Sleep in older adults with Alzheimer's disease can often be extremely fragmented, thus disturbing normal sleep-wake rhythms. This poor-quality sleep is challenging for caregivers and frequently results in admitting older adults to long-term care institutions. Many variables, such as genes, medications, depression,and environmental factors, influence sleep in persons with Alzheimer's disease. Interventions, such as exposure to light, melatonin therapy, sleep hygiene, and physical activity, are commonly used to treat or to prevent sleep problems. Neuroscience nurses can play an important role in assessing sleep characteristics and related factors, educating caregivers and staff, providing family members with emotional support, and conducting research.
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The number of people aged 65 years and older has increased worldwide and now includes about 7% of the global population (Population Reference Bureau, 2006). In the United States, the number of people aged 65 years and older, which was 36.3 million in 2004 (12% of the population), is predicted to increase to 21% by the year 2050 (U.S. Census Bureau, 2005). With this aging population has come an increasing recognition of the prevalence of dementia. The Alzheimer's Association estimated that about 5 million older American adults had Alzheimer's disease (AD) in 2008 (Alzheimer's Association, 2008). This number is expected to be increased to 7.7 million in 2030 and range between 11 million and 16 million people by 2050 (Alzheimer's Association, 2008).
Sleep disturbances are common in persons with AD. Cross-sectional studies of community and clinic samples have revealed the prevalence of sleep problems in persons with AD to be as high as 40%; these problems include difficulty falling asleep, multiple awakenings during sleep, disrupted sleep-wake rhythms, and early morning awakenings (Carpenter, Strauss, & Patterson, 1995; McCurry et al., 1999; Moran et al., 2005).
Assessing and treating sleep problems in persons with AD is important because they are associated with decreased survival (Gehrman et al., 2004), cognitive and functional decline, and behavioral and psychological symptoms (Moe, Vitiello, Larsen, & Prinz, 1995; Moran et al., 2005). Sleep problems in persons with AD are a physical and psychological burden for their caregivers (Donaldson, Tarrier, & Burns, 1998) and a major reason why such patients are admitted to long-term care institutions (Ancoli-Israel, Klauber, Gillin, Campbell, & Hofstetter, 1994). Nurses have an important role to play in identifying sleep characteristics, assessing specific needs, and providing care for persons with AD who have sleep problems.
This article presents an overview of sleep problems in older adults with AD. Normal sleep characteristics are addressed first. Common sleep characteristics and the risk factors for sleep problems in older adults with AD are then reviewed. Finally, interventions for older adults with AD and implications for neuroscience nursing practice are discussed.
Normal Sleep Characteristics
Sleep States
Sleep is composed of two states: nonrapid eye movement (NREM) and rapid eye movement (REM) sleep. On the basis of the depth of sleep, NREM sleep is subdivided into stages. In healthy young adults, sleep usually begins at the lightest stage, NREM stage 1, and progresses through stage 2 and into the deepest sleeps, stage 3 and stage 4, also known as delta or slow-wave sleep. The sleeper then progresses back to lighter sleep and then into REM sleep. Sleep stage is identified by using an electroencephalogram to detect electrical activity in the cerebral cortex, an electrooculogram to monitor eye movements, and an electromyogram to measure muscle activity (Chesson et al., 1997). The combination of these three recordings is referred to as polysomnography (Smith, Nowakowski, Soeffing, Orff, & Perlis, 2003).
Sleep quality is defined by the nighttime sleep characteristics revealed by self-report or polysomnography. It usually includes sleep onset latency, waking frequency, durations of awakening after sleep onset, amount of nighttime sleep, and sleep efficiency (i.e., the ratio of time asleep to time in bed; Floyd, 2002).
Aging and Sleep
The quantity and quality of sleep changes as a person ages. REM and NREM cycles last about 50 to 60 minutes in newborns and roughly 90 minutes in adults (Carskadon & Dement, 2005). REM sleep comprises as much as 50% of an infant's sleep but diminishes to between 20% and 25% in young adults (Lee, 1997). The occurrence of stages 3 and 4 is highest inyoung children (20%) and decreases with age to between 5% and 10%, depending on health status (Carskadon & Dement, 2005). Older adults spend more of the night in lighter sleep (stages 1 and 2) than younger adults, resulting in more sleep complaints (Kryger, Monjan, Bliwise, & Ancoli-Israel, 2004; Neubauer, 1999). Sleep efficiency also decreases in older adults (Haimov & Lavie, 1997; Redline et al., 2004). Despite spending more time in bed, older adults complain of awaking often during the night, having less total sleep time, taking longer to fall asleep, and taking more naps (Kryger et al., 2004). The major sleep period also tends to advance in relation to clock time because older adults go to bed and arise earlier than younger adults (Ancoli-Israel, Poceta, Stepnowsky, Martin, & Gehrman, 1997).
