November 2005, Volume 32, Number 6

Online Exclusive
Sleep/Wake Disturbances in People With Cancer and Their Caregivers: State of the Science
Ann M. Berger, PhD, RN, AOCN^®, Kathy P. Parker, PhD, RN, FAAN, Stacey Young-McCaughan, PhD, RN, AOCN^®, Gail A. Mallory, PhD, RN, CNAA, Andrea M. Barsevick, RN, DNSc, AOCN^®, Susan L. Beck, PhD, APRN, FAAN, AOCN^®, Janet S. Carpenter, PhD, RN, Patricia A. Carter, PhD, RN, CNS, Lynne A. Farr, PhD, Pamela S. Hinds, PhD, RN, Kathryn A. Lee, RN, PhD, FAAN, Christine Miaskowski, RN, PhD, FAAN, Victoria Mock, DNSc, FAAN, Judith K. Payne, PhD, RN, AOCN^®, and Martica Hall, PhD

Abstract

Data Sources: Published articles, books and book chapters, conference proceedings, and MEDLINE^®, the Cumulative Index to Nursing and Allied Health Literature^®, PsycINFO, and the Cochrane Library computerized databases.

Data Synthesis: Scientists have initiated studies on the prevalence of sleep/wake disturbances and the etiology of sleep disturbances specific to cancer. Measurement has been limited by lack of clear definitions of sleep/wake variables, use of a variety of instruments, and inconsistent reporting of sleep parameters. Findings related to use of nonpharmacologic interventions were limited to 20 studies, and the quality of the evidence remains poor. Few pharmacologic approaches have been studied, and evidence for use of herbal and complementary supplements is almost nonexistent.

Conclusions: Current knowledge indicates that sleep/wake disturbances are prevalent in cancer populations. Few instruments have been validated in this population. Nonpharmacologic interventions show positive outcomes, but design issues and small samples limit generalizability. Little is known regarding use of pharmacologic and herbal and complementary supplements and potential adverse outcomes or interactions with cancer therapies.

Implications for Nursing: All patients and caregivers need initial and ongoing screening for sleep/wake disturbances. When disturbed sleep/wakefulness is evident, further assessment and treatment are warranted. Nursing educational programs should include content regarding healthy and disrupted sleep/wake patterns. Research on sleep/wake disturbances in people with cancer should have high priority.

Key Points

• Sleep/wake disturbances in people with cancer and their caregivers can occur alone or as part of symptom clusters but have received little attention from healthcare providers.
• Several models offer approaches to examine the numerous factors that may underlie sleep/wake disturbances in people with cancer and their caregivers.
• A need exists to screen and assess sleep and wakefulness and to establish evidence for the reliability and validity of instruments used in this population.
• Randomized clinical trials to test interventions to promote sleep in this population are needed, but nonpharmacologic approaches found to be effective in people with insomnia can be included in patient-teaching materials.
• Future directions for research on sleep/wake disturbances have been identified and are ready for study.

Despite the evidence suggesting that sleep/wake disturbances, particularly insomnia, are among the most common complaints of people with cancer, sleep problems have received little attention from healthcare providers (Savard & Morin, 2001). Data suggest that patients with cancer have twice the prevalence of sleep problems as that reported in the general population (Savard, Laroche, Simard, Ivers, & Morin, 2003), with the majority of people reporting maintenance insomnia with several awakenings during the night (Davidson, MacLean, Brundage, & Schulze, 2002; Lee, 2003). Insomnia is associated with increased rates of medical and psychiatric illnesses and decreased quality of life (QOL) in the general population (Sateia & Pigeon, 2004). The disturbances compound the many challenges faced by people with cancer. The much-needed research on sleep/wake disturbances in people with cancer needs to build on the extensive body of knowledge that exists regarding sleep/wake disturbances in the general population and specific sleep disorders such as sleep apnea, periodic leg movement syndrome, restless leg syndrome, narcolepsy, and insomnia.

This article summarizes participants’ contributions to the Oncology Nursing Society (ONS) State-of-the-Science Conference on Sleep/Wake Disturbances in People With Cancer and Their Caregivers, which was held at ONS headquarters in Pittsburgh, PA, July 15–17, 2004. This article presents the state of the science on sleep/wake disturbances in people with cancer and their caregivers. It is divided into four main sections: sleep/wake disturbances in people with cancer, measurement of sleep/wake disturbances, nonpharmacologic and pharmacologic interventions, and implications for practice, education, and research. This article lays the foundation for directing increased attention to sleep/wake disturbances in clinical, educational, and research environments. As a result, the authors anticipate that patients with cancer and their caregivers will experience improved assessment and treatment.

Sleep/Wake Disturbances in People With Cancer

Adults and children report that sleep/wake disturbances occur during all phases of cancer care (Clark, Cunningham, McMillan, Vena, & Parker, 2004; Gibson, Garnett, Richardson, Edwards, & Sepion, 2005; Hockenberry-Eaton et al., 1998; Vena, Parker, Cunningham, Clark, & McMillan, 2004). They occur before treatment has begun (Ancoli-Israel, Moore, & Jones, 2001) and often seem to be directly related to the cancer diagnosis (Lee, Cho, Miaskowski, & Dodd, 2004; Savard, Simard, Blanchet, Ivers, & Morin, 2001).

The sleep of caregivers, who often are family members, also is disrupted. Problems with insomnia, other nocturnal sleep disturbances, and daytime fatigue are common among caregivers of people with cancer and other chronic illnesses (Carter, 2003; Carter & Chang, 2000; Hinds et al., 1999; Jepson, McCorkle, Adler, Nuamah, & Lusk, 1999; Kozachik et al., 2001; McGrath, Paton, & Huff, 2004; Nijboer et al., 2000; Nijboer, Triemstra, Tempelaar, Sanderman, & van den Bos, 1999). Reactive depression is very prevalent and can interfere with daily function, QOL, and ability to continue to provide care (Jepson et al.; Kozachik et al.; Nijboer et al., 1999, 2000). Only recently has chronic sleep loss related to stress and the 24-hour-per-day demands of caregiving been described as a significant problem (Carter & Chang). In addition, caregivers may be at risk for sleep problems after the loss of a loved one. A recent study demonstrated that the risk for long-term psychological morbidity, including sleep/wake disturbances, in a surviving partner significantly increased if a patient’s symptoms were unrelieved during the last three months of life (Valdimarsdottir, Helgason, Furst, Adolfsson, & Steineck, 2004).

