Sleep and nighttime behavioral disturbances are fairly common among patients with Alzheimer's disease (AD), occurring in approximately 13% to 46% of clinic outpatients (Carpenter, Strauss, & Patterson, 1995; Devanand et al., 1992; Méndez, Martin, Smyth, & Whitehouse, 1990; Teri, Börsen, Kiyak, & Yamagishi, 1989). The types of problems patients exhibit are multifaceted. Patients with AD are more likely to awaken during the night and to spend less time in deep, restorative stages of sleep (Bliwise, 1994; Vitiello, BHwise, & Prinz, 1992). They can experience shifts in their 24-hour circadian rhythms that can lead to irregular sleep-wake patterns, prolonged daytime napping, or even complete day and night sleep pattern reversals (Ancoli-Israel, Klauber, Gillin, Campbell, & Hofstetter, 1994; Okawa et al., 1991; Satlin, Volicer, Stopa, & Harper, 1995). Of all these problems, being awakened by the patient at night has been identified as one of the most disturbing sleep irregularities faced by dementia caregivers (McCurry et al., 1999) and is a major cause of patient institutionalization (Hope, Keene, Gedling, Fairburn, & Jacoby, 1998; Pollak & Perlick, 1991).
The loss of or damage to neuronal pathways that initiate and maintain sleep, as well as changes in the circadian timing system that determine tendency toward sleep and wakefulness, are likely contributors to the sleep disturbances observed in patients with AD (van Someren, 2000; Vitiello & Prinz, 1994). However, in addition to the physiological causes, there also may be psychological factors that contribute. The co-occurrences of sleep complaints in adults without dementia who have depressive or anxiety disorders are well known (Foley, Monjan, Izmirlian, Hays, Si Blazer, 1999; Ford & Kamerow, 1989; Maggi et al., 1998; Nofzinger, Buysse, Reynolds, & Kupfer, 1993; Ohayon, Cauclet, & Lemoine, 1998; Sheikh, 1994). Symptoms of depression and anxiety are common in individuals with AD (Cummings, 1997; Katz, 1998; Lyketsos et al., 1997; Small et al., 1997; Ten et al., 1999), and it might be expected that these conditions would also impact the sleep quality of affected individuals with dementia.
There have been few empirical studies, however, examining the relationship between mood and sleep quality in AD. McCurry et al. (1999) found no association between depression symptoms and the frequency of nighttime awakening in a sample of community-dwelling patients with AD. However, caregivers in that study did rate the sleep problems of patients who were depressed as more highly disturbing than did caregivers of patients who were not depressed. In contrast, Teri, Logsdon, Uomoto, and McCurry (1997) reponed that 43% of patients with AD diagnosed with major or minor depression had complete remission of their sleep disturbances after undergoing a 9-week behavioral treatment for depression, supporting the association between depression and sleep quality in this population. Significantly higher rates of insomnia have also been found in AD clinic outpatients with generalized anxiety disorder (GAD) than among patients without GAD (Chemerinski, Petracca, Manes, Leiguarda, & Starkstein, 1998). However, there have been no studies describing the association between sleep disturbances and anxiety in population-based samples of patients with AD.
This report describes the prevalence of anxiety symptoms tn a community-dwelling sample of patients with AD, and identifies factors independently associated with reports of patient nighttime awakening. The symptom of waking the caregiver at night was chosen for the investigation because of its significance for caregivers in previous studies, and its relevance to the clinical management of patients with AD.
Participants (N = 153) were recruited from an ongoing, community-based AD patient registry (ADPR) (Larson et al., 1990), as well as through referrals from physician practices in Seattle and community advertisements. All participants were enrolled in a treatment program designed to reduce the physical, affective, and behavioral problems in AD and to alleviate depression and burden in their caregivers (i.e., the Reducing Disability in Alzheimer's Disease [RDAD] study) (Teri et al., 2003). Pre-treatment data were analyzed for this report. Individuals diagnosed with dementia met National Institute of Neurological and Communicative Disease and Stroke and the Alzheimer's Disease and Related Disorders Association (NINCDSADRDA) criteria for "probable" or "possible" AD (McKhann et al, 1984) based on a comprehensive diagnostic evaluation (Larson et al., 1990).
Patients were required to be community-dwelling and ambulatory. All had caregivers who either lived with their patient (94%) or saw them every day (6%). Participants were not required to have any other behavioral problems and were enrolled regardless of whether they had such problems or not. Consequently, participants included those with and without co-morbid depression or anxiety symptoms, or other behavioral disturbances such as nighttime agitation and verbal aggression. A summary of patient and caregiver characteristics is provided in Table 1.