Sleep Characteristics in Older Adults With AD
Compared with healthy older adults, those with AD experience significantly poorer sleep efficiency with longer sleep latencies (Buysse et al., 1992; Gagnon et al., 2006) and have more frequent awakenings during the night compared with older adults without dementia (Bonanni et al., 2005). The increased awakenings result in decreased REM sleep (Bonanni et al., 2005) and reduced deep sleep compared with healthy older adults (Gagnon et al., 2006). Increased daytime sleep is also typical in older adults with AD as the severity of their dementia progresses (Ancoli-Israel et al., 1994; Bonanni et al., 2005; Lee et al., 2007).
Behavioral disturbances, such as nocturnal delirium, agitation, or wandering, are noticeable in older adults with AD (Gehrman et al., 2003; Little, Satlin, Sunderland, & Volicer, 1995) and are believed to be associated with disrupted biological rhythms (Okawa et al., 1991). This phenomenon is called sundowning (McCurry, Reynolds, Ancoli-Israel, Teri, & Vitiello, 2000), a constellation of increasing behavioral disturbances in patients with dementia in the late afternoon or early evening (Vitiello & Borson, 2001). The temporal pattern of sundowning has been thought to reflect a deterioration in normal diurnal rhythms (Vitiello & Borson, 2001), although peak timing of the sundowning occurrence varies from early afternoon to night (Bliwise, Carroll, Lee, Nekich, & Dement, 1993; Martin, Marler, Shochat, & Ancoli-Israel, 2000; Martino-Saltzman, Blasch, Morris, & McNeal, 1991).
Sleep-disordered breathing can also contribute to sleep fragmentation in older adults with AD (Petit, Montplaisir, & Boeve, 2005). Cessation of breathing during sleep can be caused by the obstruction of the upper airway (obstructive sleep apnea), the temporary loss of ventilatory effort (central apnea), or a combination of the two (White, 2005). Because of the frequent nocturnal awakenings, sleep apnea is often associated with restless sleep and daytime sleepiness (White, 2005).
Disturbed sleep-wake rhythms are common in older adults with AD. Phase delay (i.e., onset of the sleep period occurs later than most people and awaking in the morning is difficult) is more prominent in persons with AD than that in healthy older adults (Harper et al., 2001; Satlin, Volicer, Stopa, & Harper, 1995) and those with other types of dementia (Harper et al., 2001). Persons with AD who have both phase-delayed rhythms and frequent awakenings during the night for any reason (e.g., sundowning, sleep apnea, or other environmental cause) may experience excessive daytime sleepiness.
Causes of Sleep Disturbances
Changes in the Suprachiasmatic Nucleus and Neuronal Pathway
Certain neuronal pathways regulate arousal and the sleep-wake cycle, including the cholinergic basal forebrain nuclei, the serotoninergic dorsal and median raphe nuclei, and the noradrenergic locus coeruleus (Saper, Chou, & Scammell, 2001; Vitiello & Borson, 2001). Sleep disturbances in older adults with AD are believed to be caused by neurodegenerative changes in these brain regions. Change in the hypothalamic suprachiasmatic nucleus (SCN) has also been considered to be one of main causes of sleep disturbances in persons with AD. The SCN is a small group of neurons in the anterior hypothalamus and is thought to generate and to regulate circadian rhythms such as sleep-wake rhythms (Hoogendijk et al., 1996; Mirmiran et al., 1992). In the normal aging process and in the progression of AD, cell loss and decreased SCN volume cause disturbances in circadian rhythms and thus contribute to disrupted sleep-wake patterns, which is even more pronounced in those with AD (Swaab, Fisser, Kamphorst, & Troost, 1988; Wu & Swaab, 2007). The SCN is also known to regulate the secretion of melatonin, the "sleep hormone," by the pineal gland and plays a major role in the circadian component that regulates the timing of sleep (Cardinali, Furio, & Reyes, 2005). A decreased melatonin level in older adults with AD is related to disrupted sleep-wake rhythms (Mishima et al., 1999; Wu & Swaab, 2005).