Many nurses are aware that people with cancer have problems getting a good night’s sleep but do not realize the effects that poor sleep can have on daytime wakefulness, functional ability, and QOL (Vena et al., 2004). Furthermore, the assessment of sleep/wake disturbances and treatment of problems have not been integrated into routine clinical practice (Savard & Morin, 2001; Sherman et al., 2004). Barriers to integration of current knowledge about sleep are similar to those that commonly occur when working to translate knowledge of pain. The barriers occur at the level of patients, families, care providers, and healthcare systems. Nonetheless, as part of a comprehensive care plan, nurses should assess the sleep needs of patients and caregivers regularly and tailor interventions to meet their needs (Steele & Fitch, 1996). Sleep/wake disturbances increasingly are recognized as significant side effects of cancer treatment that affect physiologic as well as psychological function. In fact, the U.S. Department of Health and Human Services, the National Institutes of Health, and the National Heart, Lung, and Blood Institute (2003); the Institute of Medicine (2005); and ONS (2003) have identified sleep disturbances as a priority research area.

Sleep/Wake-Related Terminology

Recently, an increasing number of descriptive studies have included one or more sleep variables or terms indicating sleep/wake disturbances in some context in people with cancer. Unfortunately, the lack of consistency in terminology makes it difficult to compare and contrast studies and optimally evaluate their quality. Therefore, the authors recommend that, when possible, the terminology employed by the American Academy of Sleep Medicine (AASM) in the International Classification of Sleep Disorders (AASM, 2005) be used to provide consistency (Clark et al., 2004). For example, a primary sleep disorder is a specific diagnostic entity that includes a wide array of problems characterized by the symptoms of insomnia, excessive daytime sleepiness, or abnormal movements, behaviors, or sensations during sleep. Eight groups of sleep disorders are described by AASM.

• Insomnias: disorders that produce repeated difficulty with sleep initiation, duration, consolidation, or quality that occurs despite adequate time and opportunity for sleep and results in some form of daytime impairment
• Sleep-related breathing disorders: characterized by disordered respiration during sleep
• Hypersomnias of central origin: characterized by the primary complaint of daytime sleepiness not related to circadian rhythm sleep disorders, sleep-related breathing disorders, or other causes of disturbed nocturnal sleep
• Circadian rhythm sleep disorders: recurrent or chronic patterns of sleep disturbance resulting from alterations of the circadian timing system or misalignment between an individual’s rhythm and the 24-hour social and physical environments
• Parasomnias: undesirable physical events or experiences that occur during entry into sleep, within sleep, or during arousal from sleep
• Sleep-related movement disorders: conditions that are characterized primarily by relatively simple, usually stereotyped movements that disturb sleep (e.g., periodic limb movements)
• Isolated symptoms, apparently normal variants, and unresolved issues: symptoms that either lie at the borderline between normal and abnormal sleep or that exist on a continuum of normal to abnormal events in sleep (e.g., snoring)
• Other sleep disorders: disorders that cannot be classified elsewhere (e.g., other physiologic [organic] sleep disorders)

In contrast, terms such as sleep/wake disturbances, sleep problems, alterations in sleep, or impaired sleep are more general terms and often are used to describe complaints, symptoms, or groups of symptoms experienced by individuals. They are not diagnostic entities as defined by the AASM and often are used when a specific diagnosis has not or cannot be made. Nonetheless, two of the most common complaints or symptoms experienced by the general public that are defined in the International Classification of Sleep Disorders are insomnia and excessive daytime sleepiness. Insomnia may be a primary sleep disorder or a symptom of one of many other sleep disorders, such as sleep-related breathing disorders. Daytime sleepiness is defined as the inability to stay awake and alert during the major waking episodes of the day, resulting in unintended lapses into drowsiness or sleep; it also may be seen in a wide range of sleep disorders. Thus, understanding the causes of insomnia and excessive daytime sleepiness is essential to providing effective interventions. Numerous additional sleep-related terms can help characterize sleep/wake disturbances, including total sleep time, sleep latency, awakenings during sleep, and wake after sleep onset.

Understanding Sleep/Wake Disturbances in People With Cancer and Their Caregivers

Most organisms, including humans, exhibit a daily rest/activity (sleep/wake) pattern. The pattern is a functional property of all living matter, including humans, and is controlled by two primary factors: the amount, timing, and placement of sleep across the day (i.e., sleep homeostasis) and the underlying intrinsic circadian rhythm (Lazuna & Farr, 2003). The role of homeostatic factors and circadian rhythm in sleep regulation is best understood when sleep is examined as a physiologic as well as a behavioral process controlled by a system based in the brain and central nervous system. The sleep-regulation system provides an engine that drives sleep and wakefulness.

One model commonly used to help understand sleep is the Two-Process Model of Sleep Regulation (see Figure 1) (Achermann & Borbely, 2003; Borbely, 1982). According to the Two-Process Model, sleep begins (sleep onset) when the homeostatic (somnostat) component or need to sleep (Process S) is high. The need to sleep (Process S) increases as the time of prior wakefulness increases. The process of sleep onset also is modulated by the sympathetic nervous system (Lichstein, Wilson, Noe, Aguillard, & Bellur, 1994; Lushington, Dawson, & Lack, 2000; Vgontzas et al., 1998) and by the hypothalamic-pituitary-adrenal (HPA) axis (Vgontzas et al.). Increased activation of the sympathetic nervous system and the HPA axis can elevate arousal levels and delay the onset of sleep. Input from the systems is filtered out by the thalamus as sleep occurs, a process that must be filtered continually to maintain uninterrupted sleep.