Patient ratings. The Mini-Mental State Examination (MMSE) (Folstein, Folstein, & McHugh, 1975) was used to measure cognitive status. The MMSE is a commonly used screen for dementia that provides information on patient orientation, attention, immediate memory, language, and praxis. A total score is reported (O to 30), with lower scores indicative of greater cognitive impairment. The Physical Self-Maintenance (PSM) and Instrumental Activities of Daily Living Scales (IADL) (Lawton & Brody, 1969) provided a caregiver-rated assessment of patient ADL and IADL functioning. The combined scales consist of 14 items, which are rated on a scale from 1 (not impaired) to 5 (severely impaired). Items assess a range of activities including toileting, ambulation, shopping, transportation, and handling finances.
Patient physical function was assessed using three subscales (i.e., Body Care and Movement, Mobility, Home Management) from the physical dimension of the Sickness Impact Profile (SIP) (Bergner, 1977). The SIP is considered one of the most responsive health status questionnaires (Liang, Larson, Cullen, & Schwartz, 1985) and it has been used to evaluate health in studies of patients with AD (Krenz, Larson, Buchner, & Canfield, 1988). In addition, two subscales from the Medical Outcome Study Short Form (MOSSF-36) (Physical Functioning and Role Functioning - Physical subscales) were rated (Stewart, Hays, & Ware, 1988). The SF-36 is a brief measure of health status that has been widely used with geriatric populations (Dexter, Stump, Tierney, & Wolinsky, 1996). For both the SIP and SF-30, higher scores are indicative of greater impairment.
Patient depression was rated using the Cornell Scale for Depression m Dementia (Alexopoulos, Abrams, Young, & Shamoian, 1988). The Cornell Scale is a 19-item, clinicianrated scale of depression symptoms designed for use with patients with dementia. The clinician uses information gathered from separate interviews with the patient with dementia and the caregiver to rate each item on a 3-point scale (O = absent during week prior to interview, 1 - mild or intermittent, 2 = severe), to yield a total possible score of 38- For this study, a modified Cornell scale was created that omitted three sleep-related items (i.e., difficulty falling asleep, multiple awakenings during sleep, early morning awakening) and one anxiety item.
Patient anxiety was rated using items from the Consortium to Establish a Registry for Aizheimer's Disease (CERAD) Behavior Rating Scale for Dementia (CBRSD) (Tariot et al., 1995). The CBRSD is an interviewer-based instrument designed for the assessment of mild to moderately impaired community-dwelling patients with AD. It rates the frequency of 48 behavioral symptoms during the past month on a scale of O (did not occur in the past month) to 4 (occurred 16 days or more in the past month). Seven anxiety-related items from the CBRSD were combined to create a composite anxiety rating. The items were:
* Participant felt anxious.
* Participant has shown physical signs of anxiety.
* Participant was tired.
DESCRIPTIVE DATA FOR REDUCING DISABILITY IN PATIENTS WITH ALZHEIMER'S DISEASE AND THEIR CAREGIVERS (N = 153)
* Participant was agitated.
* Participant was restless.
* Participant was easily irritated
* Participant was "clingy" with caregiver.
Items on the Anxiety scale were assigned a weight of 1, except for the two items "felt anxious" and "shows physical signs of anxiety," which were weighted more heavily (weight = 2) because they assessed anxiety most directly. The total possible scale range for the 7-item anxiety scale was O to 36, and actual scores ranged from O to 31. Chronbach's alpha for the summary scale was .63.
FREQUENCY OF ANXIETY SYMPTOMS FROM CERAD* BEHAVIOR RATING SCALE FOR DEMENTIA ANXIETY SUBSCALE
Patient behavior problems were rated using the Revised Memory and Behavior Problem Checklist (RMBPC) (Teri et al., 1992). The RMBPC is a self-report measure on which caregivers rate the frequency of 24 behaviors during the past week on a scale of O (never occurred) to 4 (occurred daily or more often). Caregivers also rate their reaction to each behavior on a scale of O (no distress) to 4 (severe distress). Memory and disruption subscale scores were calculated as an average frequency of the items contributing to each subscale. For this analysis, a modified RMBPC disruption score was created that omitted a sleep-related item (i.e., waking caregiver up at night) from the subscale computations.