Genes
With the dramatic rise in AD diagnoses, pathological hallmarks (extracellular senile plaques, neurofibrillary tangles, and neuronal loss) have been discovered that may influence sleep (Braak & Braak, 1991). Evidence from several sources would suggest that sleep disturbances in older adults with AD may be based in part on genetic factors. Four causative genes (amyloid precursor protein gene, presenilin 1, presenilin 2, and apolipoprotein E) have been associated with AD (Morishima-Kawashima & Ihara, 2002). Apolipoprotein E in particular has been clearly associated with sleep disturbances in persons with AD (Cacabelos et al., 1996; Liu, Zhou, van Heerikhuize, Hofman, & Swaab, 1999), and monoamine oxidase A also has a significant association with sleep disruption in this population (Craig et al., 2006).
Medications
Several medications can contribute to sleep problems. Older adults metabolize drugs slower than younger adults; thus, medications such as hypnotics that are commonly prescribed to older adults are particularly cumulative and dangerous (Ancoli-Israel & Kripke, 1991). Many older adults with dementia, particularly those who reside in nursing homes, are prescribed antipsychotics, antidepressants, benzodiazepines, and nonbenzodiazepine sedative hypnotics (Simpson, Richards, Enderlin, O'Sullivan, & Koehn, 2006; Svarstad & Mount, 2002). These medications, however, may have negative side effects, including sleep disturbances. For example, Simpson et al. (2006) found that selective serotonin reuptake inhibitors resulted in a lower percentage of nighttime sleep and increased daytime napping, although trazodone hydrochloride improved nighttime sleep.
Depression
Depression is clearly associated with sleep problems in persons with AD (Lopez et al., 2003; McCurry, Vitiello, Gibbons, Logsdon, & Teri, 2006). A recent study found that the percentage of nighttime sleep was higher in older persons with AD when their level of depression was low (McCurry et al., 2006). Researchers have pointed out that the combination of dementia and depression may cause even more serious sleep disturbances than dementia alone (Ancoli-Israel, Poceta, et al., 1997). In another study, older adults with concurrent symptoms of depression and dementia showed a lower percentage of stages 3 and 4 sleep than people with either depression or dementia (Buysse et al., 1992). However, the relationship between sleep problems and depression is complex because either condition can cause the other (Ancoli-Israel & Cooke, 2005).
Environmental Factors
Environmental factors have been shown to substantively affect sleep in persons with dementia. Light level has a significant effect on sleep. Bright light appears to be a powerful synchronizer of circadian rhythms and directly influences sleep-wake patterns (Czeisler & Gooley, 2007). Light intensity is commonly reported in units of lux (Sack et al., 2007), which is the International System unit for illumination (International Bureau of Weights and Measures, 2006). One lux is equal to the light intensity of a standard candle 1 m away from the eye (Sack et al., 2007). Direct sunlight on a clear day varies from 30,000 lx to more than 100,000 lx. Several studies have shown that persons with dementia in institutions are exposed to only a few minutes of light brighter than 1,000 lx, and none or very few are exposed to light more than 2,000 lx (Ancoli-Israel et al., 1991; Ancoli-Israel, Klauber, et al., 1997; Shochat, Martin, Marler, & Ancoli-Israel, 2000). Noise from staff or residents, equipment (i.e., cleaning, linen carts), or television may also result in sleep disturbances in nursing home residents (Schnelle et al., 1998).
Interventions
Pharmacologic Interventions
Although pharmacologic treatment has been widely used for sleep disturbances, its effectiveness has not been proved in controlled trials with persons with AD (McCurry et al., 2000). Moreover, because medications may have adverse effects, pharmacologic treatment is recommended only if nonpharmacologic interventions have failed (McCurry et al., 2000; Petit et al., 2005).