In addition to Process S, there is Process C, the circadian process. The circadian oscillator resides in the suprachiasmatic nuclei, where rhythms are generated and synchronized with the environment by light and dark cues from the retina of the eye. Additional timing modifications are provided by interaction with the paraventricular nuclei and the ventromedial hypothalamus. Marker rhythms of the circadian oscillator are the core temperature rhythm and the rhythmic secretion of the hormone melatonin. At sleep onset, sleep initiation is most likely to occur during the falling phase of the endogenous component of the temperature rhythm (Strogatz, Knonaur, & Czeisler, 1986; Zulley, Weaver, & Aschoff, 1981). This occurs approximately five to six hours before the daily body temperature minimum is at its lowest point and one to two hours after the evening rise in plasma melatonin levels (Duffy, Dijk, Klerman, & Czeisler, 1998). Timing of the circadian component is adjusted by melatonin secreted from the pineal gland during the dark and inhibited by light exposure (Claustrate, Brun, & Chazot, 2005). Circadian timing also is adjusted by levels of plasma and central nervous system neurotransmitters and neuroendocrine factors such as gamma-amino-butyric acid; dopamine; growth hormone releasing hormone; prostaglandins D2, E2, and F2a; vasoactive inhibitory peptide; and growth hormone (Harrington & Mistlberger, 2003; Kunz & Achermann, 2003; Lazuna & Farr, 2003; Mignot, Taheri, & Nishino, 2002; Obal & Krueger, 2004; Ouyang, Hellman, Abel, & Thomas, 2004; Pace-Schott & Hobson, 2002).

Final awakening typically occurs when body temperature is rising (approximately one to two hours after the minimum temperature of the endogenous circadian rhythm) and sleep pressure (Process S) has decreased (Czeisler & Dijk, 2001). Therefore, the result is that sleep is regulated and sleep consolidation is achieved by an interaction between the circadian oscillator (Process C) and the homeostatic somnostat (Process S) (Czeisler & Dijk). The two processes appear to interact continuously throughout the day to drive physiologic and psychophysiologic variables (Borbely, Dijk, Acherman, & Tobler, 2001). Thus, the coordination between the two dynamic processes modulates the onset and offset of sleep as well as the rhythms of sleep propensity, wake propensity, and the degree of daytime alertness (Czeisler & Dijk; Dijk & Czeisler, 1994, 1995). In addition to the two processes, numerous demographic, lifestyle and environmental, psychological, and disease- and treatment-related factors are likely to contribute to poor sleep and daytime sleepiness experienced by people with cancer and their caregivers (see Figure 2).

For people with cancer, altered physiology directly related to the disease may play a prominent role in disrupting sleep and circadian regulatory processes. For example, abnormalities in the circadian production of cortisol have been reported in patients with cancer (Mazzoccoli et al., 2003; Raida et al., 2002). An absent or blunted rhythm of melatonin secretion also has been noted in patients with lung or colorectal cancer (Bartsch & Bartsch, 1999; Khoory & Stemme, 1988; Viviani, Bidoli, Spinazze, Rovelli, & Lissoni, 1992). Changes over time in nighttime melatonin levels in patients with breast or ovarian cancer also have been reported (Payne, 2002). In addition, cancer cells produce and induce production of cytokines, substances that promote sleep (Ardestani, Inserra, Solkoff, & Watson, 1999). More detailed summaries have been published (Clark et al., 2004; Lee, Dantzer, et al., 2004; Lee, Landis, et al., 2004; Vena et al., 2004). Further research is needed to understand more fully the extent to which the pathophysiology of cancer affects sleep and wakefulness.

Other models derived from or related to the Two-Process Model of Sleep Regulation have been proposed and address sleep/wake disturbances or health outcomes. The Conceptual Model of Impaired Sleep (Lee, 2003) describes impaired sleep as being related primarily to either sleep deprivation or sleep disruption, both of which can lead to adverse health outcomes in physiologic, cognitive-behavioral, emotional, and social domains. The PPP Model (Spielman & Glovinksy, 2004) proposes three main categories affecting sleep, particularly insomnia: predisposing, precipitating, and perpetuating factors. Predisposing factors are the biologic, genetic, and demographic traits that increase a person’s risk and susceptibility to insomnia. Precipitating factors are situations and conditions that, although they may be temporary, actually trigger insomnia. Perpetuating factors are those that reinforce insomnia over longer periods of time. The Two-Process Model of Sleep Regulation, the Conceptual Model of Impaired Sleep, and the PPP Model offer various approaches to examining factors that may underlie sleep/wake disturbances in people with cancer and their caregivers. Use of a particular model is dependent on the focus of a specific research study.

Symptom Clusters

Clinical experience suggests that patients with cancer often present with multiple symptoms, which Dodd, Miaskowski, and Paul (2001) labeled a symptom cluster. Findings from several studies suggest that sleep disturbance may be part of a symptom cluster that includes pain, depression, and fatigue (Dodd et al.; Gift, Jablonski, Stommel, & Given, 2004; Gift, Stommel, Jablonski, & Given, 2003; Given et al., 2002; Given, Given, Azzouz, Kozachik, & Stommel, 2001). In most of the studies to date, the symptom cluster of pain, fatigue, and sleep disturbance was associated with poorer functional status or decreased QOL. The question of which comes first remains unknown.