Patient nighttime behavioral disturbance was assessed by asking caregivers how frequently patients woke them up at night during the past week. Frequency of being awakened and caregiver reaction were rated in a similar manner to the RMBPC. Frequency ratings correlated significantly with questions about nighttime disturbance in other study measures, including sleep items from the Cornell (multiple awakenings at night, r = .43) and the CBRSD (difficulty falling asleep or remaining asleep, r = .37).
Nighttime awakenings have been shown in previous studies to be associated with the same cognitive and functional variables as a larger composite sleep behavior scale extracted from the RMBPC (McCurry et al., 1999). Sleep medication use was also evaluated by asking caregivers to provide a list of all drugs they and the patient had taken during the past month at night to help sleep. For this analysis, patient use of psychotropic medications (e.g., sedative or hypnotic, anti-anxiety, anti-psychotic, antidepressant medications, over-thecounter sleep aids) and alcohol use (frequency and dose) were recorded.
Caregiver ratings. Caregiver depression and burden were assessed using the Hamilton Depression Rating Scale (HDRS) (Hamilton, 1967), and the Screen for Caregiver Burden (SCB) (Vitaliano, Russo, Young, Becker, & Maiuro, 1991). The HDRS is a 20-item interviewer-based measure that assesses frequency of depressive symptomatology during the past 2 weeks. Scores of 12 or higher are considered indicative of depression. In this sample, 7% of caregivers had an HDRS score in the depressed range.
The SCB is a 25-item questionnaire designed to measure objective and subjective burden among spousal caregivers of patients with AD. Average objective burden scores of 10 and subjective burden scores of 38 have been reported for caregivers, with subjective burden scores in excess of 42 considered "quite high" (Vitaliano et al., 1991). In this sample, only 4% of caregivers (M = 6) had subjective burden scores of 38 or greater. Caregiver sleep reports were based on a sleep questionnaire previously used with AD caregivers in an outpatient geriatric clinic (McCurry & Teri, 1995). A summary sleep disturbance score was created by summing six Likert-scale items to yield a total possible score of 24.
Data were analyzed using Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL) and SAS (SAS Institute Inc., Gary, NC). To identify variables associated with patient sleep disturbance, the variable for frequency of nighttime awakenings was dichotomized to at least once a week versus less frequent disturbance. Because this is a cross-sectional study, prevalence odds ratios (OR) were calculated, using logistic regression (Hosmer & Lemeshow, 1989). All variables with univariate p values less than .20 were candidates for the multivariate models, but only those with multivariate p values less than .05 were included. Factors associated with the CERAD anxiety scale were examined in a similar manner, using linear regression. Model fit, the scale of each variable, and the influence of outliers were assessed in all models.
A summary of participant's scores on the primary demographic and assessment measures is provided in Table 1 . As can be seen, the majority of participants were White men with moderate levels of cognitive impairment. Caregivers were largely their White female spouses. Patient scores on physical performance measures (SIP, SF-36) were comparable to values that have been reported elsewhere for older adults with chronic medical conditions, including AD (Krenz et al., 1988; Wells et al., 1989). Patients and caregivers generally scored in the non-depressed range, which accounts for the large standard deviations relative to mean depression scores observed on Table 1.
STEPWISE REGRESSION ANALYSES MODELING PATIENT ANXIETY SCALE SCORES
In contrast, anxiety symptoms were common among study patients. Between 34% to 77% of participants were reported to have exhibited each of the symptoms on the CERAD anxiety scale (Table 2). One-third (35%) of all participants were tired or lacking in energy 16 or more days in the past month. Twenty-two percent showed physical signs of anxiety or fear such as appearing nervous or startling easily (somatic anxiety), 14% complained of feeling anxious (psychic anxiety) or were physically restless, and 1 1 % were agitated or irritable. Twenty-seven percent of participants had two or more anxiety symptoms, and 5% had four or more anxiety symptoms occurring 16 or more days in the past month (range = 0 to 5 symptoms).
Twenty-nine percent of caregivers reported that the patient had awakened them at least once in the past week. Seven percent (n= 11) were taking a sedative or hypnotic, anti-anxiety, or antidepressant medication, or over-the-counter sleep aid at night to help sleep. Twenty-one percent (n = 32) were reported to consume one to two drinks of alcohol at least once a week. Among those participants taking sleep medications, mood disturbances were common. For example, 10 of 11 participants had feelings or physical symptoms of anxiety during the past month, 7 of 11 had total anxiety scale scores in the top 25th percentile for this sample, and 5 of 11 had Cornell scores consistent with moderate levels of depression.
