±5.5	8.3±4.8	9.2±5.1
Fragmentation and movement	Patient	43.6±19.6	45.2±18.9	42.5±16.7	45.7±17.1	44.9±19.2	44.3±20.8	42.4±17.1	<0.05
	Carer	36.8±18.5	36.0±18.8	39.6±21.2	37.6±16.5	41.4±20.7	35.4±19.2	38.5±17.8
Activity level (counts)	Patient	87.0±24.6	87.3±12.2	77.5±24.2	78.6±19.1	77.7±23.3	78.6±20.6	78.4±22.1	<0.01
	Carer	101.5±35.5	102.1±33.8	96.7±31.4	94.3±28.8	94.4±29.2	94.7±26.9	95.9±26.7
Time immobile (% daytime)	Patient	48.1 (9.1–63.6)	42.2 (13.5–64.7)	47.0 (11.7–70.0)	42.0 (12.2–68.0)	47.1 (8.5–61.9)	45.1 (10.4–72.8)	46.3 (13.4–65.2)	<0.05
	Carer	29.1 (5.9–57.1)	28.5 (7.1–53.3)	28.5 (6.7–58.9)	31.6 (6.2–54.9)	31.6 (7.8–64.3)	29.8 (10.6–58.7)	29.6 (6.9–69.3)
No. of naps	Patient	15 (1–39)	16 (2–42)	16 (1–43)	14 (3–38)	15 (2–37)	15 (0–50)	17 (0–41)	<0.01
	Carer	10 (0–35)	8 (1–33)	7 (0–40)	10 (1–43)	8 (1–55)	9 (0–35)	9 (1–31)
Length of naps (minutes)	Patient	9.2 (5.5–11.5)	8.7 (5.9 11.5)	9.1 (6.8–13.8)	9.0 (6.2–11.1)	8.8 (5.7–11.6)	9.0 (0–11.8)	8.9 (0–11.9)	NS
	Carer	9.6 (5.5–14.0)	8.5 (6.6–14.6)	7.8 (5.2–14.8)	9.0 (6.5–12.0)	9.1 (5.9–12.2)	8.5 (7.5–12.1)	9.8 (5.5–14.8)

NS = not significant.

Interrelationship of Subjective and Objective Data 

The interrelationships between subjective and objective data are summarized in Table 5. Comparison was made within the patient and the caregiver groups based on those who stated that they slept well (patients: n=32; carers: n=35) and those who stated they did not sleep well (patients: n=28, carers: n=25) on the history questionnaire.

Table 5. Summary of Objective and Subjective Data Interrelationships

NS = not significant.

There was no difference in objective SE, sleep fragmentation, or daytime activity comparing those patients and carers who reported that they slept well and those who reported not sleeping well. Patients who reported that they did not sleep well had significantly higher anxiety (HADS, P<0.005) and increased body pain (SF-36 body pain, P<0.05) compared with those patients who reported sleeping well, and carers who reported sleeping well were significantly less anxious (HADS, P<0.01) and had less global distress (MSAS-GDI, P<0.01) and psychological symptoms (MSAS-PSYCH, P<0.001) compared with those carers who reported sleeping well.

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Discussion 

This is the first study to simultaneously obtain subjective and objective data on patients with advanced cancer and their nonprofessional carers for sleep, daytime activity, and quality of life. Poor sleep was a frequent complaint in patients with advanced cancer and their carers; 47% of the patients and 41% of the carers reported that they did not sleep well. A large study of patients with advanced cancer has reported a subjective prevalence of 49% for sleep problems,²⁶ and 36%–95% of carers of patients with cancer (not necessarily advanced cancer) have reported sleep problems in the form of daytime dysfunction and sleep quality and duration.¹⁴, ¹⁵, ²⁷

For some patients and carers, sleep problems appeared to exist before the diagnosis of cancer, but for many, the cancer diagnosis either caused or added to their sleep problem. Literature about this finding is scarce; of those who met the specific criteria for “insomnia” in a cohort of 300 patients with nonmetastatic breast cancer, one in three of them described the onset of sleep problems as occurring after the diagnosis of cancer.²⁸ In this study, we did not find any difference in sleep between different cancers; other studies have shown no difference between different cancers,², ⁶, ²⁹ whereas some have reported differences between patients with breast and lung cancer.⁷

Despite a large proportion of the patients and carers complaining that they did not sleep well, both groups reported sleeping an average of eighthours per night. There was no significant difference in the number of hours slept by those who reported sleeping well and those reporting poor sleep. This suggests an appropriate duration of sleep time, yet, patients and carers commonly reported problems with getting off to sleep and waking up in the middle of the night. This was reflected in the Actiwatch data; although SE was good, there were high levels of sleep fragmentation and movement in patients and carers, suggesting disturbed sleep, which may be an indication of poor sleep quality. This may indicate that those patients who complained of not sleeping well despite an average of eighthours sleep per night did not have restorative sleep during the time that they reported being asleep. Further studies exploring sleep quality are needed.