Genetics and Sleep

Most sleep disturbances in healthy people result from complex interactions between an individual’s genes and his or her environment (Taheri, 2004). Modern techniques in molecular genetics are being used in insect and animal models to begin to elucidate the genetic basis for circadian rhythms and sleep disturbances. Studies in animals and humans have shown that the sleep/wake and circadian clock systems are linked closely with each other on the molecular and systems levels (Turek, 2004). An excellent review on the genetics of sleep disorders (Taheri) described studies in animals that are beginning to elucidate the molecular mechanisms that underlie narcolepsy, obstructive sleep apnea, and restless leg syndrome. At least 10 circadian clock core genes have been identified in mammals to date, including findings related to diurnal preferences (morningness and eveningness) (Archer et al., 2003). Undoubtedly, future studies will help to determine the molecular basis for sleep disturbances that occur in the context of other medical conditions such as cancer.

Measurement of Sleep/Wake Disturbances

Key Sleep Parameters

One of the major challenges facing sleep research is measurement. “Difficulty sleeping,” a term commonly used by patients, caregivers, and practitioners, can have very different meanings and causes. Symptoms of sleep/wake disturbances may include difficulty getting to sleep; difficulty staying asleep; restless sleep or the feeling that sleep is not refreshing; or sleepiness, the inability to stay awake when desired. In otherwise healthy populations, relatively little is known about the various manifestations of sleep disturbances and how they interact to result in a patient’s report of “difficulty sleeping.” In patients with cancer, particularly children, even less is known. Between one-third and three-quarters of adult patients with cancer experience difficulty sleeping (Andrykowski et al., 1997; Davidson et al., 2002; Engstrom, Strohl, Rose, Lewandowski, & Stefanek, 1999; Fortner, Stepanski, Wang, Kasprowicz, & Durrence, 2002; Miaskowski & Lee, 1999). Children with cancer and their caregivers or parents also report sleep disturbances, but the actual incidence of disturbed sleep in children is unknown (Ferrell, Rhiner, Shapiro, & Dierkes, 1994; Gedaly-Duff et al., 2002; Hockenberry-Eaton et al., 1998).

In each of the descriptive studies described in the earlier paragraph, different parameters were used to define difficulty sleeping. Daytime sleepiness that may be a result of nocturnal sleep difficulties has not been included in the studies yet, but it is an important component of poor sleep, as well as an indicator of poor QOL. As researchers and clinicians attempt to explore sleep quality and its importance to health, their efforts would be advanced significantly if consensus were achieved regarding which sleep parameters to measure and which measurement instruments to use in a standard fashion. Based on a review of the literature and consensus of the expert clinicians and researchers participating in the ONS State-of-the-Science Conference on Sleep/Wake Disturbances in People With Cancer and Their Caregivers, nine parameters of sleep disturbance are proposed to provide a common language of sleep disturbance for measurement of the problem in all studies involving adults and children with cancer as well as their caregivers. The parameters are total sleep time, sleep latency, awakenings, wake time after sleep onset, napping during the day, excessive daytime sleepiness, quality of perceived sleep, stability of circadian rhythms, and sleep efficiency (see Table 1). No single parameter is recommended because poor sleep cannot be captured in its totality by any one parameter. Instead, the nine parameters collectively describe the characteristics of a sleep/wake disturbance.

Table 1 includes clinical tools and research instruments to assess the nine sleep parameters. In addition to the few sleep tools or instruments that have been validated in patients with cancer (e.g., the Pittsburgh Sleep Quality Index [PSQI]), clinical tools and research instruments that have been used with other patient populations also have been included. Clinical tools were chosen based on their ease of use in busy clinical settings and the ability to modify therapy quickly based on findings. Research instruments were chosen based on what is known about reliability (precision), validity (accuracy), and sensitivity of the instruments in research settings (Beck, Schwartz, Towsley, Dudley, & Barsevick, 2004; Carpenter & Andrykowski, 1998).

Of note, the Clinical Sleep Assessment for Adults and the Clinical Sleep Assessment for Children were developed as brief assessments for sleep problems in clinical settings (see Figure 3) (Lee & Ward, 2005). The tools were derived from an extensive clinical assessment protocol called BEARS, an acronym that stands for bedtime issues, excessive daytime sleepiness, night awakenings, regularity and duration of sleep, and snoring (Owens & Dalzell, 2005). Both need extensive testing in clinical practice but are administered easily, can be scored for research purposes, and have excellent face validity. They are useful for obtaining a brief sleep history in inpatient and ambulatory care settings, as well as for identifying people in need of specific intervention strategies such as improvements in sleep hygiene, changes in lifestyle, or referrals to sleep disorder specialists. When time is limited, a subset of four of the seven questions can be used (see notes in Figure 3). Using the tools can facilitate a focused approach to understanding sleep disturbances, improving sleep, and maximizing QOL for all people with cancer during and after treatment.

As with any tool or instrument, each of the clinical tools and research instruments listed in Table 1 has limitations. Clinicians and researchers are urged to read more about a particular tool or instrument before using it in practice or research. Validation of clinical tools and research instruments in patients with cancer and their caregivers is highly encouraged.

Considerations for Assessment of Sleep

One consideration in the choice of a sleep measurement is the temporal nature of the sleep/wake cycle. The assessment of a biologic process that normally fluctuates in a circadian pattern is inherently challenging. Instruments that are easy to administer and interpret are needed to more fully appreciate the nature of sleep and sleep disturbance.

Although sleep/wake disturbances can be assessed subjectively and objectively, the subjective and objective measurements do not necessarily correlate (Berger & Johnson, 2004; Young-McCaughan et al., 2003). Certain research instruments, such as sleep diaries, assess individuals’ perceptions of problems falling asleep and sleep quality, whereas others, such as wrist actigraphy, assess actual physical movements during sleep-activity periods.

Valuable sleep information can be obtained from bed partners, parents of children, and caregivers. For example, the final section of the PSQI includes specific questions to be answered by bed partners, and the Clinical Sleep Assessment (Child) is completed by parents of young or otherwise nonverbal children. Understandably, sleep information obtained from bed partners or caregivers is affected by their own sleep patterns. Skilled clinicians are able to synthesize the data as treatments plans are developed in clinical settings; however, quantitative methods to handle the data should be developed for research purposes.