To identify variables independently associated with patients' awakenings, stepwise logistic regression was conducted to compare participants who had awakened their caregiver in the past week (n = 45) against participants with infrequent or no awakenings (n = 108). Potential independent variables included patient demographic (age, gender, ethnicity, living with caregiver), cognitive (MMSE), functional (PSM, IADL), physical (SIP, SF-36) and behavioral characteristics (CBRSD Anxiety, RMBPC memory and disruption subscale scores, alcohol and sleeping medication use), as well as caregiver levels of depression, burden, and sleep disturbance. Patient anxiety and physical function impairments were significantly related to patient awakenings, having a prevalence OR of 2.0 (95% confidence interval [CI] = 1.4 to 2.9) for a 7-point higher CERAD anxiety scale score, and a prevalence OR of 1.6 (95% CI = 1.2 to 2.3) for a 10-point higher SIP Body Care subscale.
These results indicate that the presence of anxiety doubled the odds of patients waking their caregivers. Depression was not significant in the model, nor was any other demographic, cognitive, or behavioral variable. There were no differences in the frequency of nighttime awakening reported by caregivers who lived with their patient versus those who lived apart, nor did sleep medication use significantly contribute to model results. However, because the vast majority of participants lived together and used no medications, statistical power to detect differences was low.
When the individual anxiety -related problem behaviors were examined using univariate analyses, the individual symptoms feeling anxious, showing physical signs of anxiety, agitation, and easily irritated were significant risk factors for patient awakenings. The ORs were 1.3 (95% CI = 1., 1.0, 1.7) for feeling anxious, 1.5 (95% CI = 1.2, 1.8) for showing physical signs of anxiety, 1.5 (95% CI = 1.1, 2.0) for agitation, and 1.4 (95% CI = 1.0, 1.8) for irritability. Tired and restless were nearly significant (each ? = .06). Of these, showing physical signs of anxiety remained significant in multivariate analyses (OR 1.5; CI = 1.2, 2.0), along with the SIP Body Care subscale (OR 1.8; CI = 1.3, 2.5).
The finding that depression, a commonly associated symptom of anxiety and sleep problems, was not significant in the multivariate analyses warranted additional examination. Regression analyses were conducted to identify variables independently associated with total CBRSD anxiety scale scores. Independent variables included patient demographic (i.e., age, gender, ethnicity, living with caregiver), cognitive (MMSE), functional (PSM, IADL), physical (SIP, SF-36), and behavioral (Cornell, RMBPC memory and disruption subscale scores, alcohol and sleeping medication use) characteristics. Caregiver levels of depression, burden, and sleep disturbance were also included in the model.
Depression as measured by the Cornell scale, was most strongly associated with anxiety in this sample, accounting for 38% of the observed variance (Table 3). Higher caregiver subjective burden score, fewer physical role limitations, and more severe memory impairment on the RMBPC were also significant (p < .05). These findings confirm that depression and anxiety are highly related. Thus, the absence of depression in the multivariate model predicting patient awakenings is explained by the fact that although depression may also be a contributing factor, a higher proportion of the variance in patient nighttime awakening is caused by anxiety.
This investigation provides new information about the relationship between anxiety and nighttime awakenings in a community-residing sample of individuals with AD. Patient tiredness or loss of energy was the most frequent anxiety symptom reported, followed by somatic symptoms of anxiety (e.g., appears nervous or is easily startled), psychic symptoms of anxiety (e.g., expresses worry about being left alone), restless behaviors, and irritability or agitation. Twenty-seven percent of participants had two or more anxiety symptoms, and 5% reported four or more anxiety symptoms during at least 16 days in the past month. Anxiety symptoms were associated with higher levels of depression, impairments in physical function related to body care, memory disturbance, and caregiver burden.
The frequency of patients awakening their caregiver at night was significantly greater among patients with AD who had higher levels of anxiety and impairment in their ADLs. Patients with anxiety were two times as likely to wake up their caregiver as were patients without anxiety. Controlling for whether or not patients lived with their caregiver and for sleeping medication use did not affect the regression results, although because the vast majority of participants lived together and used no medications, statistical power to detect differences was low.
Depression, although strongly associated with total anxiety scores, was not significant in the multivariate analyses for patient nighttime awakening. Impairments in physical functioning and symptoms of anxiety also explained a greater proportion of the variance in patient rates of nighttime awakenings than did depression. These findings are similar to Teri et al. (1999), who found that although comorbid anxiety-depression occurred in more than half of a populationbased sample of patients with AD (N = 523), the behavior problems associated with this comorbidity were explained entirely by the presence of anxiety. Further work examining the relationship of anxiety and depression to sleep in AD is needed. Nevertheless, these results suggest the importance of assessing for anxiety as well as depression in future research with patients with AD.