Sedative-hypnotic drugs (e.g., zolpidem tartrate and triazolam) could benefit persons with AD, particularly those who have difficulty falling asleep and frequent nocturnal awakenings (McCarten, Kovera, Maddox, & Cleary, 1995; Shaw, Curson, & Coquelin, 1992; Shelton & Hocking, 1997). However, adverse events, such as an increased risk for falls (McCurry et al., 2000) and hip fractures (Cumming & Le Couteur, 2003; Wang, Bohn, Glynn, Mogun, & Avorn, 2001), have been frequently reported. If the individual sleeps through the night with the hypnotic, there is less chance of falling; however, there is increased risk for falling if the dose is such that the person is still sleepy and unsteady in the morning upon final awakening. Antipsychotic medications, such as olanzapine and risperidone, have often been used to induce sleep in patients with AD who experience nocturnal agitation. Although these medications have been shown to decrease agitation significantly (Brodaty et al., 2003; Street et al., 2000), clinicians should prescribe them cautiously because the risk of sudden death has been documented (Liperoti et al., 2009; Schneider, Dagerman, & Insel, 2005). Cholinesterase inhibitors (e.g., donepezil hydrochloride and galantamine hydrobromide) may also improve sleep in persons with AD (Ancoli-Israel, Amatniek, Ascher, Sadik, & Ramaswamy, 2005; Mizuno, Kameda, Inagaki, & Horiguchi, 2004) but could have adverse sleep effects (Burns et al., 1999; Rogers, Doody, Mohs, & Friedhoff, 1998).
The use of melatonin to treat sleep disturbances has received attention over the past 10 years (Bliwise, 2004). In studies using various dosages (3, 6, and 9 mg) of exogenous melatonin in persons with dementia, melatonin has been shown to improve sleep, to decrease daytime sleepiness, and to reduce sundowning (Cardinali, Brusco, Liberczuk, & Furio, 2002; Cohen-Mansfield, Garfinkel, & Lipson, 2000). Combination therapy (5 mg melatonin administration with light exposure) has also been shown to increase daytime wake time and to strengthen rest-activity patterns (Dowling et al., 2008). In contrast, other studies of persons with AD reported no significant effect on sleep when melatonin was administered in doses of 2.5 and 10 mg (Singer et al., 2003) or 6 mg (Serfaty, Kennell-Webb, Warner, Blizard, & Raven, 2002). Although no adverse effects (i.e., nausea, headache, dizziness, and drowsiness) have been reported for short-term use in persons with dementia (Cohen-Mansfield et al., 2000; Serfaty et al., 2002), the long-term safety of melatonin administration has not been evaluated (Arendt & Skene, 2005).
Nonpharmacologic Interventions
Light Therapy
Because persons with AD, especially those in institutions, are not exposed to adequate amounts of light, many studies have attempted to improve their sleep using bright light. Light exposure in the evening typically delays sleep-wake rhythms (i.e., sleep onset occurs to a later time), whereas light exposure in the morning advances the rhythms (i.e., sleep onset occurs to an earlier time; Chesson et al., 1999; Dowling & Mastick, 2010). Morning and evening light therapy have been applied to older adults with AD using various light intensities (from 1,500 to 8,000 lx) and durations of exposure (1 or 2 hours a day for 1 week to several weeks). Beneficial effects on sleep have been reported, including increased nocturnal sleep time, reduced waking time, increased sleep efficiency, decreased daytime napping (Fetveit & Bjorvatn, 2005; Fetveit, Skjerve, & Bjorvatn, 2003; Mishima et al., 1994), stability of rest-activity patterns (Ancoli-Israel et al., 2003; Dowling, Mastick, Hubbard, Luxenberg, & Burr, 2005), and decreased behavioral disturbances such as sundowning (Satlin, Volicer, Ross, Herz, & Campbell, 1992). Light has virtually no side effects (Chesson et al., 1999; Sloane et al., 2007) if administered at the proper time, but it can cause manic activity or hyperarousal if administered at the wrong time of day. Despite numerous benefits as well as possible harm from use, the means to appropriately determine the exact timing, duration, frequency, and intensity of the light therapy have not been standardized. The effectiveness of light therapy in community-dwelling people with dementia is less clear (Colenda, Cohen, McCall, & Rosenquist, 1997), and it may be less practical because the protocols are demanding for caregivers.
Sleep Hygiene and Physical Activity
Sleep hygiene refers to daily behaviors, environmental conditions, and other sleep-related factors that can be adjusted and are believed to promote sleep quality (American Sleep Disorders Association, 1997; Stepanski & Wyatt, 2003). It can include setting desirable bed and rising times, improving the sleep environment and routine, and eliminating possible triggers (e.g., bed partner snoring and street noise) for nighttime awakenings (McCurry, Gibbons, Logsdon, Vitiello, & Teri, 2003, 2005). Applying a sleep hygiene program for community-dwelling older adults with AD has resulted in improved sleep. Individualized sleep hygiene programs, conducted by trained caregivers, have resulted in a significant improvement in nighttime sleep, a decrease in daytime sleepiness and depression, and an increase in the number of days exercised every week (McCurry et al., 2005). Physical activity (Alessi et al., 1995) and combinations of other interventions, such as improving the physical environment and increasing daylight exposure (Alessi et al., 2005; Alessi, Yoon, Schnelle, Al-Samarrai, & Cruise, 1999), have also resulted in decreased daytime sleep and agitated behaviors in older adults with dementia who reside in institutions.