Time frame is an important consideration in the choice of a sleep measurement. For example, the two most frequently used measurements of daytime sleepiness are the Stanford Sleepiness Scale (Hoddes, Zarcone, & Dement, 1972) and the Epworth Sleepiness Scale (Johns, 1992), both self-report measurements. The Stanford Sleepiness Scale was developed to assess sleepiness several times throughout a day in conjunction with the multiple sleep onset latency test (a polysomnography study of daytime sleepiness) and can be performed on an hourly basis to examine change in sleepiness during the day as well as time of day when sleepiness is greatest. The Epworth Sleepiness Scale, on the other hand, asks about how likely it would be for a person to doze off in various activities that typically are performed over the course of a day (e.g., watching TV), week (e.g., as a passenger in a car), or month (e.g., attending the theater). Prospective measurements, such as a sleep diary or the Stanford Sleepiness Scale, and retrospective measurements, such as the Epworth Sleepiness Scale, have strengths and weaknesses related to reliability that clinicians and researchers need to consider when matching a research instrument to a specific research question or clinical concern.

Interventions

Nonpharmacologic

Since 1985, psychological and behavioral factors increasingly have been recognized as contributing to the development of insomnia. More than a dozen nonpharmacologic, cognitive, and behavioral interventions have been developed; however, the populations in which they have been tested have been otherwise healthy people with insomnia. Only discussion of interventions for insomnia in adults is possible because information is limited in regard to children. To identify commonly used nonpharmacologic interventions to promote sleep or prevent insomnia, a two-step search of the literature indexed was conducted using the major literature search engines (MEDLINE^®, Cumulative Index to Nursing and Allied Health Literature^®, and PsycINFO). Key words used for the primary search included sleep, sleep disturbance, intervention, and insomnia. From the findings, primary research, research summary, and meta-analysis articles were selected.

The secondary search of the literature was conducted using the names of the interventions used in the articles identified in the primary search (e.g., sleep restriction, sleep hygiene, relaxation therapy, massage, yoga). When possible, classic sources were identified and retrieved for each intervention and compared with recent sources to provide definitions, rationale, and recommendations or strategies for each intervention. The findings are summarized in Table 2. Although the authors recognize the limitations of the generalizability of the studies, the body of knowledge provides a foundation from which to generate knowledge of interventions that are effective in people with cancer and their caregivers.

Nonpharmacologic interventions to promote sleep and prevent or treat insomnia often were used as combination therapies (cognitive and behavioral therapies) depending on the needs or restrictions of the study populations. The use of different combinations of interventions may explain some of the differences across studies in terms of the recommendations or strategies suggested for implementation. However, definitions and rationales for the use of interventions were consistent across sources.

Meta-analyses of nonpharmacologic interventions for disturbances in sleep: To determine possible therapeutic modalities to improve sleep in people with cancer and their caregivers, a search was conducted for meta-analyses of nonpharmacologic cognitive and behavioral interventions for insomnia in noncancer populations. Searches of MEDLINE, CINAHL, PsycINFO, and the Cochrane Library from 1994–2004 were conducted using the key term sleep interventions and limit of meta-analysis. Five analyses were found that provided the state-of-the-science information on the effectiveness of nonpharmacologic interventions to improve sleep in presumably healthy noncancer populations (see Table 3). None of the reviews addressed insomnia interventions in populations with cancer.

The Cochrane Database has published highly controlled, systematic reviews on bright light therapy, physical exercise, and cognitive and behavioral interventions to improve sleep. Each systematic review includes information about the search strategy used. Cognitive and behavioral interventions are defined as treatments that aim to improve sleep by changing poor sleep habits and challenging negative thoughts, attitudes, and beliefs about sleep. The interventions include a broad range of treatments, from educational packages to those that employ behavioral strategies. Only cognitive and behavioral treatments provided level 1 (strongest) evidence of short-term effects in reducing sleep onset latency and wake after sleep onset; however, the treatment effects were not durable over time (Montgomery & Dennis, 2003). Two earlier meta-analyses (Morin, Culbert, & Schwartz, 1994; Murtagh & Greenwood, 1995) provided stronger evidence that nonpharmacologic interventions produced reliable and durable clinical benefits in reducing sleep onset latency and wake after sleep onset. Differences in the conclusions of the two earlier meta-analyses compared to a more recent report by Montgomery and Dennis (2003) may be attributed, in part, to more rigorous inclusion criteria that resulted in fewer studies being included in the recent analysis. Larger effects were found for people who were referred by clinicians and not regular users of hypnotics (Murtagh & Greenwood). Current reviews are limited by the lack of randomized, controlled trials of sleep in people with cancer and their caregivers. As evidence grows regarding the effects of interventions for insomnia and other sleep/wake disturbances in cancer and noncancer populations, additional meta-analyses are recommended.

Nonpharmacologic intervention studies of sleep/wake disturbances in patients with cancer: Clark et al. (2004) examined research published from 1980–2003 on sleep/wake disturbances in people with cancer. Fifty-two pieces of evidence, including descriptive and intervention studies, were used in the evidence tables and rated from level 1 (strongest) to level 3 (weakest) of evidence. Readers are encouraged to review the evidence tables to gain perspective on the state of the science.

From 2003–2004, an increasing volume of descriptive studies was published that included the variable of sleep in some context in patients with cancer. A search of MEDLINE, CINAHL, and PsycINFO was conducted to identify all nonpharmacologic intervention studies that examined sleep disturbance or sleep quality outcomes in adults with cancer; the search revealed 20 studies (as of March 2005) that met the criteria (see Table 4).