These findings have implications for clinicians caring for patients with AD. Behavioral treatments for depression have been shown to improve sleep in AD (Teri et al., 1 997), and antidepressant medications are widely used to improve sleep and reduce agitation in these patients (Lasser & Sunderland, 1998). However, the current study suggests that although depression is a common comorbid condition of dementia (Katz, 1998; Mulsant & Ganguli, 1999; Porsteinsson, Tariot, & Schneider, 1997), treatments targeting other psychiatric or physical symptoms may be equally or more efficacious for managing nighttime disturbances in these patients.
Alessi, Yoon, Schnelle, Al-Samarrai, and Cruise (1999) were able to increase percent total sleep and duration of sleep episodes in institutionalized patients using a combination of light physical exercise and other behavioral strategies (e.g., keeping patients out of bed in the late afternoon and evening, providing quiet nighttime incontinence care). A number of studies of timed light exposure have demonstrated beneficial therapeutic effects on the sleep of patients with dementia, although most of these also have been with institutionalized participants (Campbell et al., 1995; McCurry, Reynolds, AncoliIsrael, Teri, & Vinello, 2000; Mishima, Okawa, Hozumi, & Hishikawa, 2000).
A behavioral training program including education about sleep hygiene practices and dementia care has also been shown to be effective in improving the sleep of communitydwelling dementia caregivers (McCurry, Logsdon, Vitiello, & Teri, 1998). Future research is needed to examine how factors such as physical activity, light exposure, and sleep hygiene practices interact with depression and anxiety to influence the development and treatment of sleep and nighttime behavioral disturbances in dementia.
Several study limitations should be noted. First, the study relied on caregiver reports of how frequently they were awakened by the patient the past month to identify patient sleep disturbances. Future studies would be strengthened by the inclusion of standardized sleep measures or ambulatory monitoring to assess patient and caregiver awakenings. Similarly, the CERAD anxiety scale used in this study was developed as a measure of convenience from a more general assessment scale for psychiatric disturbance in dementia. It should be noted, however, that there easts no standard for defining or measuring anxiety in a dementia population.
The items selected for this composite scale were primarily based on Diagnostic and Statistical Manual IV (DSM-IV) criteria for GAD (American Psychiatric Association, 1994). The finding that 6 of the 7 items were significant risk factors for sleep disturbance in univariate analyses and showing physical signs of anxiety remained significant in multivariate analyses strengthens the conclusion that assessment of anxiety may be important in understanding and treating sleep disturbances in patients with AD. Nevertheless, recognizing that the use of different anxiety and sleep measures might yield different results, future confirmatory studies to explore the relationship between anxiety and sleep in AD are needed.
Study results may also be confounded by the fact that many anxiety symptoms (including sleep disturbances) are non-specific and overlapping with the symptoms of other psychiatric syndromes, including depression. This symptom overlap increases the difficulty in interpreting the degree of independent association between anxiety and sleep in individuals with AD. The nature of this current sample and analysis also do not make it possible to describe any other medical, environmental, or interpersonal factors that can contribute to anxiety and sleep disturbances in individuals with dementia. Nurses providing clinical care for dementia patients should always be sensitive to the needs and circumstances of each individual person when developing their treatment care plan. Additional research with dementia patients is needed to clarify the full phenomenology of the anxiety construct and its unique contribution to dementiarelated behaviors, independent of other diagnostic classifications.
Finally, the analyses described m this article are correlational and do not permit statements about the causal direction of relationships among variables. However, even such correlational data provide new information and highlight the need for more rigorous investigation of anxiety and nighttime behavioral disturbances in AD. Future research directed at understanding the causal relationships will clearly lead to more effective treatments for patients with AD.
The current findings suggest that anxiety and nighttime awakening are highly interrelated in dementia patients. Treatments targeting both may be more efficacious than those focusing on anxiety or sleep alone.
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DESCRIPTIVE DATA FOR REDUCING DISABILITY IN PATIENTS WITH ALZHEIMER'S DISEASE AND THEIR CAREGIVERS (N = 153)
FREQUENCY OF ANXIETY SYMPTOMS FROM CERAD* BEHAVIOR RATING SCALE FOR DEMENTIA ANXIETY SUBSCALE
STEPWISE REGRESSION ANALYSES MODELING PATIENT ANXIETY SCALE SCORES