Implications for Nursing
Sleep problems in older adults with AD can affect their health and their caregivers' sleep and care-related stress. Neuroscience nurses in institutions (e.g., nursing homes) and community settings are in a pivotal position to prevent sleep problems in their patients or initiate interventions that will mitigate their harmful effects.
Assessing sleep characteristics and identifying the causal factors of sleep problems in persons with AD are essential. Monitoring a patient's nighttime sleep (e.g., total sleep time, sleep efficiency, duration of sleep latency, number and duration of awakenings, and nocturnal wandering or agitation) and daytime sleep (e.g., total napping time) at least for 1 to 2 weeks should be the first step in evaluating sleep problems.
In institutions, nurses or staff can assess the sleep of residents with AD. However, heavy workloads preclude staff from observing patient sleep patterns over long periods. The easiest and most realistic way to monitor sleep habits is to use sleep diaries, which include bedtime, rise time, episodes of nocturnal awakenings, and any other events contributing to sleep disturbance. After sleep data have been collected and sleep problems have been documented, nurses should review medical records to identify the causal factors of sleep disturbances, such as medication use and comorbidities that include mental health issues like depression or physical health issues like hypertension and obesity. Broad assessment of their living environment is also essential. For example, routines of care, staffing patterns and duties, staff-resident interactions, behaviors of other residents, and location of residents' rooms in relation to sources of light and noise should be explored (Vitiello & Borson, 2001). Interviews with staff and administrators may elicit important information that would otherwise be overlooked during patient assessment, which often focuses on clinical issues (Vitiello & Borson, 2001). Nurses play an integral role in implementing nonpharmacologic interventions such as light therapy and sleep hygiene programs. To determine the timing of exposure to light, characteristics of sleep-wake rhythms of individuals (i.e., phase delay or advance) should be the basis. Morning light exposure could be beneficial to an individual with phase delay as evening light exposure could be to an individual with phase advanced rhythms. Because artificial light therapy usually requires a light box, it is often difficult to engage a patient's full attention and participation. To ensure compliance, nurses must engage patients in the therapy by scheduling a daily routine (e.g., tea or meal time) in front of the light box. Because a sleep hygiene program requires adherence to a structured routine, nurses must educate other staff members about it for the program to be a successful intervention.
In community settings, caregivers are a valuable source information about the sleep problems of persons with AD and possible causal factors. To help these caregivers identify sleep problems, nurses should teach them how to use sleep diaries. Daytime routines, mood and behavioral problems, and past and present relationships with caregivers must be also assessed (Vitiello & Borson, 2001). To improve the sleep of persons with AD over time, nursing interventions should include caregiver participation. Nurses can plan sleep hygiene programs (see Table 1) and teach caregivers how to promote better sleep for individuals with AD. Because caregivers may be intimidated by the burden of changing sleep habits of their relatives with AD, nurses who plan a sleep hygiene program must examine its feasibility and evaluate adherence to its schedule.
Emotional support for caregivers or family members is also necessary. The stress, burden, and sleep deprivation entailed in caring for persons with dementia may dissuade caregivers from implementing changes recommended to improve a person's sleep. Nurses can discuss the caregivers' problems and concerns, address their clinical problems as they arise (Teri, Logsdon, & McCurry, 2002), and make referrals to an appropriate support group.
Nurse scientists can conduct and evaluate many interventions and modify or develop new cost-effective strategies. Further research on the effectiveness of interventions should include testing duration, intensity, and the frequency of light therapy; dose and timing of melatonin; and the effectiveness of short- and long-term combined interventions (e.g., light therapy with sleep hygiene).
Summary
Compared with healthy older adults, older persons with AD exhibit decreased sleep efficiency, decreased stages 3 and 4 deep sleep and REM sleep, and disrupted sleep-wake rhythms. Recognizing sleep characteristics and the factors that contribute to sleep problems in this population will improve the ability of healthcare personnel to appropriately and successfully treat these problems. Nurses can play a prominent role in helping these patients to sleep better at night and to maintain their function during the day. Improving a patient's sleep at night will also improve the sleep of his or her caregiver and family members so that they too will have better daytime functioning and interactions with the patient.
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