All of the interventions employed combinations of cognitive or behavioral techniques. The most commonly used intervention technique was training in relaxation strategies (Allison et al., 2004; Berger et al., 2002, 2003; Cannici, Malcolm, & Peek, 1983; Carlson, Speca, Patel, & Goodey, 2003, 2004; Davidson, Waisberg, Brundage, & MacLean, 2001; Simeit, Deck, & Conta-Marx, 2004). All of the studies reported improvement in or stability with some sleep parameters. Four studies tested the effect of mindfulness meditation techniques (Carlson et al., 2003, 2004; Cohen, Warneke, Fouladi, Rodriguez, & Chaoul-Reich, 2004; Shapiro, Bootzin, Figueredo, Lopez, & Schwartz, 2003) and reported similar improvements in some sleep parameters. Exercise was tested in three studies (Coleman et al., 2003; Mock et al., 2001; Young-McCaughan et al., 2003). Most of the interventions were conducted in three to eight sessions; exercise interventions (Mock et al.; Young-McCaughan et al.) and mindfulness stress reduction (Carlson et al., 2003, 2004) included practice two to seven times per week. The individualized sleep-promotion plan (Berger et al., 2002, 2003) was reinforced and revised every 21–30 days.

Notwithstanding the positive findings of most of the cited studies, the quality of the evidence in support of cognitive and behavioral interventions for sleep was generally consistent but lacking in randomized multienter trials with at least 100 participants (Hadorn, Baker, Hodges, & Hicks, 1996). Only six of the 20 studies used randomized clinical trial designs (Cannici et al., 1983; Coleman et al., 2003; Dalton, Keefe, Carlson, & Youngblood, 2004; de Moor et al., 2002; Kim, Roscoe, & Morrow, 2002; Shapiro et al., 2003); four used quasiexperimental designs (Cohen et al., 2004; Mock et al., 2001; Simeit et al., 2004; Smith, Kemp, Hemphill, & Vojir, 2002). Only three studies had sample sizes greater than 100 participants (Dalton et al., 2004; Kim et al.; Simeit et al.), a criterion for the strongest level of evidence (Hadorn et al.; Ropka & Spencer-Cisek, 2001). Because combinations of intervention strategies were used, specifying the essential elements that accounted for the success of a given intervention is difficult. Future studies need to disentangle such issues by statistical methods before conclusions can be drawn about the most effective interventions to improve sleep in patients with cancer. The studies also were limited by a lack of clear definition of terms regarding sleep or use of measurements that may contain only a single-item rating of sleep.

Pharmacologic

Numerous pharmacologic approaches can be used to enhance sleep. Few of the approaches have been studied in populations with cancer, although the drugs are used commonly clinically in people with cancer. Table 5 summarizes specific medications by class or category, hypnotic dose, and onset and duration of action. Specific features of drugs also are noted.

Hypnotics are the most commonly prescribed medications and include benzodiazepines and nonbenzodiazepine hypnotics, sometimes referred to as Z drugs. The drugs vary in their half-lives. Those with longer half-lives can cause daytime sleepiness and impair waking cognitive and motor function, and those with shorter half-lives may wear off before desired or scheduled wake-up times.

Antidepressants including serotonin reuptake inhibitors (SSRIs) and tricyclic antidepressants also may aid sleep, depending on dosages used. They have demonstrated some benefit for treatment of concomitant depression, neuropathic pain, hot flashes, and night sweats. SSRIs have varying effects on anxiety and daytime activity. The drugs have a narrow therapeutic index, and signs of toxicity should be monitored closely.

To evaluate the efficacy of current pharmacologic approaches, a search was conducted to identify meta-analyses. The search strategy included MEDLINE, CINAHL, PsycINFO, and the Cochrane Library covering 1994–2004, using the key terms insomnia, sleep disturbance, hypnotics, pharmacotherapy, and meta-analysis. Stimulants were not included in the search; however, they are being tested to improve daytime sleepiness and fatigue in people with cancer. The efficacy of hypnotic drugs has been evaluated in five meta-analyses published from 1997–2004. None of them was specific to the use of the drugs in patients with cancer or their caregivers. Specific details are summarized in Table 6. The reports were limited by the diversity of outcomes and variable methods of summarizing results that made it difficult to pool findings. Most studies were of short duration; thus, limited knowledge exists about long-term efficacy and side effects of the drugs.

Consistent evidence exists that benzodiazepines and nonbenzodiazepine hypnotics reduce self-reported sleep onset latency time and number of awakenings and improve self-reported sleep duration, total sleep time, and sleep quality. No clear evidence has been found that one type of hypnotic is superior to another. Benzodiazepines were associated with increased daytime sleepiness, dizziness, or lightheadedness but not discontinuation of drug. One meta-analysis examined behavioral and pharmacologic approaches and concluded that the duration of effects from behavioral therapy was significantly longer than those from pharmacotherapy (Smith, Perlis, et al., 2002). Because of a lack of evidence specific to cancer populations, clinicians should evaluate systematically how each patient responds to a prescribed agent with regard to insomnia and side effects of the medication (Clark et al., 2004).

Herbal and complementary supplements used to promote sleep: To examine the evidence for complementary and alternative pharmacologic substances to improve sleep in people with cancer, a search was conducted for studies and reviews of research published from 1990–2005. CINAHL and PsycINFO were searched, using the key terms cancer and sleep and complementary therapy, cancer and insomnia and complementary therapy, and insomnia and complementary therapy. The identified substances primarily included the herbal supplements valerian, kava, and St. John’s wort, plus the hormone supplement melatonin. Milder sedatives identified as needing clinical study included chamomile, lavender, lemon balm, and passionflower. A summary of the findings is presented in Table 7.

Although patients with cancer were included as participants in a few studies, research testing pharmacologic complementary and alternative substances to treat sleep disturbances that focused specifically on people with cancer is almost nonexistent. In addition, most of the studies have had major design flaws, small sample sizes, uncontrolled confounding variables, and other threats to internal and external validity (Block, Gyllenhaal, & Mead, 2004; Gyllenhaal, Merritt, Peterson, Block, & Gochenour, 2000; Stevinson & Ernst, 2000).