Patients who reported sleeping well had significantly less anxiety (HAD) and less body pain (SF-36 body pain), compared with those who reported sleeping difficulties. This finding is consistent with other studies that suggest that pain³, ⁵, ⁶, ¹³, ²⁹, ³⁰ and anxiety⁵, ⁷, ²⁸, ³⁰ play a role in sleep disturbance or vice versa. Likewise, carers who reported sleeping well were significantly less anxious (HADS) and had less global distress (MSAS-GDI) and psychological symptoms (MSAS-PSYCH) as compared with those carers who reported not sleeping well. Patients reported significantly higher daytime sleepiness (ESS) than carers, which is in keeping with other papers studying patients with cancer and controls.³¹, ³²

It is recognized that caring for someone with a chronic illness has an impact on carers' overall health and well-being,¹² but the impact of sleep disturbance on the health and quality of life of carers has not been well documented. Although median objective SEs were greater than 90%, 46% of carers had SE of less than 90%. Sleep fragmentation was also high in many carers, and as an outcome of this sleep disruption, carers were observed to take naps in the daytime. These findings concur with published data in that caregivers appear to have significantly disturbed sleep, which impacts on their daytime function.¹⁴, ¹⁵, ³³ Carers took significantly fewer naps and were significantly more active, regardless of how they reported that they slept compared with patients. Carers appear to prioritize the care of the patient, resulting in a reduction in their own quality of life and self-care. Perhaps carers neglect their need for sleep despite its importance in maintaining their emotional, physical, and mental strength. In a study of 51 carers of patients with advanced cancer, it was found that despite scores indicative of sleep disturbance, carers were reluctant to take hypnotics to improve their sleep because of caregiving duties.³³

Interestingly, there was no difference in SE, sleep fragmentation, or daytime activity when comparing those patients and carers who reported that they slept well and those who did not. However, Actiwatch works by detecting movement and it may be unable to differentiate between a patient who is asleep and a patient who is awake but not moving. It is, therefore, likely to overestimate levels of SE.¹⁹, ³⁴, ³⁵ This study shows that sleep fragmentation may be common in patients and carers, which suggests disturbed sleep. However, Actiwatch does not provide an objective measure of sleep quality. Thus, we have not been able to corroborate the patients’ and carers’ subjective assessment of their sleep.

Patients are notoriously bad at estimating the duration of sleep and wakefulness, particularly when they have a problem with sleep. It is particularly important to have objective measures to properly evaluate this symptom, but these measures need to be sensitive, specific, and validated in the patient population being investigated. Actiwatch has limitations, as discussed previously, and further studies using ambulatory polysomnography will need to be the next step. Work is required to investigate the consequences of poor sleep for patients and carers and to use objective measures of sleep quality that are practical and appropriate for patients with advanced cancer. Although the overall agreement rates between actigraphy and polysomnography for sleep and wakefulness in normal individuals have been very high, the accuracy declines as the quality and quantity of sleep diminishes.¹⁹, ³⁴, ³⁶ When compared with full polysomnography, Actiwatch has been found to overestimate TST and SE,¹⁹, ³⁴ and has a low ability to pick up wakefulness in sleep-disordered individuals.³⁴ The development of sophisticated ambulatory devices that will record both quantity and quality of sleep are now available. But one drawback of such devices is that the data capture may be possible only over shorter periods of time.², ³⁵

Clinical research in patients with advanced cancer is associated with particular difficulties in regard to recruitment and accrual of patients, attrition, and outcome measures. This study demonstrated the considerable effort required to recruit an adequate number of patients. To enroll 60 patients and their carers, it was necessary to screen the case records of 2974 patients—a ratio of 50 to 1. This is an important consideration in planning future studies.

Limitations 

Actiwatch has not been used before in an advanced cancer patient population to investigate potential sleep problems using objective measures. We chose to use it because it is a cheap, easy-to-use, noninvasive tool that can be used in the home environment, with minimal disruption to the patient or other individuals. However, in this study, it has not corroborated the evidence from the patient and carer history and diary cards, in that it has demonstrated no difference between patients who slept well and patients who had disturbed sleep.

There is currently no valid instrument to measure the sleep-wake, so we used the best-available tools. Likewise, there is no single question that allows us to determine if patients are sleeping well or not. Therefore, we used a question that is used in clinical practice, “Do you usually sleep well?”, as the patients' and carers' perception of their sleep is important. Until research in this area improves, this study provides some meaningful clinical results.

We did not ask patients and carers about comorbidities, but these may play an important role in sleep disturbance. Alongside future quantitative work, qualitative studies are needed to explore the nature and impact of sleep disturbances in patients with advanced cancer and their carers.

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Conclusions 

A substantial proportion of this sample of advanced cancer patients and their carers complained of poor sleep despite reporting “normal” duration of sleep. Objective measurements using Actiwatch revealed good SE, but high levels of sleep fragmentation and movement suggesting that sleep quality may be disturbed. There was no difference between patients and carers who reported that they had poor sleep and those who said they slept well, in objective measures of SE, sleep fragmentation, and daytime activity. Further work is required to investigate the consequences of poor sleep for patients and carers and to use objective measures of sleep quality that can be easily used for patients with advanced cancer.

In the meantime, health care professionals need to openly address this symptom for patients and their carers and explore potentially reversible causes, especially anxiety and pain, in those patients and carers who report sleep disturbance.

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Acknowledgments 

The authors thank the patients and carers who took part in this study, especially as many of the patients were in their final stages of their illness, both for wearing the Actiwatch and for taking time to complete the sleep diaries and questionnaires.

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