A meta-analysis of the effects of melatonin on sleep revealed only minimal clinical benefits, with sleep onset latency reduced by 3.9 minutes, sleep duration increased by 13.7 minutes, and sleep efficiency increased by 3% (Brzezinski et al., 2005). Studies of effects of valerian on sleep have used weak designs and produced inconsistent results, leading the U.S. Pharmacopoeia to conclude that insufficient evidence exists in the scientific literature to recommend valerian for insomnia (Stevinson & Ernst, 2000). Kava studies have revealed mixed results. Adverse reactions and safety concerns, including a number of cases of hepatic failure that required liver transplantation, prompted a U.S. Food and Drug Administration alert in 2002. In particular, patients with cancer were instructed not to take kava (Block et al., 2004; Memorial Sloan-Kettering Cancer Center, 2005), and the supplement is banned in several countries (Consumer Reports, 2004). St. John’s wort may have anxiolytic effects with relevance to sleep, but herb-drug interactions with chemotherapeutic agents and other common drugs make the herb a potentially dangerous choice for use in patients with cancer (Block et al.).

To summarize, the evidence to support the use of herbal sedatives is weak and inconsistent, whereas data on adverse effects are not collected and reported regularly. In fact, the lack of pure, standardized ingredients in available compounds is a major limitation to research and clinical use of the supplements. In many cases, patients are at risk for adverse outcomes related to herbal substances or their contaminants.

Despite the limitations, consumers who are eager for help with sleep disturbances increasingly are turning to over-the-counter and Internet sales of complementary and alternative therapies advertised as “natural” and safe. An Institute Of Medicine report released in January 2005 revealed that one-third of American adults have used such therapies and that they are untested and often unsafe (Use of Complementary and Alternative Medicine Committee, 2005).

Currently, the National Center for Complementary and Alternative Medicine Web site (National Center for Complementary and Alternative Medicine, 2005) lists more than 30 cancer clinical trials (www.nccam.nih.gov/clinicaltrials/cancer) and three cancer side-effect clinical trials in progress using complementary and alternative medicines with people with cancer (www.nccam.nih.gov/clinicaltrials/cancersideeffects). Results from the studies will provide researchers and clinicians with more scientifically rigorous information about the outcomes of the use of complementary and alternative medicines in patients with cancer.

Oncology nurses should be familiar with the research evidence concerning complementary and alternative therapy medicine and supplements and assess their use for people with cancer to better assist patients and caregivers to make informed decisions. A continued need exists for well-designed, large-sample, double-blind, placebo-controlled clinical trials to determine the efficacy and safety of complementary and alternative therapies for sleep/wake disturbances in people with cancer.

Nursing Implications

Practice

This state-of-the-science summary of sleep/wake disturbances in people with cancer and their caregivers provides information to guide evidence-based practice, the “conscientious explicit and judicious use of theory-derived research-based information in making decisions about care delivery to people or groups of patients and in consideration of people needs and preferences” (Ingersoll, 2000, p. 152). This article addresses all steps of an evidence-based practice process: Clinical nurses and advanced practice nurses often are the first healthcare team members to hear patient complaints of sleep disturbances. Complaints of sleep disturbance can emanate from a variety of problems (Berger, 1998; Carpenter et al., 2004; Clark et al., 2004; Davidson et al., 2002; Montplaisir & Godbout, 1990; Montplaisir, Lorrain, & Godbout, 1991; Parker, 2004; Roscoe et al., 2002; Vena et al., 2004). To understand the nature of sleep complaints, clinicians should perform assessments in a systematic manner using valid and reliable tools to obtain information needed to target interventions or appropriate referrals such as sleep specialists (Clark et al.; Vena et al.).

Because of the high incidence of sleep/wake disturbances in people with cancer, sleep-screening tools, such as the Clinical Sleep Assessment (Adult) and Clinical Sleep Assessmen (Child), should be integrated into oncology clinical practice. The challenge is to determine when and how to perform screening. Not all patients report disturbed sleep; however, a subset of patients report problems at varying times throughout the cancer experience (Berger et al., 2003; Carpenter et al., 2004; Davidson et al., 2002; Engstrom et al., 1999; Koopman et al., 2002; Lee, Landis, et al., 2004). Clinicians can initiate sleep assessments by routinely asking a preliminary question during each clinical contact: “Are you having sleep problems or difficulty staying awake during the day?” If a patient offers an affirmative response, standardized assessments can be performed.

Data generated from screening tools can prove beneficial for specific patients as well as for groups of patients. At the individual patient level, clinicians can use assessment data to make appropriate patient referrals for further evaluation as necessary. In addition, clinical assessment data for a specific patient can be used to design and prescribe a tailored intervention that increases the skills of self-assessment, self-management (e.g., sleep hygiene), or self-monitoring of negative effects of sleep disturbance (e.g., excessive daytime sleepiness). At the group level, clinical screening data can be used as a benchmark, prior to intervening, as part of quality-improvement projects. Group-level screening data also can be used to provide prevalence and intensity information about sleep disturbances that can be compared within or across patient populations and ultimately enable more appropriate selection and testing of interventions.

The Joint Commission on Accreditation of Healthcare Organizations recommends that hospitals and clinics complete periodic quality-improvement projects. Clinical sleep tools for screening can provide an excellent means to report on assessments of the nine sleep parameters and on interventions designed to reduce sleep disturbances.

Education

Nursing education has not included sufficient information about sleep and circadian rhythms in undergraduate curriculum content, despite the fact that considerable emphasis has been placed on physical activity, nutrition, and stress management as key components of health and wellness (Lee, Landis, et al., 2004). A nursing task force, including members of the Association of Professional Sleep Societies, recently developed educational competencies for sleep and chronobiology (Lee, Landis, et al.). Educators are encouraged to learn more about the recommendations and to incorporate the competencies into curricula. Undergraduate objectives are organized into learning objectives, clinical competency objectives, and clinical evaluation methods that can be integrated into medical-surgical and psychiatric nursing courses. Graduate-level learning activities are designed to prepare advanced practice nurses to work as members of interdisciplinary teams at accredited sleep disorder centers or in general practice settings. The content also can be used to organize staff development offerings for clinical nurses, advanced practice clinical nurses, nurse educators, and researchers.

• Nursing education programs should include an overview of normal sleep, the prevalence of sleep/wake disturbances in cancer populations, a conceptual understanding of the processes that regulate sleep and waking, the measurement of sleep and waking (clinical and research), and currently available evidence-based therapies and interventions.
• Nursing education programs and staff development programs should include the importance of patient education regarding general strategies, such as good sleep hygiene, to optimize sleep and waking.

Research

Studies in cancer populations are a high research priority because sleep disturbances are common in people with cancer, and poor sleep may be hazardous to health and safety. Issues that currently are being addressed by the larger sleep scientific community include the lack of a standard procedure to determine and document outcomes of successful sleep intervention. Criteria beyond sufficiency of sleep time that also need consideration include definition of intervention endpoint (single or multiple), how best to measure intended outcomes, and whether a patient’s self-report of perceived quality of sleep is a more appropriate endpoint than biologic outcomes.

Sleep scientists recognize that a critical component of randomized clinical trials is the selection of reliable, valid, conceptually sound, sensitive, and clinically relevant outcome instruments. Evidence-based guidelines depend on the development and use of such instruments in a standardized manner. Sleep scientists also are aware that they need to move beyond insomnia as the exclusive focus of their research and link sleep research with other related symptoms such as pain, depression, fatigue, and anxiety that are applicable to the population being studied (Morin, 2003). A summary of directions for future research related to sleep disturbances in people with cancer and their caregivers appears in Figure 4.

Summary

Much remains to be learned about the nature and purposes of sleep in the general population, making the assessment and treatment of sleep disturbances in patients with cancer and their caregivers especially challenging. Nonetheless, the state of the science and theory development have evolved to a beginning understanding of the complexities of the problems in cancer populations. Numerous factors have been identified that can contribute to sleep/wake disturbances in people with cancer, providing the initial descriptive work needed to guide the development and testing of population-specific interventions designed to enhance sleep. In addition, an exploration of how sleep may affect other symptoms experienced by people with cancer, how it may affect their tolerance of treatment, and how genetics plays a role in the expression of sleep/wake disturbances may be especially relevant to long-term survival rates and QOL. The information could guide the identification of people at high risk for sleep/wake disturbances as well as the development of new interventions.

The authors would like to acknowledge Daniel Buysse, MD, professor of psychiatry in the School of Medicine at the University of Pittsburgh in Pennsylvania, for participating in the conference and reviewing the manuscript.

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Ann M. Berger, PhD, RN, AOCN^®, is an associate professor, an advanced practice nurse, and the Niedfelt Nursing Professor in the College of Nursing at the University of Nebraska Medical Center in Omaha; Kathy P. Parker, PhD, RN, FAAN, is the Edith F. Honeycutt professor in the Nell Hodgson Woodruff School of Nursing at Emory University in Atlanta, GA; Stacey Young-McCaughan, PhD, RN, AOCN^®, is a colonel in the U.S. Army Nurse Corps and chief of the Department of Clinical Investigations in Fort Sam Houston, TX; Gail A. Mallory, PhD, RN, CNAA, is the director of research at the Oncology Nursing Society in Pittsburgh, PA; Andrea M. Barsevick, RN, DNSc, AOCN^®, is an associate member and director of nursing research at Fox Chase Cancer Center in Philadelphia, PA; Susan L. Beck, PhD, APRN, FAAN, AOCN^®, is interim associate dean for academic programs in the College of Nursing at the University of Utah in Salt Lake City; Janet S. Carpenter, PhD, RN, is an associate professor in the School of Nursing at Indiana University in Indianapolis; Patricia A. Carter, PhD, RN, CNS, is an associate professor and assistant dean for student and clinical affairs in the School of Nursing at the University of Texas at Austin; Lynne A. Farr, PhD, is an emeritus professor in the College of Nursing at the University of Nebraska Medical Center; Pamela S. Hinds, PhD, RN, is the director of nursing research at St. Jude Children’s Research Hospital in Memphis, TN; Kathryn A. Lee, RN, PhD, FAAN, is a professor and the Livingston Chair in Nursing in the Department of Family Health Care Nursing in the School of Nursing at the University of California, San Francisco; Christine Miaskowski, RN, PhD, FAAN, is a professor in the Department of Physiological Nursing at the University of California, San Francisco; Victoria Mock, DNSc, FAAN, is a professor in and the director of the Center for Nursing Research at Johns Hopkins University in Baltimore, MD; Judith K. Payne, PhD, RN, AOCN^®, is an assistant professor in the School of Nursing at Duke University in Durham, NC; and Martica Hall, PhD, is an assistant professor of psychiatry and psychology in the School of Medicine at the University of Pittsburgh in Pennsylvania. The conference on which this article is based was supported by the National Cancer Institute (R13 CA108758-01); the ONS Foundation’s Center for Leadership, Information and Research and the Oncology Nursing Society, both in Pittsburgh; Ambulatory Monitoring, Inc., in Ardsley, NY; and Mini Mitter Co., Inc., in Bend, OR. The views of Young-McCaughan are her own and do not purport to reflect the position of the Army Medical Department, Department of the Army, or the Department of Defense. (Submitted April 2005. Accepted for publication August 5, 2005.)

Author Contact: Ann M. Berger, PhD, RN, AOCN^®, can be reached at aberger@unmc.edu, with copy to editor at ONFEditor@ons.org.

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